neuropsychological studies of the frontal lobes

Psychological Bulletin1984, Vol95, No. 1,3-28

Copyright I984t>y theAmerican Psychological Association, Inc.

Neuropsychological Studies of the Frontal Lobes

Donald T. StussSchools of Medicine (Neurology) and Psychology

University of Ottawa andOttawa General Hospital, Ottawa,

Ontario, Canada

D. Frank BensonDepartment of Neurology

University of California, Los Angeles,School of Medicine

This review summarizes the current state of knowledge of prefrontal lobe functionsas derived from studies and observations of adult humans following frontal lobedamage. Following an overview of the neuroanatomy and neuropathology, frontallobe activities are presented under the following headings: motor functions; sensory,perception and construction functions; attention; abnormal awareness; flexibility-perseveration; language; memory; cognition; personality; localization; and hemi-spheric activity. Six specific prefrontal functions are suggested as the principaldisorders underlying many if not all of the described manifestations.

In 1928 the American neurologist Tilneysuggested that the entire period of human evo-lutionary existence could be considered the"age of the frontal lobe." A great deal of in-direct evidence supported such a claim. Spe-cific knowledge of frontal lobe functions, how-ever, has remained relatively limited and hy-potheses concerning these functions remaincontroversial, a state reflected in the well-known description of activities of the frontallobes as a riddle (Teuber, 1964). Some authorscredited frontal association cortex with thehighest intellectual and moral functions (Hal-stead, 1947; Rylander, 1939), whereas otherswere unable to confirm exclusive roles for thiscortical area (Hebb, 1945; Mettler, 1949; Teu-ber, 1959; Weinstein & Teuber, 1957).

Several reasons can be rioted for the con-tinuing riddle, Many frontal lobe lesions pro-duce no primary neurologic deficits; therefore,possible subtypes of frontal lobe dysfunctioncannot be readily demarcated by neighbor-

This study was supported in part by Grant #NSO6209from the National Institutes of Health to Boston UniversitySchool of Medicine,-the Research Service of the VeteransAdministration,' University of Ottawa Faculty of SocialSciences Grant, the National Research Council of Canada,the Ontario Mental Health Foundation, and the AugustusS. Rose Endowment Fund. The library search assistanceof Francine Sarazin is gratefully acknowledged. BonitaPorch is thanked for the preparation of the manuscript.

Requests for reprints should be sent to Donald T. Stuss,Human Neurosciences Research Unit, RM 2166, Uni-versity of Ottawa, 451 Smyth Road, Ottawa, Ontario K1H8M5, Canada.

hood neurologic findings. Because these def-icits cannot be subclassified, the term frontallobe syndrome is used to refer to an amor-phous, varied group of deficits, resulting fromdiverse etiologies, different locations, and varirable extents of abnormalities. A second sourceof confusion stems from inappropriate as-sessment procedures, lack of adequate controlgroups, and interinvestigator variations in testprocedures. In addition, frontal lobe pathologyis often misinterpreted as a psychiatric prob-lem. When the subtlety of deficits, the widevariations of symptomatology, and lack ofclarification from neurologic, psychologic, andpsychiatric disciplines are considered together,the reason the activity of the frontal lobes re-mains a riddle becomes clear.

This review will briefly view the currentstate of knowledge of frontal lobe functions.Somewhat arbitrarily the frontal lobe activitieswill be presented as phenomenological unitswith the major focus on behavioral changesthat occur in adult humans following acquiredfrontal lobe damage. Reference to the animalliterature will be limited to corroborative ev-idence, except for the section on neuroanat-omy, where nonhuman data is the basis.

Neuroanatomical Considerations

Anatomically the frontal lobes are the mas-sive cerebral area anterior to the rolandic fis-sure and above the sylvian fissure. There aretwo roughly symmetrical lobes, each of whichcan be further divided into three main areas:

DONALD T. STUSS AND D. FRANK BENSON

dorsal-lateral, medial, and basilar-orbital. Ac-tually, the frontal lobe may be divided in anumber of ways.

First, using Brodmann area numbers, threemajor subdivisions are noted. Area 4, the pre-central gyrus, is the primary motor area, withArea 6 and the posterior part of Area 8 calledthe premotor area. Areas 44 and 45, alsoknown as Broca's area, are considered part ofthe premotor area (Jouandet & Gazzaniga,1979). Area 8 represents the frontal eye fields.The remainder of the frontal lobe, includingAreas 9, 10, 11, 12, 46, 47, 13, 14, and 15, iscalled prefrontal cortex, and can be furthersubdivided into basal-medial (9-13, 24, 32),dorsal-lateral (9, 10, 11, 12, 46, 47), mesial(9, 10, 11, 12), and orbital (10, 11, 12, 13, 14,15, 47). Functional differences between thesesections are not clear, but some postulates willbe discussed.

As a second approach, three main cytoar-chitectural divisions can be outlined in thefrontal cortex. Agranular cortex refers to themotor area (Areas 4 and 6), in which the ex-ternal pyramidal layer (III) and internal py-ramidal layer (V) are so large that they becomeone deep layer, with virtually no internal gran-ular layer (IV). In the prefrontal cortex, onthe other hand, Layer IV, the inner granularlayer, reappears producing a distinct granularcortex. Lying between the granular and agran-ular cortices is a third, transitional area calledthe dysgranular cortex—the frontal eye field.

A third anatomical definition of the frontallobe concerns thalamic-cortical connections(Akert, 1964; Goldman, 1979; Nauta, 1971).The motor cortex receives projections fromthe ventral lateral nucleus and the premotorarea from the medial ventral anterior nucleus.The prefrontal cortex is directly connected tothe dorsal medial nucleus of the thalamus andappears to be divisible into several distinctregions. Important connections also exist be-tween frontal and nonspecific thalamic nuclei(Goldman, 1979; Scheibel & Scheibel, 1967).

Territories of vascular distribution provideyet another means of subdividing the frontallobes. The dorsal-lateral convexities are pri-marily served by the middle cerebral artery,the medial frontal areas by the anterior cerebralartery. The lateral orbital surface is middlecerebral territory, whereas the medial orbitalarea is fed by the anterior cerebral.

The importance of the frontal lobes derivesfrom rich connections, both afferent and ef-ferent, with almost all other parts of the centralnervous system. Frontal connections with cor-tical sensory areas, providing information fromthe external milieu, occur either by direct cor-tical-cortical afferents or via the thalamus. Theoccipital, parietal, and temporal sensory as-sociation cortices connect to both the anteriortemporal and the inferior parietal areas; inturn, each of these has direct afferent con-nections to the frontal cortex. There is a dif-ference, however. The inferior parietal-frontalconnection is distributed over a wide, primarilydorsal-lateral area, while the temporal-frontalconnection projects both to dorsal-lateral andorbital cortex (Nauta, 1971, 1972).

Knowledge of these connections is becomingmore specific. The dorsal bank of the sulcusprincipalis on the dorsal-lateral convexity hasfour primary ipsilateral connections (Goldman& Nauta, 1977b). There are parallel contra-lateral projections, apparently allowing the twohemispheres to converse. An ipsilateral-con-tralateral projection initiates as well from theposterior-medial orbital frontal area.

The prefrontal cortex receives projectionsfrom olfactory sensation; it is thus the onlycortical area interacting with all four sensorymodalities (Nauta, 1971,1972). Two olfactory-frontal pathways have been described (Potter& Nauta, 1979).

The frontal lobes also have well-developedconnections with limbic and subcortical areasthat provide monitoring of the internal milieu(Nauta, 1971, 1972, 1973). Most of thesepathways proceed via the dorsal medial (DM)nucleus of the thalamus and are transmittedeither to the orbital-frontal cortex (medial DMcells) or to the convexity (lateral DM cells).In addition, there are some primary efferentlimbic connections that traverse directly to thecingulate gyrus. These cingulate-frontal con-nections are specific (Pandya, Van Hoesen, &Mesulam, 1981).

The connections between the brain stemand frontal lobes are partially discussed inother sections, including frontal-limbic andfrontal-thalamic connections. Luria (1973)indicates that the frontal lobes are involvedin the regulation of arousal and tone throughthe activating input to the brainstem reticularformation from the orbital and medial frontal

NEUROPSYCHOLOOICAL STUDIES OF THE FRONTAL LOBES

cortex. This reticular system is generally di-vided into two parts (Benson & Geschwind,1975)—the brainstem reticular formation,which modulates and modifies arousal (Bre-mer, 1954; Moruzzi & Magoun, 1949; Rossi& Zanchetti, 1957), and the interlocking butessentially antagonistic system, the diffusethalamic projection system (DTPS), whichcontrols phasic activity. It has been suggestedthat this frontal-brainstem reticular system(including thalamus) is an apposed but com-plementary selective gating system, providingcontrol of the most complex forms of con-scious activity (Scheibel, 1980).

Three main brainstem connections to dor-sal-lateral prefrontal and cingulate cortex,corresponding to known monoamine path-ways, have been reported (Porrino & Gold-man-Rakic, 1982). These connections are fromthe ventral midbrain, the central superior nu-cleus and caudal portion of the dorsal raphenucleus, and from the locus coeruleus andproximal medial parabrachial nucleus. Ap-proximately similar projections to the orbitalprefrontal cortex were also noted. The pre-frontal cortex is closely linked with the brain-stem areas of sleep and arousal.

Frontal-tectal connections are derived notonly from frontal eye field zones (Astruc, 1971;Kuypers & Laurence, 1967), but also from themiddle third of the dorsal bank of the principalsulcus (Goldman & Nauta, 1976). In addition,there are connecting pathways between theprincipal sulcus and the nearby frontal eyefields.

Knowledge of prefrontal-striatal pathwaysindicates that the frontal cortex projects notonly to the head of the caudate (projectionsare maximum here), but also to the entirecaudate (Goldman & Nauta, 1977a). It appearsthat cortical zones that are connected witheach other also have projections, at least inpart, to the same area in the caudate (Yetarian& Van Hoesen, 1978).

At best, this brief synopsis of the anatomyof the frontal lobe and its connections suggestsa possible cognitive globe on which ourknowledge of frontal lobe functions may bemapped. Although cytoarchitectural specificityappears lacking, some degree of functional def-inition to the different frontal regions and therelated frontal systems may be inferred fromtheir anatomical connections.

Neuropathology

The wide variety of etiologies that can pro-duce frontal lobe dysfunction constitutes amajor element in the riddle of the frontal lobes.Only a brief synopsis of the many recognizedproblems can be described here and these willbe subdivided, somewhat artificially, into thefollowing three groups for ease of discussion:primary neurologic disorder, frontal braintrauma, and frontal psychosurgery.

The first of these subgroupings is the mostdifficult to discuss because it contains a myriadof widely different disorders. Some of the dis-orders are widespread, affecting much of thebrain, but show some degree of predilectionfor frontal structures (e.g., general paresis ofthe insane); others involve subcortical struc-tures primarily, affecting frontal function onlysecondarily. Nonetheless, they are often listedamong frontal disorders (e.g., Huntington'sdisease, multiple sclerosis). Cerebral vasculardisease is only rarely a purely frontal phe-nomenon. With the exception of the relativelyuncommon obstruction of the anterior cere-bral artery, most strokes that involve the fron-tal lobe also cause damage to deep structures,to more posterior structures, or both. Evenbrain tumors, which can arise totally withinthe frontal lobe, almost always produce distanteffects (pressure phenomena, vascular insuf-ficiency) before being recognized as a frontaldisorder. Primary neuropathological involve-ment restricted to the frontal lobes is rare;most consequent behavior is contaminated bydistant effects. Nonetheless, most of the ac-cepted descriptions of frontal phenomenologyderive from such clinical sources. In particular,much of the masterful work on the frontallobes produced by A. R. Luria over the years(1965, 1966, 1969, 1973) was derived fromhis evaluations of patients with frontal lobetumor and, despite the recognized limitations,represents some of the best clinical-patholog-ical observations currently available.

Trauma to the brain deserves separate con-sideration. Whereas closed head trauma tendsto have widespread cerebral consequences,some open head injuries, particularly thoseproduced by high velocity missiles or shrapnel,can produce relatively localized frontal dam-age. Because of the large size and compara-tively great distance from essential, more cen-

DONALD T. STUSS AND D. FRANK BENSON

trally located brain structures, significantfrontal damage is often compatible with life,leaving the person behaviorally disturbed butotherwise relatively intact. The literature con-tains many excellent descriptions of such in-dividuals (Faust, 1960; Feuchtwanger, 1923;Kleist, 1934a) and a great deal of the knowl-edge of frontal lobe psychiatric symptom-atology stems from this source (Lishman,1966). It must be recognized, however, thatbrain injury is never totally focal, and the widevariety of both neighborhood and distantsymptomatology contaminating these studiesrepresents another source of confusion in theclinical descriptions of frontal phenomenology.

Psychosurgery can be considered the thirdmajor etiologic source of data on frontal func-tion. In the late 1940s and early 1950s many(probably over 100,000) prefrontal destructiveprocedures were performed. Most were bilat-eral and, technically, were fairly exact. As such,prefrontal leukotomy could be expected toyield considerable information concerning be-havior following focal frontal lobe damage; theoutcome, however, has been disappointing.Several obvious factors can be cited as thesource of this problem. For one, most indi-viduals who underwent prefrontal psychosur-gery were behaviorally abnormal (schizo-phrenic, phobic, depressed, violent); presurg-ical evaluation was difficult (and rarely done),and postoperative findings were often contam-inated by the premorbid behavioral problems.In addition, most of the diagnostic proceduresperformed in those years were limited to psy-chiatric outcome; little attempt was made tostudy alteration in any behavior except thepremorbid problem. The follow-up after psy-chosurgery was characteristically short (averageduration less than 6 weeks but often only over-night). The few psychologic studies of frontalfunction in these subjects concentrated on in-tellectual competency and failed to demon-strate other aspects of frontal damage (Green-blatt & Solomon, 1958/1966; McKenzie &Kaczanowski, 1964; Valenstein, 1977). Eventhese studies were limited to short postoper-ative duration. Very few long-term studies offrontal lobe function have been made in pa-tients who had undergone psychosurgery, andmost of these have been limited both in termsof the evaluation performed and in the numberof patients examined. Recently, however, a se-

ries of reports have been published of neu-rological, neuroradiological, and a compre-hensive battery of neuropsychological tests ad-ministered to a small number of individualswho had undergone prefrontal leukotomy 25to 30 years earlier (Benson et al, 1981; Naeser,Levine, Benson, Stuss, & Weir, 1981; Stuss,Kaplan, Benson, Weir, Naeser, & Levine,1981).

Motor Functions

Of all frontal lobe functions, the control ofmotor responses is the most obvious. It haslong been recognized that the frontal portionof the brain subsumed motor actions, in con-trast to the sensory activities of the parietal,temporal, and occipital lobes (Meynert, 1872).Bianchi (1895) posited that the frontal lobenot only initiated the "final common pathway"for brain responses but served to integrate in-formation from other parts of the brain andthus to modulate the final response. The re-sulting frontal motor activities are complexand must be subdivided for study. Two of themost significant portions of the frontal lobe,the pre-central and the pre-motor areas, havebeen well studied. Their motor functions aredescribed in all neuroanatomy texts and neednot be detailed here. The remaining motoractivities, those stemming from prefrontal areaparticipation, are far more complex and, todate, defy specific descriptions. It is from thissystem that sophisticated motor responses toa variety of high-level stimuli are coordinated.

In global terms, the description of motorfunction after prefrontal damage from anyetiology has been crudely separated into twotypes, reflecting Kleist's (1934a) localizationdifferences. The hypokinetic patient is slowand apathetic, responds in an automatonlikemanner, and demonstrates little initiative orspontaneity (Blumer & Benson, 1975; Gold-stein, 1944; Kleist, 1934a; Lishman, 1978;Walch, 1956). Lesion localization tends to bemaximal in the prefrontal convexity, but this"apathetico-akinetico-abulic" syndrome ismost typical of massive frontal lobe damage(Luria, 1973). The second type, with majorpathology involving the orbital area, showshyperkinesis, restlessness, and impulsivity(Feuchtwanger, 1923; Kleist, 1934a). Such pa-tients may explode into action, respond ap-

NEUROPSYCHOLOGICAL STUDIES OF THE FRONTAL LOBES

propriately, and then relapse into a constantmultidirected restlessness. Although both'typeshave been described frequently, the pathologyis seldom so well localized as to provide pureexamples.

Examination of patients using differentmotor tasks led Luria (1965,1973) to postulateat least two major types of motor disorderfollowing frontal lobe pathology. The first,caused by lesions in pre-motor zones, resultsin a problem in the execution of dextrousmovements such as rhythm tapping or drawinga series of symbols requiring an alteration ofdesign. If the lesion also extended deeper toinvolve the basal ganglia, compulsive repeti-tion of an initiated action resulted. Thus, ifthe patient is asked to copy a circle, the move-ment is completed correctly but cannot beinhibited, and a series of repetitive circularmovements ensue. This response suggests in-tact motor programs allowing the patient tocarry out the specified action; damage to thecontrol aspect of motor behavior, however, re-sults in the inability to cease the behavior.

The second major type of frontal motor dis-order is more frequently associated with mas-sive prefrontal pathology in which the motorprogram itself is disturbed so that the schemeof action is replaced by an inert stereotype.Luria devised many tasks that demonstratedthis latter type of frontal motor control defect.For example, if such a patient is asked to drawa circle, the movement is completed correctlywithout superfluous lines. If then requested todraw a cross, the patient draws another circle.Similarly, when asked to do the opposite ofthe examiner or to perform a conflicting actionthe patient echoes the examiner. For instance,if told to tap twice when the examiner tapsonce and vice versa, these patients soon doexactly what the examiner is doing, eventhough they can still correctly verbalize therequirements of the task. Imitative action isnot lost and, in fact, is so strong that it over-comes the well-understood verbal directions.In contrast, patients with promoter pathologyare more likely to tap perseveratively, failingeven to imitate correctly. A third variation isa go/no-go task requiring the patient to re-spond to one signal but not to a second signal.Inability to inhibit responses to the no-go sig-nal is frequently seen following prefrontal pa-thology.

Another major disturbance, the participa-tion of prefrontal areas in praxis abnormality,is also controversial. Some exclude the frontallobes from any involvement in ideomotor,ideational, constructional, and dressingapraxia (Hecaen, 1969; Hecaen & Assal,1970). Others state that constructional anddressing disturbances are not truly apracticphenomena (Benson & Geschwind, 1971).Glossokinetic (melokinetic) apraxia wasthought to involve Areas 4 and/or 6 exclusively(Fulton, 1937; Kleist, 1934b; Nielsen, 1951)and may be more of a motor deficit than atrue apraxia (Hecaen & Albert, 1978). As such,glossokinetic apraxia may be better described!as Luria's premotor syndrome.

The frontal lobes do participate in somepractic functions, however. Bucco-linguo-facialapraxia has often been described with lesionsinvolving the left frontal motor association(i.e., premotor) cortex, although supramar-ginal gyrus and unilateral right hemispherelesions have also been reported (Geschwind,1965; Goldstein, 1909;Hartmann, 1907; Rose,1908). Unilateral limb apraxia has been re-ported after frontal' lobe lesions, and two typescan be differentiated. Sympathetic or ideo-motor apraxia (Geschwind, 1967; Liepmann,1905), usually associated with Broca aphasia,apparently results from a lesion destroying theorigin of motor fibers in the dominant hemi-sphere that cross the corpus callosum to thehomologous nondominant motor area. An-other type, unilateral, kinetic apraxia of themagnetic type (Denny-Brown, ,1958) is saidto occur with pathology in superior or medialfrontal cortex of either hemisphere, with orwithout involvement of the corpus callosum.

There is a need for much further researchin the motor difficulties that follow frontal lobedamage. Drewe (1975), for example, suggestedthat the go/no-go task is not unitary in natureand that lesions in different frontal lobe regionscould subserve different aspects. Motor deficitsof the kinds described above could not be elic-ited in patients with large prefrontal leukotomylesions (Benson & Stuss, 1982). Future re-search will require precise localization of le-sion, sophisticated motor testing, and attentionto compensatory capabilities.

In summary, the motor functions of thefrontal lobe are manifold and current knowl-edge of any except the most primary functions

8 DONALD T. STUSS AND D. FRANK BENSON

remains vague. There is reason to separatefrontal motor activities into categories with atleast some relation to the sophistication of theaction and to correlate this separation withdifferent areas of frontal lobe. At this juncture,however, even the categorization of frontalmotor activity must remain suspect, and fewfirm conclusions can be made.

Sensory, Perception, andConstruction Functions

Neurologically, the frontal lobes are gen-erally considered to be motor areas, withoutprimary sensory functions. Accumulating ev-idence from clinical observations and psycho-logical research, however, implicates the frontallobes in a number of sensory-perceptual func-tions. One clear example is the clinical ob-servation that unilateral sensory neglect, char-acterized by an inability to attend to onesensory field (hemi-inattention) can be dem-onstrated opposite the side of some frontallobe lesions (Damasio, Damasio, & Chui,1980). This may vary in intensity from a full-blown hemisensory defect to a minimal sen-sory deficit elicited only as unilateral extinctionto double simultaneous stimulation testing.

There is also strong experimental evidencethat frontal lobes and/or their connections arerelevant to the unilateral inattention phenom-enon. Experimental lesions placed in the fron-tal lobes of animals can produce similar sen-sory abnormalities (Bianchi, 1895; Kennard,1939; Welch & Stuteville, 1958). Unilateralablation of Area 8, the frontal eye field, canproduce a temporary contralateral visual fieldneglect (Doty, 1973) despite intact visual fieldperimeters (Jenkner & Kutschera, 1965). Aseries of studies and observations by Heilmanand colleagues (Heilman & Valenstein, 1972;Watson & Heilman, 1979; Watson, Heilman,Cauthen, & King, 1973; Watson, Heilman,Miller, & King, 1974) suggests that the atten-tion-arousal deficit can be caused by lesionsin any portion of a sizeable frontal-limbic-reticular loop. Their studies suggest that sen-sory inattention may be caused by lesions inmany different but interrelated areas of thecentral nervous system, including the frontalcortex. Unilateral inattention will be discussedfurther in a later section, but this work clearly

shows that frontal and/or frontal system pa-thology can produce an apparent sensory losson the contralateral side.

Supportive evidence for the involvement ofthe frontal lobes in sensory-perceptual func-tions has also been developed from psycho-logical research. For instance, deficits in visualsearch are commonly observed after frontallobe damage (Luria, 1973). With bilateralfrontal damage, inertia of gaze is so great thatvisual attention can be focused on only oneaspect of the visual field. With lesser degreesof pathology the deficit is better described asdisorganized visual search and can be dem-onstrated by monitoring eye movements dur-ing a patient's examination of a thematic pic-ture (Luria, Karpov, & Yarbuss, 1966). Whenasked to tell the meaning of a thematic picture,frontal damaged patients would give an answerbased on their first visual fixation with littleattempt to monitor additionally with a fullexamination of the picture. Eye movementmeasurements verified this observation, re-vealing that whereas the eye movements ofnormal subjects were directed and organized,those of frontal lobe patients were haphazard.

Teuber, Battersby, and Bender (1949) alsoexamined visual search in patients with focalfrontal lobe damage. They used a task withan array of 48 patterns scattered randomlyover a screen with a duplicate of one of thepatterns projected in the center of the field.The subject was requested to actively searchfor the match. Frontal lobe patients had pro-longed search times with greatest difficulty inthe visual field contralateral to the unilaterallesion, independent of any gaze paresis. Theinvestigators suggested that this could resultfrom disinhibition of occipital fixation mech-anisms following loss of the (inhibitory) actionof the frontal eye fields. Patients with lesionsinvading the frontal eye fields were also im-paired in inhibiting initial saccades at a po-tentially distracting stimulus (Guitton, Buch-tel, & Douglas, 1982). Cogan (1966) stressedthe importance of the frontal lobes in Balint'ssyndrome, citing frontal influence on volun-tary occular movements (to verbal command)as well as an inhibitory effect on occipital cen-ters. A similar explanation has been suggestedin a recently published case of Balint's syn-drome (paresis of gaze on volition, optic ataxia,

NEUROPSYCHOLOGICAL STUDIES OF THE FRONTAL LOBES

and decreased visual attention) with both bi-frontal and bilateral occipital pathology(Hausser, Robert, & Giard, 1980).

The importance of the frontal lobes in sen-sory-perceptual tasks was given considerableimpetus by the research of Teuber and col-leagues (Teuber, 1964). Despite nonimpairedperformance on tests of general intelligence,attention, and memory, specific frontal lobedeficits were demonstrated on sensory-per-ceptual tasks. Thus, using variations of theAubert task (tilting chair test), Teuber andMishkin (1954) did four experiments thatclearly disassociated frontal from parietal pa-tients. Patients with frontal lobe damage weremost impaired when their body was tiltedwhile they attempted to set a line straight.Parietal-damaged patients were most impairedwhen the line was tilted against a conflictingvisual background. In general, frontal patientsmade more overcompensatory mistakes,whereas posterior patients and normals hadless overcompensation, possibly because theirintact frontal lobes could monitor and correctsensory-motor imbalances.

Using the Necker Cube Test as an extremecase of reversible figures, Cohen (1959) andTeuber (1964) independently demonstratedthat frontal lobe lesions in either hemispherecaused a significant decrease in a number ofreversals achieved in comparison to otherbrain-damaged groups and normal subjects.Dissociation between subject groups was alsoachieved on a perceptual orientation task.Right frontal-damaged patients were morevulnerable on personal orientation tasks butparietal lobe patients were inferior at tasksinvolving orientation in their surroundings(extrapersonal space).

Other visual-perceptual tasks have beenshown to be sensitive to frontal lobe pathology.Although all patient groups performed poorlyon the picture arrangement subtest of theWechsler Adult Intelligence Scale (WAIS),frontal-damaged patients (especially right)tended to leave all or many of the pictures inthe presented order, compensating with looselyconnected explanations (McFie & Thompson,1972; Walsh, 1978). On a measure of visu-alized relative movement, Albert and Hecaen(1971) demonstrated that although more def-icits occurred in the right hemisphere damaged

patients, the greatest degree of error occurredwith frontal lesions, and these could involveeither hemisphere. The importance of thefrontal lobes for this visual sensory task wasimpressive. The authors suggested that theperception of position appears to be a righthemisphere function but that the perceptionof relative movement apparently demandsfrontal lobe activity.

The role of the frontal lobes in construc-tional disturbances has been controversial.Many authors have excluded the frontal lobesas the cause of constructional apraxia (Hecaen,1969; Hecaen & Assal, 1970). Benton (1967)and Benson and Barton (1970), however, dem-onstrated that lesions in either hemisphere ofthe frontal lobe could result in constructionaldisturbance. Luria and Tsvetkova (1964) pro-posed that construction disturbances representa disorder in one of the specific frontal lobefunctions of intention, programming, regu-lation, or verification. Lhermitte, Derouesne,and Signoret (1972) demonstrated this in ablock design and complex figure movementexperiment. If the frontal-damaged patientswere presented the model for the block designwith each block outlined, or if they were taughtto copy the complex figure in a structured,sequential fashion, their performance im-proved, suggesting that the deficit was pri-marily one of planning.

This short outline of sensory-perceptual-constructive functions of the frontal lobe sug-gests disturbances on a continuum from morebasic to higher perceptual levels. As the taskinvolves greater degrees of direction, organi-zation, monitoring, and correction, it is morelikely to suffer if there is frontal lobe damage.Whether this is the entire explanation, however,remains to be determined.

AttentionDisturbance of attention is a common ob-

servation after frontal lobe damage. "From thefirst examination of the (frontal lobe) patient,the disorder of attention is noticeable: it isnecessary to repeat questions and orders sev-eral times to obtain a response" (Hecaen &Albert, 1975, p. 139). Development of thisobservation evolves from research on animalswith frontal lobe pathology performing tasksthat require delayed responses. Deficits were


first considered an impairment of short-termmemory (Jacobsen, 1935). Subsequent studies,however, implicated a basic impairment in di-rected attention; for example, placing monkeysin the dark to eliminate distracting stimuliproduced improved performance (Isaac & DeVito, 1958; Malmo, 1942). Several conceptshave been postulated to explain the attentiondeficits: hyperactivity (Orbach & Fischer, 1959;Richter & Hines, 1938); hyper-reactivity (Buf-fery, 1967; Ruch & Shenkin, 1943); and a def-icit in habituation (Grueninger & Pribram,1969; Kimble, Bagshaw, & Pribram, 1965). Avariation proposed that hyperactivity wasreally a disorder of cortical inhibition (Ko-norski, 1967).

Many observations of attentional deficitshave been made in humans suffering frontallobe damage. Frontal tumors classically resultin confusion, disordered arousal and alertness,and impairment of attention (along with otherdeficits) (Hecaen, 1964). Frontal trauma mayproduce similar results (Goldstein, 1936,1944), as can frontal lobectomy (Angelergues,Hecaen, & Ajuriaguerra, 1956; Rylander,1939). Most of these clinical observations havebeen based on deficient responses to testingor demonstration of easy distractability. Theconcept of attention as a higher order phe-nomenon deserves consideration, also. Atten-tion has been described as the adoption ofspecific cognitive strategies in response tostimulus demand (Moscovitch, 1979). By thisextended definition, many of the frontal def-icits described by Luria (1973) can be consid-ered deficits in attention.

Some human attention disorders have beencategorized as specific clinical entities. Theyare usually described on two levels: arousaland attending. Arousal reflects two factors:first, the ability to be awakened and to main-tain wakefulness; second, the ability to followstimuli or commands. Another level, attention,signifies the ability of an alert individual todirect effort and concentration for specific pe-riods of time to specific tasks. Brain diseasemay lead to varying degrees of altered arousaland attention (Plum & Posner, 1980). Oneform is a clouding of consciousness with im-paired alertness as the major defect. Such apatient cannot think quickly and is easily dis-tracted, even though oriented. Another statehas been called confusion. In this state, the

patient is alert and may be able to follow com-mands, yet is bewildered, distractible, and of-ten poorly oriented. With continued decreaseof the level of consciousness, a state of stuporor coma is reached in which the patient hasno meaningful interaction with the environ-ment.

The clinical state that most clearly repre-sents a primary disorder of attention or arousalis akinetic mutism in which there is an intactsleep-wake cycle but little measurable cog-nitive function. In this state no gross alterationof sensory-motor mechanisms exist, but thepatient lies inert and speechless (Bricolo, Tur-azzi, & Feriotti, 1980; Segarra, 1970). Twovarieties of akinetic mutism have been pro-posed, based on lesion location (Benson &Geschwind, 1975; Plum & Posner, 1980). Onetype has the appearance of somnolence; thepatient is immobile with eyes closed. The re-sponsible lesion is classically described in thelow neuro axis, primarily in the mesence-phalic-diencephalic area. In the second type,coma vigil (Benson & Geschwind, 1975), thepatient is immobile but the eyes freely followvisual stimuli, suggesting some level of vigi-lance. The lesion for coma vigil involves theposteromedial-inferior frontal areas and/or thehypothalamus. The pathology underlyingcoma vigil, although usually accepted as beingmost severe in the frontal area, almost certainlyinvolves other cortical areas, also (Plum &Posner, 1980).

The disorders of attention produced bypathological involvement of the brainstem-frontal system can be conceptualized as ex-isting on three levels: the reticular activatingsystem providing tonic levels of arousal andalertness, the diffuse thalamic projection sys-tem correlated with phasic levels of alertness,and the frontal-thalamic gating system re-sponsible for selected and directed attention.Based on neuroanatomical and clinical cor-relations, this tripartite division provides aconceptual aid for understanding the functioncalled attention. The brainstem-frontal systemcan be viewed as a unified and integrated com-plex with pathology in the brainstem reticularactivating system influencing the tonic statesof alertness (Benson & Geschwind, 1975). Se-vere pathology results in coma or somnolentakinetic mutism. A lesser degree may show"drifting attention" if phasic alertness is intact.

NEUROPSYCHOLOGICAL STUDIES OF THE FRONTAL LOBES 11

The patient will respond to a stimulus butattention rapidly drifts back to "a somnolentstate. Such patients are described as obtundedor stuporous (Plum & Posner, 1980).

A second type of attention disorder, wan-dering attention, is the converse of drifting.The patient appears fully alert and cooperative,indicating that the tonic alertness is intact, butthe phasic component is deficient in that thepatient is easily distracted by external stimuli.The alert attention wanders. The latter prob-lem can be conceived as a deficiency of thediffuse thalamic projection system. Finally, inthe section on neuroanatomy, a thalamic gat-ing system was described that enabled con-scious, directed attentive behavior. This gatingsystem appears to be under the influence ofascending fibers of the reticular activating sys-tem and descending impulses from the frontalcortex, so that afferent and efferent infor-mation can be integrated, interpreted, and usedto control sensory pathways. Pathology in thissystem would result in disorders of more com-plex behaviors requiring planning, selection ofbehavior, and monitoring of performance.

Although the concepts above are useful forunderstanding the neuroanatomical-behav-ioral correlates of attention, limitations shouldbe recognized. For example, little has beensaid of the reticular activating system-limbiccombination that involves the dorsomedial-orbital frontal areas. This interaction may haveconsiderable importance in vegetative and af-fective attentional interplay (Nauta, 1971).

In addition, negative results on measures ofattention following localized frontal braindamage deserve notice. Both Feuchtwaiiger(1923) and Teuber (1964), studying patientswith frontal gunshot wounds, could not findspecific attentional changes. In two more re-cent, studies, patients with massive bifrontalpathology were not impaired in digit span per-formance (Benson, Gardner, & Meadows,1976; Stuss, Alexander, Lieberman, & Levine,1978). Negative findings have also been dem-onstrated following prefrontal leukotomy. Ina long-term follow-up of neuropsychologicalfunction following prefrontal leukotomy(Benson et al, 1981; Stuss, Benson, Kaplan,Weir, & Delia Malva, 1981), three groups ofleukotomized schizophrenics, divided accord-ing to recovery status, were compared with anonleukotomized schizophrenic group and a

normal control group. A series of attentiontests was administered to probe sustainedmental activity, inhibition of interfering stim-uli, and tracking (Digit Span, Digit Symbol,Knox cube, Stroop test, Trail Making A andB, and Serial Sevens). The only significant cor-relation obtained was with active psychosis.Many subjects with large frontal lobe lesions(as demonstrated by CT scan) performed aswell as or better than the normal control sub-jects.

Several reasons can be offered for the neg-ative results, including questionable test va-lidity and the effects of the rigidly structuredtesting situation. Also, schizophrenia itself mayimpair attention. The frontal leukotomy mayhave created a double negative (decreasing theschizophrenic effect of decreasing attention)resulting in the intact performance. Regardlessof theoretical conjectures, the results of thistype of testing demonstrate that frontal lobelesions per se do not necessarily produce im-paired attention and that sizeable bifrontal le-sions may be present in a patient who performsnormally on a battery of standard attentiontests.

Syndromes of Abnormal Awareness

Among the most confusing problems inneurology and psychiatry are abnormalities inawareness, involving either the body or theenvironment. The separate disorders ofawareness appear heterogeneous and includesuch apparently diverse entities as confabu-lation, neglect, anosognosia, reduplicativeparamnesia, and the Capgras syndrome. Thesesymptoms remain mysterious and, predictably,a psychogenic causation has been suggestedfor each, often as an "unusual psychiatric syn-drome" (Freedman & Kaplan, 1975). As withso many mysterious entities, frontal lobe pa-thology has also been suggested in some ofthese disorders, and in actuality, there is someevidence to support this suggestion. On thisbasis, a few disorders of awareness will be de-scribed and discussed.

One common disturbance of awareness isapathy, or lack of concern. This has alreadybeen discussed among the motor disturbancesbut apathy is present to some degree in..allsyndromes of disturbed awareness and eitherrepresents an important etiologic factor or


stems from the same underlying disorder asmany of these syndromes.

Abnormal awareness df body appears to bethe most common of these disorders and isalso the most thoroughly discussed. Unfor-tunately, the discussion has not cleared themystery. Complex categorizations of disor-dered body awareness have been described(e.g., Critchley, 1953, suggested nine, Benson& Geschwind, 1975, outlined four). A rela-tionship between these disturbances, at leastto some degree hierarchical, has been suggestedand implies a common disturbance. This isan unsubstantiated assumption.

The basic disturbance of body awareness isunilateral inattention, often called neglect.This is a common neurologic finding best ex-emplified as a tendency not to report stimulito one side on double simultaneous stimula-tion, even though the patient accurately reportsall unilaterally presented stimuli. Frontal lobedamage that produced unilateral neglect hasbeen clearly described (Bianchi, 1895; Da-masio et al., 1980; Heilman & Valenstein,1972; Kennard, 1939). Welch and Stuteville(1958) demonstrated inattention to all sensorystimuli on one side of the body following le-sioning of the opposite arcuate sulcus of thefrontal lobe in monkeys. More recently, Heil-man and associates (Heilman, 1979; Watsonetal., 1973; 1974) have demonstrated a similarunilateral inattention with pathology in otherareas including the mesencephalic reticularactivating system and the cingulate cortex.They posit a reticulo-limbic-frontal circuitfor attention and imply that pathology any-where in this circuit decreases attention to theopposite side.

Denny-Brown and Banker (1954) proposeda different explanation of unilateral inattentionunder the title of amorphosynthesis. Theyposited a unilateral decrease in sensory input,unbalancing a previously finely-tuned percep-tual balance between the two hemispheres;unilateral sensory system pathology would al-low similar degrees of stimulation to be un-equal in their cortical effect. Both the Denny-Brown and the Heilman explanations appearreasonable, and it appears plausible that eitheror both may be correct in explaining a giveninstance of unilateral neglect. Thus there maybe qualitatively different types of unilateral

inattention based on different areas of ana-tomical malfunction.

A further, more severe, step in the suggestedhierarchy of inattention is a state called un-awareness. Most often this describes patientswho are unaware of their paralysis. They agreeif told that they cannot move a limb but con-tinue to act as though the limb were intact.Not only is there a unilateral neglect but suchpatients appear unable to maintain the infor-mation that they have a problem. Patients withthis more advanced degree of unawareness al-most always show a notable degree of apathy.

Closely associated with unawareness butsomewhat distinct and considerably more dis-abling is a state of unconcern. In this situationthe patient will also admit the evidence of dis-ability but shows lack of interest to the levelof disdain. While not denying the disability,the patient's actions and remarks suggest thatthe problem is of no importance. Again, apa-thy is almost invariably a striking finding.

The ultimate stage in this hierarchy is thetotal denial of an illness; this has been calledanosognosia and most commonly describes apatient who totally denies the presence of anobvious hemiplegia. Similar denial can be seen,however, with blindness (Anton's syndrome),amputation, or purely neurobehavioral phe-nomena such as amnesia, aphasia, and so on.It has been suspected that active denial of anobvious disability demands strong psychic ac-tivity (suppression of an unhappy fact) and,on this basis, it is suggested that the denial ofillness is motivated (Weinstein & Kahn, 1955).There is strong reason to doubt that anosog-nosia is entirely (or even partially) psycho-genically based, however. All patients with thisdisorder have evidence of significant organicbrain disorder, and the disorder almost alwaysappears in patients with bilaterally abnormalelectroencephalograms (EEGs; Weinstein &Kahn, 1955).

There is some evidence to suggest that fron-tal lobe abnormality may play a role in thesyndromes of abnormal awareness of the bodydescribed above. This is not firm, however,and will be discussed after several additionalsyndromes are presented.

A well-known syndrome that can be classedwith the abnormalities of awareness is con-fabulation. Confabulation is defined as the


presentation of incorrect, sometimes bizarre,information to a standard question. Confab-ulation is most often noted in the presence ofmemory disturbance (amnesia), but the bizarreresponses presented again suggest a psycho-genie motivation. Although confabulation haslong been recognized, only recently have for-mal studies of confabulation been performed.In one (Mercer, Wapner, Gardner, & Benson,1977), a series of patients with amnesia werecarefully studied for confabulation, degree ofamnesia, suggestibility, and ability to self-cor-rect. The degree of confabulation did not cor-relate with either the severity of the memorydisturbance or suggestibility but was closelyrelated to the lack of ability to self-correct.This inability to self-correct suggested an ab-normality of awareness. In another study ofconfabulation, 5 patients with severe, fantastic,and spontaneous confabulations were studiedboth psychologically and anatomically (Stusset al., 1978). These patients differed from mostpatients with confabulation by their wildlyfantastic responses and the fact that the con-fabulation was presented spontaneously ratherthan in response to prompting from the ex-aminer. The anatomical study in each case ofextraordinary confabulation demonstrated se-vere bifrontal structural pathology. These twostudies together suggest that the bifrontal dis-turbance present in the spontaneous confab-ulation syndrome may also be present in themilder forms of confabulation where structuralpathology is not present. The association ofdifferent degrees of confabulation with differ-ent levels of severity of impairment of the sameunderlying disorder appears to have been con-firmed (Kapur & Coughlan, 1980; Shapiro,Alexander, Gardner, & Mercer, 1981). Thissuggests that the decreased concern (self-cor-rection) in both types of confabulation rep-resents a disorder of awareness, a frontal mal-function.

Two disorders that may be related to con-fabulation, reduplicative paramnesia and theCapgras syndrome, were also studied clinically.Both disorders feature reduplication. Redu-plicative paramnesia has traditionally referredto reduplication of place; the patient knowsthe name of the hospital but places it in adistant locale (usually the patient's hometown). In the Capgras syndrome the redupli-

cation concerns persons, usually close relativessuch as wife, parents, or children. These in-dividuals are said to be imposters who look,talk and act like the real family members butthe patient is convinced that they are not thetrue family members. In recently reportedstudies on these two syndromes (Alexander,Stuss, & Benson, 1979; Benson et al., 1976),severe bifrontal structural pathology was pres-ent in each case. There was pathology in otherportions of the brain that was different in thetwo syndromes but all patients showing thistendency for reduplication had significant bi-frontal pathology. Again, a disorder of aware-ness is the prominent feature.

From this short review of the clinical andpsychological features of abnormal awarenessit can be suggested that many syndromes, in-cluding confabulation, reduplicative param-nesia, the Capgras syndrome, and some of thedisorders of body awareness such as unaware-ness, unconcern, and anosognosia indicatesignificant frontal lobe malfunction. Even themildest degree of unilateral inattention (ne-glect) may be indicative of frontal pathology.Although there is a consistency of frontal in-volvement in the syndromes of disorderedawareness, the evidence supporting the role ofthe frontal lobe remains circumstantial. Ob-viously, much more work must be performedto understand these syndromes, and it is prob-able that the role of the frontal lobe abnor-mality will only represent part of the problem.Nonetheless, the clinical studies strongly sug-gest that disturbances of awareness can indicatefrontal malfunction.

Flexibility-Perseveration

Perseveration, defined as an abnormal rep-etition of a specific behavior, is a common signof frontal lobe pathology (Halstead, 1947; Lu-ria, 1973; Luria, Pribram, & Homskaya, 1964;Nichols & Hunt, 1940). Perseverative behaviorhas been reported in diverse tasks includingmotor acts, verbalizations, sorting tests, draw-ings, writing, and tracking tests. So pervasiveis this phenomenon following frontal lobedamage that Denny-Brown, in a review of Lu-ria's works, considered that perseveration mayhave been of sufficient severity to have beenresponsible for much of the reported impair-ment (reported in Hecaen & Albert, 1978).


Two facts are important. First, despite pop-ular belief, perseveration and inflexibility can-not be considered exclusive hallmarks of thefrontal lobe (Critchley, 1953; Hecaen & Albert,1975). These symptoms may reflect the sizeof the lesion rather than the location (Good-glass & Kaplan, 1979). In addition, Luria(1973) notes that elementary motor persev-eration, the inability to inhibit a movementonce begun, occurs primarily in patients whosepremotor lesion extends sufficiently deep toinvolve the basal ganglia, suggesting that atleast this one type of perseveration requiresspecific frontal-subcortical damage.

Secondly, it appears that the term persev-eration may be too global and that more spe-cific analyses are required. The uninhibitedmotor response of a patient with frontal-basalganglia involvement may be qualitatively dif-ferent from the inability of another frontallobe patient to overcome a previously estab-lished response pattern on the Wisconsin CardSorting Test (Milner, 1964). Also, the qualitiesof the perseverated act may be controlled byenvironmental-reward contingencies. Pribram,Ahumada, Hartog, and Ross (1964) suggestedthat when a reward situation was constant forthe duration of a problem and then changedto an equally consistent reinforcement pattern(similar in many ways to the Wisconsin CardSorting Test), frontally lesioned monkeys per-severated the response that had been successfulin the immediately preceding condition. If,however, the reward situation varied from trialto trial within the condition, the monkeys re-sponded with increased variability. This ex-tended random search behavior itself seemedto become a perseverative tendency. In thismanner the task itself affected the presence(and possibly the type) of perseveration.

Perseveration occurs commonly in patientsfollowing frontal damage, but it can also beseen in patients without any frontal damageand is not present in all frontal-damaged pa-tients. Whether perseveration indicates size oflesion, correlation of frontal damage with basalganglia damage, a special environment/rewardcorrelation, or some mixture of these is cur-rently unclear. That inflexibility and persev-eration are important findings in many in-dividuals with frontally determined behaviorproblems is clear, however, and these findingspervade many of the other frontal signs.

Language

The occurrence of language defects withfrontal pathology has been recognized sincethe revolutionary demonstrations of Broca(1861, 1865), and like so much of the field,frontal communication disorders have been asource of controversy. Marie (1906) challengedthe notion of language in the frontal area, sug-gesting instead that anarthria, a speech defect,occurred following damage there. Althoughnever totally accepted, his suggestion has onlyrecently been disproved, and there remainsmore mystery than accepted fact in the speechand language functions of the frontal lobes.For discussion of frontal language activities,some long accepted but unproved conceptsmust be used. Most investigators accept thelanguage dominance of the left frontal lobeand, for convenience, the comparatively well-accepted terms of classic aphasiology will beused for this discussion. In this system Brocaaphasia, transcortical motor aphasia, aphemia,and the aphasia of the supplementary motorarea are the language disturbances germaneto discussion of frontal communication dis-orders. Although these syndromes are not ac-cepted as specific entities by all investigators,the basic features have been well described.

Broca Aphasia

This generally accepted aphasia syndromehas always been associated with pathology in-volving the frontal lobe. Primarily an expres-sive disturbance, Broca aphasia is character-ized by a nonfluent (sparse, effortful, dysar-thric, dysprosodic, and agrammatic) output,relatively good comprehension, poor repetitionand troubles with naming, reading, and writ-ing. Traditionally, involvement of the poste-rior-inferior frontal lobe (Broca's area) of thedominant hemisphere is said to underly Brocaaphasia but most recognize that considerablybigger lesions, particularly deep into the insula,are necessary for the entire syndrome (Kleist,1934b;Mohr, 1973; Mohretal., 1978). Alongwith the aphasia there is usually a right hemi-plegia and a number of other behavioral find-ings may be present,

Aphemia (

Also known as pure word dumbness andanarthria, this disorder is a vocal output dis-


turbance with no abnormality of languagecomprehension (spoken or written) and nor-mal language production through writing.Aphemia often starts with mutism, but even^tually there is a return of verbal output of poorquality, breathy, soft, slow, and dysprosodic.It is usually suggested that the pathology inaphemia involves Broca's area or tissue justbelow this area (Bastian, 1898; Benson, 1979),but there is no significant cortical or deepspread. That aphemia represents a portion ofthe full Broca aphasia picture appears probablebut unproved.

Transcortical Motor Aphasia

Closely resembling Broca aphasia with theexception that repetition is comparatively in-tact, cases with transcortical motor aphasia(TCM) almost invariably show pathology thatspares Broca's area but involves cortical areasanterior or superior to it in the frontal lobe,Apraxia involving either bucco-facial or limbactivities is common, and some degree of righthemiplegia is always present. An inability toinitiate spontaneous speech, but no difficultyin the act of repetition, is the striking feature,leading to functional descriptive terms suchas frontal dynamic aphasia, verbal adynamia,and so on. Luria (1966) has stressed this dy-namic quality as a frontal language distur-bance. Again, some degree of TCM may bepresent in the Broca aphasia syndrome.

Supplementary Motor Area

That output disturbances occur with sup-plementary motor area pathology has beenrecognized for years (Foerster, 1936; Penfield& Roberts, 1959), but only recently has a clear,consistent syndrome been outlined (Rubens,1976; Alexander & Schmidt, 1980). The dis-turbance is characterized by a decrease of ver-bal output, facial expression, and gesture, butnormal comprehension and repetition, an ab*senee of paraphasia, and normal emotionalfacial responses (Damasio, Van Hoesen, &Damasio, 1980), The underlying characteristicis a lack of dynamism in spontaneous activitiesthat disappears during automatic response andthus closely resembles TCM.

The dynamic quality of the last two entitiesrepresents one of the more characteristic fron-tal language features and is present to some

degree in all frontal language disturbances: Thedifficulty can be described as a problem inspeech initiation and is illustrated using theword fluency test (Milner, 1964), probablybetter labeled a word-generation test. In thistest the patient is asked to produce a list ofwords belonging to a given category (animals,clothing, words beginning with the letter S,etc.). Other investigators (Benton, 1968; He-caen & Ruel, 1981; Ferret, 1974; Ramier &Hecaen, 1970) have demonstrated that indi-viduals with frontal pathology are particularlypoor at generating words. Caution is neededin interpretation, however; both right and leftpathology can disturb performance on this test(although there appears to be some hemi-spheric specificity), as dp aphasias from otherleft hemisphere areas and the cortical demen-tias. In contrast, prefrontal leukotomy did notresult in impaired word, generation (Stuss &Benson, 1983a). Newcombe (1969) found nospecific frontal lobe impairment with semantic(e.g., lists of animals) fluency tests, In general,however, the word fluency tests are sensitiveand demonstrate one primary manifestationof frontal language disorder; they are not spe-cific for frontal pathology, however.

A second major characteristic of frontallanguage disturbance involves syntactical lan-guage usage. Although agrammatism, a tenrdency to omit all syntactical language struc-tures, has long been described in the verbaloutput of Broca aphasia (Goodglass & Berko,1960), it has also been demonstrated thatfrontal pathology produces similar problemsin the comprehension of grammatic structuresof both spoken and written language (Samuels& Benson, 1979; Zurif, Caramazza, & Myer-soh, 1972). It has even been suggested that ananterior (syntactic) versus posterior (semantic)division of linguistic capabilities can be con-sidered. Although definitive proof remainsscanty^ there is a strong suggestion that syn-tactical language functions are primarily a left(frontal) function.

The ability to maintain a sequence, eitherverbal or nonverbal, is also reported as a frontalcharacteristic (Albert, 1972) and, as such, af-fects the comprehension of language. Thus,many patients with frontal pathology willcomprehend individual words well, but if givena sequence of words, will appear to compre-hend only a few (either the first or the last).


Some investigators have considered the limitedability of certain patients to repeat an auditoryspan disturbance (Warrington & Shallice,1969); others emphasize the rank ordering as-pect of sequential comprehension as the majordefect. Both aspects are subsumed under theterm sequence, a function that can be severelydisturbed by frontal pathology.

Finally, it has been proposed that a loss ofthe regulatory power of language can resultfrom frontal damage (Luria, 1966). Thus,frontal patients may verbalize a task correctlybut cannot use the verbalization to direct be-havior. Luria (1973) described frontal and pa-rietal patients who were asked to squeeze hardor soft to a signal (red, hard; green, soft). Nei-ther group performed this test well, but wheninstructed to use verbal cues to aid in the task,the parietal patients improved dramaticallyand the frontal patients remained poor. Thisis a verbal-action dissociation and will be dis-cussed further in the section on cognition.Nonetheless, it can be considered another ex-ample of frontal language disturbance.

In summary, pathological involvement ofthe frontal lobe produces a variety of languageabnormalities that reflect loss of control. Inaddition, there is a strong suggestion that somespecific, high-level attributes (syntactical lan-guage) are primarily or totally under frontalcontrol.

Memory

The idea of a memory deficit after frontallobe damage comes from the early animal ex-periments. Jacobsen (1935, 1936) observedthat monkeys with frontal lobe damage suc-cessfully performed immediate discriminationtasks but were impaired if delayed responsewas required. Subsequent research has lookedat factors such as distractibility (Finan, 1942;Malmo, 1942), drive (Pribram, 1950), andstimulus and task specificity (Jacobsen & Nis-sen, 1937; Pribram, 1961) to replace the con-cept of a memory deficit. Gross and Weis-krantz (1964) suggested that it was not amemory loss but an inability to use the mem-ories that were stored.

The possibility of a memory deficit withhuman frontal lobe pathology has also beenraised. Hecaen (1964), on the basis of his owntumor series and review of the literature, con-

cluded that some patients with frontal lobetumors were impaired in learning verbal pairedassociates. Deficits in maze learning by frontallobe patients have been reported (Corkin,1965; Milner, 1965; Walsh, 1960). Frontal lobepathology can result in impaired judgment ofrecency (Milner, 1971, 1974; Ladavas, Umilta,& Provincial!, 1979). These results suggest that,as indicated in the animal literature, frontallobe pathology interferes with certain memoryfunctions.

Negative results have been obtained in manystudies, however. Moreover, the frontal am-nesia suggested above may be, in some in-stances, more apparent than real (Milner,1964). Many frontal disorders, including un-concern, perseveration, and lack of initiative,suggest that apparent frontal memory im-pairment may merely reflect other disordersof complex behavior. Thus, deficits in mazelearning may be more parsimoniously inter-preted as a disregard for instructions and rulesplus perseveration; the recency effect may pri-marily represent disordered sequencing ratherthan a true memory disorder.

Luria suggests that the frontal memory dis-order is a binary deficit, consisting of an in-ability to create a stable intention to rememberplus an impairment of shifting recall from onetrace to another (Luria, 1971, 1973). Hecaenand Albert (1978) similarly proposed a deficitof selective attention and lack of initiative asthe primary source of the apparent memorydeficit. The disorder is a "forgetting to re-member" in which the details have not beenforgotten, but cannot be accessed at the time.

Study of the memory function in patientswho had undergone prefrontal leukotomymany years earlier lends support to these find-ings (Stuss, Kaplan, Benson, Weir, Chiulli, &Sarazin, 1982). These patients could learn newmaterial (logical memory, paired associates)in an apparently normal manner. If an inter-ference task were superimposed before re-testing (Cermak & Butters, 1972; Peterson &Peterson, 1959), however, the performanceswere significantly impaired. An exaggeratedinability to maintain new information in theface of interference would appear to be animportant frontal memory deficit (Malmo,1942, 1948; Malmo & Amsel, 1948).

These cumulative observations suggest thatfrontal damage does lead to disturbed function


on formal memory tests but that the frontalmemory problems differ distinctly from tem-poral or diencephalic amnesias. Details of thisdifference remain vague, however, and muchwork needs to be done to isolate the role ofthe frontal lobe in the overall memory func-tion.

Cognitive Functions

Much of the controversy and confusionconcerning frontal lobe function derives fromthe observations and studies of cognitive func-tions in frontal lobe damaged patients. His-torically, the prefrontal area was consideredby many to be the cortical region associatedwith the highest human functions (Jackson,1932). Individual case studies suggested thatextensive bilateral frontal damage could resultin cognitive deficiencies (Ackerly & Benton,1948), and loss of abstract thought was con-sidered to be an early sign of frontal lobe dam-age (Goldstein & Gelb, 1918). Loss of abstractthinking was reported in psychosurgery studies(Malmo, 1942) except after topectomy, whereimpairment was only transient (Mettler, 1949).Similar results have been noted in both lesionand tumor studies (Halstead, 1947; Rylander,1939).

Certain evidence conflicted with this stand,however. Cognitive deficits were not presentin all patients with frontal lobe damage(Feuchtwanger, 1923; Rylander, 1939) and,even when noted, were often difficult to rep-licate (Rylander, 1943). In a series of studies,Hebb concluded that frontal lobe patients didnot perform inferiorly on tests of intelligencecompared with patients with posterior lesions.One patient, in fact, improved after extensivebilateral frontal lobectomy (Hebb, 1939, 1945;Hebb & Penfield, 1940). These negative resultson intelligence tests were later replicated (Pol-lack, 1960;Teuber, 1959; Weinstein & Teuber,1957).

Additional research has pointed out somepossible reasons for the apparently discrepantfindings. In general, the observations have beencorrect, but underlying the demonstrated cog-nitive deficits there are often complicating dis-orders such as difficulties in attention, prob-lems in planning, and impaired monitoring ofperformance (Halstead, 1947; Hecaen & Al-bert, 1975;Luria, 1973;Milner, 1964; Teuber,

1964). Another problem stems from confusionin terminology (e.g., the use of abstract wordsversus the ability to think abstractly; Goldstein,1944). Research in the last few years has grad-ually defined some characteristic cognitive def-icits suffered by patients with frontal lobedamage.

Frontal lobe patients have no difficulty withthe basic operations (e.g., adding and sub-tracting) required to complete arithmeticaltasks. When given more complex problemsrequiring multiple steps, the patient tends torespond impulsively to an early stimulus andfails to analyze or execute the component stepsrequired for problem solution. Luria presentsexamples of questions designed to isolate thisdeficit (Luria, 1973; Luria & Tsvetkova, 1964).Certain arithmetic questions from the WAISare useful. For example, "The price of cannedpeas is two cans for 31 cents. What is the priceof one dozen cans?" is almost impossible formany frontal lobe patients to answer, eventhough the direct arithmetical task of multi-plying 6 times 31 is completed with compar-ative ease.

Block design tasks appear sensitive to frontallobe dysfunction in a special way. Lhermitteet al. (1972) documented specific steps in blockbuilding solutions during which the frontallobe patients may fail. Walsh .(1977) studiedsubjects with modified prefrontal leukotomywho had comparable pre- and postoperativeIQ levels. Performance in block design im-proved considerably when the patients, testedpostoperatively, were assisted by partial pro-gramming. This suggests that an organizationaldeficit was the primary problem. Goodglassand Kaplan (1979) noted that the patients withright frontal pathology focused on the salientfeature of the block design, leading to a brokenexternal configuration.

Maze tests also appear sensitive to frontallobe dysfunction. Perhaps the most frequentlyused in the Porteus Maze Test (Porteus, 1950),which requires advanced planning of the routeto be followed, anticipation of possible blockedpassages, and completion of the planned ac-tion. Almost all postleukotomy studies dem-onstrated clear impairment on the PorteusMaze (Malmo, 1948; Mettler, 1952; Petrie,1949; Porteus & Kepner, 1944; Porteus & Pe-ters, 1947). Other maze tests are not as spe-cifically susceptible to the effect of frontal lobe

18 DONALD T. STUSS AND D, FRANK BENSON

damage as the Porteus Maze, but with most,frontal patients will show specific qualitativeerrors. Although the patients apparently un-derstood and could repeat the rules, they wereunable to follow them or use knowledge ofincorrect performance to alter their behavior(Benton, Elithorn, Fogel, & Kerr, 1963; Milner,1964; Walsh, 1960).

Perhaps the most widely accepted measureto show executive functional deficit is the sort-ing task. One unpublished study, reported byShallice (1982), stated that the category sortingtask was the only one of 10 tests for frontalskills that produced significant anterior-pos-terior difference. Sorting tasks are not pri-marily tests of abstraction or concept for-mation but, under certain methods of admin-istration, measure application of rules ratherthan knowledge of facts. Although some degreeof abstraction is required, performance insorting tasks can be severely impaired in pa-tients who readily recognize and verbalize (ab-stract) all of the underlying concepts.

Halstead (1940, 1947; Shure & Halstead,1958), using the Halstead Category Test, dem-onstrated that frontal lobe patients had greaterimpairment than patients with lesions else-where in the brain. This differential effect wasnot replicated with Grant and Berg's (1948)modification of the Weigl (1941) Sorting Test(Teuber, Battersby, & Bender, 1951). Theseauthors found that frontal damage after missilewounds resulted in less impairment on thistest than did damage in parietal areas. Theirmodification of the test, however, did not allowbuildup of the prior correct response beforecriterion change. Milner (1963, 1964), usingpatients who had lobectomies for seizure ther-apy reasons, used the same test (WisconsinCard Sorting Test) but changed the criterionwithout warning after 10 consecutive correctresponses. With this technique, frontal lobepatients were more impaired than patientswith damage elsewhere. These findings havebeen replicated frequently in patients with pa-thology in frontal systems from many etiol-ogies (Drewe, 1974; Walsh, 1978) includingParkinson's dementia (Bowen, Kamienny,Burns, & Yahr, 1975).

Several factors underlying impairment inWisconsin Card Sorting Test (WCST) perfor-mance can be discriminated. Subjects nor-mally verbalize the three underlying criteria.

Frontal patients, however, are unable to"change responses in accordance with varyingenvironmental stimuli" to overcome previ-ously established response patterns (Milner,1964). There is a tendency to perseverate pre-vious responses, seemingly replicating the ten-dency to perseverate seen in frontal animals(Harlow & Settlage, 1948; Mishkin, 1964;Pri-bram et al., 1964). There is a curious disso-ciation between knowing and doing (Luria,1973; Milner, 1964; Teuber, 1964), such thatverbalization no longer controls active behavior(Luria & Homskaya, 1964). Frontal lobe pa-tients know their errors, but are unable to usethat knowledge to modify behavior (Konow& Pribram, 1970). This thought-action dis-sociation has been described as a disconnectionof feedback-feedforward systems so thatknowledge of errors cannot be utilized (Pri-bram, 1971). Milner (1982) suggests that thischaracteristic frontal disorder is a more generalproblem in the use of external cues to directresponses rather than a selective verbal reg-ulation deficit. There is, in addition, a dis-tinctive lack of self-criticism that has been de-scribed as "a general loss of some feedbackmechanism, a disturbance in signals of error,or an inadequate evaluation of the patient'sown action . . . a deficit in matching actioncarried out with the original intention" (Luria& Homskaya, 1964). Superimposed on thisproblem is a basic unconcern, a common fea-ture in frontal lobe disturbance.

A study of cognitive function in prefrontalleukotomy patients illustrates some of the im-portant distinctions that must be considered(Stuss et al., 1983; Stuss, Kaplan, & Benson,1982). Three groups of leukotomized schizo-phrenic patients were compared with two con-trol groups—a nonleukotomized schizo-phrenic group and a normal control group.Four tests were administered: the WechslerAdult Intelligence Scale, a test of comprehen-sion in metaphorical language (Winner &Gardner, 1977), a visual-verbal test of ab-straction (Feldman & Drasgow, 1,960), and theWisconsin Card Sorting Test. The resultsclearly demonstrated that some patients withvery large bifrontal lesions could perform ad-equately on general intellectual tests such asthe WAIS. These patients could also performbasic tests of abstraction competently. Theyhad difficulty, however, in verbalizing abstract


responses, shifting perceptual sets even withina simple abstraction test, and maintaining longsequences of correct responses.

Recent efforts have been made to under-stand frontal lobe deficits in terms of cognitivepsychology and artificial intelligence theory(Shallice, 19 82; Shallice & Evans, 1978). Shal-lice (1982) postulates two separate operationsin problem solving. Contention scheduling isthe term used to describe the fast, efficient,routine use of limited resources. With the in-troduction of nonroutine factors (e.g., a newproblem), a general programming, planning,and monitoring system, the Supervisory At-tentional System, is made operational. Usinga "Tower of London" task that appears to de-pend entirely on the general programming unitrather than on known routine programs, Shal-lice was able to demonstrate the effect of leftanterior pathology. This selective deficit maybe similar to the concept of left hemisphere(frontal) dominance for the programming ofvoluntary actions (Milner, 1982).

, - In summary, patients with frontal lobedamage do suffer significant cognitive distun-bances. The disability, however, is differentfrom that suffered by patients with lesions inother cortical areas and can be missed by manyof the current tests of cognition. Improvedneuropsychological techniques, possibly as-sisted by theoretical concepts and experimentalprocedures, from cognitive psychology, willlead to a better understanding of the role ofthe frontal lobes in cognition.

Frontal Lobe Personality

General Description

Probably the most widely accepted (and ob-vious) alteration secondary to frontal lobe ab-normality concerns change in personality, "thefrontal lobe personality," or "frontal-lobish-ness," Although widely recognized and totallyaccepted, specific descriptions of this alterationare difficult to present; a morass of behavioralabnormalities have been described under theterm frontal lobe personality. These includeunrestrained and tactless behavior; moodchanges including jocularity and bawdy, puer-ile joking ("Witzelsucht"); blunted feelings;callous unconcern; boastfulness; and gran-diose, obstinate, and childishly egocentric be-havior. Related intellectual changes include

deterioration of memory and intellectual abil-ities, although these are often said to be moreapparent than real. There appears to besuppression or actual inability to produceimaginative or original thinking; there is a dis-tinct diminution of spontaneity and initiative.Inattentiveness, distractibility, and ineffectiveor careless working habits are frequently ob-served. Apathy, dullness, indifference, andslowness of thought are described as-part ofthe syndrome. At times drowsiness, lethargy,and general retardation may be present, mostoften in progressive tumor situations. A va-cancy of facial expression has been observed,as well as a tendency to be careless in dress,to eat gluttonously, and be unconcerned. Withprogressive frontal disorder, complicationssuch as generalized convulsions, dysphasia,grasp reflex, forced groping, and frontal motordisturbances may all be seen. Through all ofthis, there is almost constantly a striking lackof insight. Descriptions of frontal lobe per-sonality, therefore, cover a vast variety ofsymptomatology and there is considerablevariation among patients.

The first report of change in personality fol-lowing frontal injury dates-to 1835 (Blumer& Benson, 1975) and describes an adolescentwith a self-inflicted frontal gunshot wound.Although the patient became blind, the patientwas described as happy, vivacious, and jocular.The most widely recognized early case of fron-tal personality alteration is that of PhineasGage (Harlow, 1868), a hard-working, sober,reliable, family-oriented construction foremanwho sustained a major injury to the frontallobes. Miraculously, the patient survived hisinjury without basic neurologic disability but,in the words of his fellow workers, "he was nolonger Gage." Harlow (1868) described Gage'spost-injury personality as follows:

The equilibrium or balance, so to speak, between his in-tellectual faculties and animal propensities seems to havebeen destroyed. He is fitful, irreverent, indulging at timesin the grossest profanity, manifesting but little deferencefor his fellows, impatient of restraint or advice when itconflicts with his desires, at times pertinaciously obstinate,yet capricious and vacillating, devising many plans of op-eration, which are no sooner arranged than they are aban-doned in turn for others appearing more feasible. A childin his intellectual capacity and manifestations, he has theanimal passions of a strong man. (pp. 339-340)

This description has stood the test of time and


remains a classic description of frontal lobepersonality.

Another excellent description of profoundfrontal lobe personality changes was providedby Brickner (1936), discussing the behavioralalterations of an individual who had bothfrontal lobes removed surgically as treatmentfor a perisagittal meningioma. Detailed de-scriptions of this individual's personality bothbefore and after surgery provide much thesame picture noted above.

Many descriptions of frontal lobe person-ality changes came from the physicians whocared for the brain-injured of the two WorldWars. Sizeable numbers of individuals sur-vived with major frontal lesions, and their re-sidual psychiatric and personality disorderswere carefully recorded (Faust, 1960; Kleist,1934a; Lishman, 1966). Again, large lists ofsymptoms were presented by most authors butsome grouping by phenomena was done. Forinstance, Kretschmer (1956) divided the fron-tal brain injury group into three major classes:a lateral convexity injury group whose majorcharacteristic was apathy and lack of drive;an orbital group whose major finding was un-restrained, disinhibited actions; and a basalgroup whose personality problems were com-plicated by autonomic abnormalities.

Luria (1966) reported evaluations of manypatients with frontal damage caused by bothtrauma and tumor, and emphasized the per-sonality alterations. He suggested that the al-terations were the result of disturbances of at-tention and concentration plus the inabilityto handle activities demanding a complex se-quence of mental activities.

Certain information on frontal lobe per-sonality changes was available from the studiesof patients who had undergone psychosurgeryfor psychiatric disease. In one large study,Greenblatt and Solomon (1958/1966) definedfour major alterations in behavior that werepresent following prefrontal leukotomy: shal-lowness of affect, decreased drive, social un-concern, and inability to anticipate (planahead). These subjects should have providedinvaluable information because they hadcarefully positioned, relatively precise frontallobe lesions, making them almost an idealsubject group for frontal studies. The resultsproved to be difficult to evaluate, however,largely because of their premorbid psychiatric

problems, and there is relatively little sub-stantiated information on personality changessubsequent to prefrontal psychosurgery.

Finally, Blumer and Benson (1975) de-scribed two significantly different personalitytypes based on structural damage to differentportions of the frontal lobe. Following Kleist,they suggested that there was a dorsal-lateralconvexity disturbance characterized by apathy,lack of drive, inability to plan ahead, and totalunconcern. They noted that these patients ap-peared to have depressed mentation but thattests of intellectual function demonstratednormal or near normal capabilities, so the termpseudo-depressed was suggested for this group.Examples were presented of both tumor andtrauma presenting with this personality alter-ation and having a focus of pathology in thedorsal-lateral convexity.

The second frontal personality abnormalitylisted by Blumer and Benson was quite dif-ferent. In this personality change the majorcharacteristics were a puerile, jocular attitude,sexually disinhibited humor, and inappropriateand near total self-indulgence with a corre-sponding lack of concern for others. Based onthe nature of these characteristics the termpseudo-psychopathic was suggested. Again,several varieties of pathology including bothtrauma and tumor were capable of producingthis personality alteration. The common factorwas the location of pathology in the orbitalaspect of the frontal lobe.

Although they noted that all of their caseshad suffered bilateral frontal involvement,Blumer and Benson admitted the possibilitythat frontal personality alterations might followunilateral disease. The nature of the morecommon causes of frontal pathology (tumorand trauma) were such, however, that purelyunilateral involvement was rarely noted. Thereis some suggestion from the psychosurgery lit-erature that alterations in personality did occurfollowing unilateral frontal leukotomy pro-cedures (Greenblatt & Solomon, 1958/1966).Only a small number of unilateral operationswere performed, however, and they are difficultto interpret because of the premorbid psy-chiatric abnormality. The question whether asignificant frontal personality alteration canoccur with unilateral frontal disease remainsopen but there is good evidence that majorpersonality changes do occur following frontal


lobe damage and that more than one person-ality type may result.

Although widely accepted, the concept offrontal lobe personality alteration remainsvague. At least two behaviorally separablefrontal lobe personality syndromes, describedabove as pseudo-depressed and pseudo-psy-chopathic, are reported, but most individualswith significant frontal pathology have somemixture of these problems. In addition, mostof the personality abnormalities described inthe literature include alterations in both af-fective state and intellectual quality. Betterunderstanding of the frontal lobe personalitydemands a better understanding of the mul-tiple, interrelated disorders that follow frontallobe damage (Damasio & Van Hoesen, 1983;Stuss & Benson, 1983b). It seems probablethat premorbid personality features are alsosignificant in the final clinical picture, althoughthis is far more difficult to prove than to sur-mise.

Localization And Hemispheric Asymmetryof Frontal Lobe Function

The. questions of localization and asym-metry of frontal lobe function overlap and re-volve about the organizational specificity ofthis cortical area. Without question, the frontallobes have proved to be the most difficult cor-tical area to map. Many of the frontal defectsthat have been described appear global in na-ture, with little evidence for specific localiza-tion. Part of this problem stems from the non-focal nature of the more common pathology.Frontal tumors usually produce bilateral ef-fects and are frequently undetected until ex-tensive damage has occurred. Significant fron-tal head trauma almost always results in wide-spread, nonlocalized pathology. In addition, areview of the neuroanatomy of distant con-nections to various parts of the frontal lobesfails to provide simple stimulus-response pat-terns. Multiple factors serve to make local-ization within the frontal lobe difficult. Despitethese difficulties, however, some localizingspecificity is apparent.

The most generalized concept of localizationis the division between the dorsal-lateral andthe basal-medial section (Girgis, 1971). Thedorsal convexity is most often associated withdisorders of movement and intellectual func-

tion. For movement, the location of the lesionon the lateral convexity is relevant. More pos-terior frontal lesions tend to result in diffi-culties in organization of movement, whereasmore anterior lesions result in deficits in motorprogramming and a dissociation between lan-guage and behavior (Luria, 1965, 1973). Anumber of reports of findings following psy-chosurgery suggested that dorsal-lateral lesionsled to greater behavioral deficits (Girgis, 1971;Hamlin, 1970; Lewis, Landis, & King, 1956;Malmo, 1948; Petrie, 1952; Smith & Kinder,1959). Also Milner (1971) reports that per-formance on the Wisconsin Card Sorting Testis maximally impaired with dorsal-lateral le-sions.

Possible reasons for the freedom from deficiton standardized intellectual tests by patientswith orbital-frontal lesions are summarized byWalsh (1978). The tests depend on long-storedinformation and on skills relatively insensitiveto subtle changes of behavioral regulation.Walsh (1978) reported, however, that not evenmedial orbital lesions were completely freefrom intellectual changes. Moreover, researchin cognitive functions in patients with orbi-tal-frontal pathology suggested that althoughIQ may be unimpaired, specific errors relatedto perceptual shifts and an inability to main-tain consistent patterns of organized responsescould be seen (Stuss et al., 1983; Stuss, Kaplan,& Benson, 1982).

Basal-medial lesions have often been relatedto disturbed impulse control, faulty activation,and shallow affective responses. Seemingly, thisdisorder is responsible for fantastical confab-ulation (Luria, 1973; Stuss et al., 1978), andunderlies certain personality disturbances.Personality alterations can occur with pa-thology anywhere in the frontal lobes, however,and specific behavioral patterns appear to de-pend on lesion localization. Thus, convexitylesions are characterized by a lack of drive,disinhibition, indifference, lack of productivethinking, euphoria, and inability to make de-cisions, whereas orbital lesions result inaggression, disinhibition, demanding and in-terfering actions, and increased sexual potency.

Hemispheric specificity or unilateral dom-inance of a single frontal function is not clearlydemonstrable. A verbal/nonverbal split is mostoften cited, with the best examples using re-cency and fluency tests. Milner (1971, 1974)


reported that the temporal ordering of eventswas hemisphere specific, with left frontal le-sions causing decreased verbal recency andright frontal lesions causing decreased non-verbal recency. Benton (1968) noted that leftfrontal patients are impaired in verbal fluencybut right frontals had more difficulty on con-structional tasks and the copying of designs.The fluency issue was further clarified, showinga more specific dissociation between verbaland nonverbal fluency and hemispheric dom-inance (Jones-Gotman & Milner, 1977). Morerecently, Milner (1982) suggested a more pre-cise hemispheric specificity based on analysisof the temporal organization of behavior. Leftfrontal lobe patients were impaired on all vol-untarily (subjective) controlled ordering of ac-tions, but the right-frontal patients were de-ficient only if the task was nonverbal. In con-trast, for tasks demanding the monitoring ofthe temporal sequencing of externally orderedevents (recency), the right-frontal patients wereimpaired regardless of modality, whereas theleft frontal patients had a moderately severeproblem only for verbal stimuli.

Other hemispheric differences have beennoted. Smith (1966) originally reported no IQalterations with frontal lobe damage, but whenthe patients were divided into left and rightfrontals, a significant difference was noted,with the left having lower IQ scores. McFieand Thompson (1972) observed a selective def-icit of picture arrangement capability afterright frontal lobe damage.

The results reported above suggest bothhemispheric differences and anatomically lo-calized dysfunction following frontal damage,but the tenuousness of the findings show anobvious need for much more study beforediagnostically acceptable conclusions can bemade.

Summary

Although this article has outlined a numberof apparent frontal lobe functions, it is obviousthat the functions of this massive and phylo-genetically novel prefrontal cortex are com-plex, interrelated, and as yet incompletely un-derstood. Part of the riddle of the frontal lobesderives from the size and complexity of thecortical area in question, but knowledge hasalso been hindered by inadequate test pro-

cedures and inability to obtain control of suchvariables as lesion size, location, and even lat-eralization. Consequently, current explana-tions of apparent frontal lobe malfunction re-main limited and vague. This does not lessenthe importance of the prefrontal area to humanbehavior nor does it diminish the importanceof the clinical research and theoretical insightsmade by investigators in past years.

It would appear that a few specific prefrontalfunctions can be extracted. These are broadand vague and certainly incomplete but doprovide direction for appropriate investigationand a base for theoretical considerations.

1. Prefrontal damage can separate action(response) from knowledge; this is illustratedby tests in which the patient could verballydefine (and apparently understand) the actionexpected but could not carry out the behaviorthat corresponded to this knowledge. This im-pairment was striking in complex tests suchas the sorting task, but prefrontal patients wereoften unable to use language (knowledge) tocorrectly guide even simple motor actions.

2. Prefrontal damage can impair the abilityto handle sequential behaviors. Language as-sessment revealed an inability to put items inan organized sequence; memory assessmentsuggested deficient judgment of recency, a taskthat requires ability to sequence; and sequen-tial motor tasks were often impaired, resultingin perseverative performance.

3. Prefrontal damage can impair the abilityto establish or change a set, resulting in ap-parently random or markedly perseverativebehavior. Impaired ability to both form andalter a set was noted in tests of attention and,most markedly, in the tasks of sorting andplanning.

4. Prefrontal damage can also impair theability to maintain a set in the face of inter-ference. The performance of the leukotomizedsubjects in the sorting task clearly revealedthis impairment. Interference as defined bythe Stroop test and the consonant trigrammemory tests also impeded performance inmany patients with prefrontal pathology.

5. Prefrontal damage impairs the ability tomonitor personal behavior. Erroneous actionscontinue uncorrected. Striking examples ofthis were noted in the inability of patients touse feedback in the sorting tasks and appearsto underlie some of the frontal disturbances


such as confabulation and the Capgras syn-drome.

6. Prefrontal tlamage can produce attitudesof unconcern, unawareness, and apathy, suchthat the patients ignore or actively deny manyof their difficulties.

These descriptions of impaired function donot represent all malfunctions secondary toprefrontal damage, but they appear in manyof the described incapacities of patients withdamage to this area. Whether they are facetsof one main deficit or based on functions ofspecific location cannot yet be determined. In,addition, as the frontal lobes are only infre-quently disturbed individually, these problemsare often combined ;with impaired functionsecondary to the damage in other brain areas.These combinations make up a major portionof the so-called frontal behaviors. The im-portance of the six abnormalities outlinedabove to the resulting picture is usually dis-cernable, but whether these impairments areexclusive to frontal malfunction is yet to bedetermined.

In conclusion, the neuropsyehblogic picturesecondary to prefrontal pathology is a complexand confusing set of behaviors. With appro-priate clinical/anatomical/psychological cor-relations many of these problems should be-come explicable, and in this process, muchwill be learned about prefrontal functions spe-cifically and human behavior in general.

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Received February 14, 1983Revision received June 6, 1983

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