11 neuroanatomical correlates of dreaming: the supramarginal gyrus controversy (dream work)

7/25/2019 11 Neuroanatomical Correlates of Dreaming: The Supramarginal Gyrus Controversy (Dream Work)

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Neuroanatomical Correlates of Dreaming: TheSupramarginal Gyrus Controversy (Dream Work)Calvin Kai-ching Yu aa Department of Counselling and Psychology, Hong Kong Shue Yan College, Braemar HillRoad, North Point, Hong Kong, e-mail:Published online: 09 Jan 2014.

To cite this article: Calvin Kai-ching Yu (2001) Neuroanatomical Correlates of Dreaming: The Supramarginal GyrusControversy (Dream Work), Neuropsychoanalysis: An Interdisciplinary Journal for Psychoanalysis and the Neurosciences,3:1, 47-59, DOI: 10.1080/15294145.2001.10773336

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Original Articles

Neuroanatomical Correlates of Dreaming: TheSupramarginal Gyrus Controversy (DreamWork)

Calvin Kai-ching Yu (Hong Kong)

Abstract: This paper aims to resolve the contradictory findingsbetween T and human lesion methods concerning the role ofthe inferiorparietal lobule supramarginal gyrus in the functionalarchitecture of dreaming, and to provide a more comprehensiveneuroscientific justification for its presumed psychoanalytic coun-terpart, dream work, a mechanism that has long been consideredto be the sine qua non o f the Freudian dream model. n contrastto prevailing belief, the author argues that the classical psychoan-alytic notion of this dream mechanism is compatible with, andalso supported by, the most recent neurobiological findings. Newpsychoanalytic insights and refinement are also drawn, based on

neuroscientific evidence, which breathe new life into th Freudiantheory o f dreaming.

Introduction

This is the first of three articles on the status of Freudian dream theory in the light of recent neuroscientificfindings. This first study concerns the role of the inferior parietal lobule in contemporary neurological models of dreaming and its implications for the Freudiannotion of dream work.

Solms (1995, 1997, 2000), basing his claims onthe clinicoanatomical method, put forth the argumentthat in dream formation abstract thoughts and memories are converted into concrete perceptions via the

Acknowledgment: The author dedicates this series of articles to MarkSolms, from whom (apart from Freud) he has learned most in his life. Hewould also like to thank Allen R. Braun, G. William Domhoff, Eric A.Nofzinger, and Pierre Maquet for the materials they provided. Thanks alsoto Hester McIntyre for her indefatigable support.

Calvin Kai-ching Yu, M.Sc., is a Lecturer in Psychology, Departmentof Counselling and Psychology, Hong Kong Shue Yan College, HongKong.

path of the inferior parietal lobule, in particular thesupramarginal gyrus (BA40), taking into account itspresumed functions at the highest levels of perceptualinformation processing and symbolic operations.

The evidential basis for this claim is Solms' s(1997) finding that inferior parietal lesions produce atotal cessation of dreaming, whereas unimodal visualcortical lesions produce modality-specific deficits ofvisual dream imagery. According to Solms, the normal

sequence of events in perceptual processing is thusreversed in dreams following the rule of regression: t he fabric of the dream-thoughts is resolved into itsraw material (Freud, 1900, p. 543). Furthermore,since dorsolateral frontal lesions have no apparent effect on dreaming, Solms (1997) argues that the focalpoint of cerebral activity shifts from the dorsolateralfrontal region, the executive end of the motor systemsin waking life, toward the perceptual systems, via theregressive pathway provided by the inferior parietalregion. This, according to Solms (1997), is exactlywhat Freud meant by topographical regression,perhaps the most essential part of the normal process

whereby dreams are formed (the dream work). Theinferior parietal lobule, from this point of view, isthought to be an indispensable ingredient of the functional architecture of dreaming. Moreover, this attribution of an important functional role to the inferiorparietal lobule applies equally to the neuropsychological-psychoanalytic model of Solms (1995, 1999)and the alternative, integrated model of Hobson(Hobson, Pace-Schott and Stickgold, 2000 .1

lThe inferior parietal region appears as zone in Solms's model,as depicted by Hobson, and zone 9 in Hobson's own model (Hobsonet aI. 2000).


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Some recent PET studies (e.g., Maquet, Peters,Aerts et aI., 1996; Braun, Balkin, Wesensten, Gwadryet aI., 1998), however, reveal that the inferior parietal

cortex, including the supramarginal gyrus (BA40), towhich Solms attributes such important functions indream formation (and where lesions apparently produce a total loss of dreaming) is significantly deacti-vated during REM sleep. Furthermore, although Solms(1999, 2000) has tried to apply neuroscientific findingsto the Freudian dream theory, the picture he describesis not at all complete. Topographical regression, forexample, is only one of the aspects of dream regression. Dream work, which includes equally basic mechanisms of condensation and displacement, has notbeen fully accounted for in Solms s model. Thus,Braun (2000) argues that the sophisticated process ofdream work requires considerable mobilization of thebrain s reflexive, executive mechanisms. These mechanisms are conventionally linked with the dorsolateralprefrontal cortex. Yet this region, no less than the inferior parietal lobes, is unequivocally deactivated duringdreaming (Braun, Balkin, Wesensten, Carson et aI.,1997) and lesions here have no effect on dreams(Solms, 1997).

The disparity between the clinicoanatomical andPET methods with respect to the inferior parietal lobes

is striking and has important implications for the scientific viability of psychoanalytic dream theory. Theprimary aim of this study is to attempt to clarify theevidential basis for this disagreement between the twomethods, and to attempt to find a resolution.

Method

Subjects

Three different sets of data were analyzed in the cur

rent study in order to achieve a more comprehensiveand reliable picture of the part played by the inferiorparietal lobule in dreaming sleep than has hithertobeen available: (1) all previous case reports from theclinical l iterature in which precise anatomical datawere provided, prior to Solms s (1997) monograph;(2) all the available CT and MRI scans of the clinicalcases studied in Solms s monograph; and (3) all theavailable PET data in the published literature. The current study involves a detailed reanalysis and comparison of these three sets of data.

Calvin Kai-ching Yu

Sample 1: Published ases from the linical Literature

The first sample consisted of 61 clinical cases of global

cessation of dreaming reported in the neurological literature (Wilbrand, 1887, 1892; Muller, 1892;Grunstein, 1924; Lyman, Kwan, and Chao, 1938;Piehler, 1950; Humphrey and Zangwill, 1951; Gloningand Sternbach, 1953; Boyle and Nielsen, 1954; Nielsen, 1955; Ettlinger, Warrington, and Zangwill, 1957;Ritchie, 1959; Michel, Jeannerod, and Devic, 1965;Farrell, 1969; Benson and Greenberg, 1969; Feldman,1971; Moss, 1972; Wapner, Judd, and Gardner, 1978;A Epstein, 1979; Basso, Bisiach, and Luzzatti, 1980;Michel and Sieroff, 1981; E. Epstein and Simmons,1983; Corda, 1985; Schanfald, Pearlman, andGreenberg, 1985; Pena-Casanova, Roig-Rovira, Bermudez, and Tolosa-Sarro, 1985; Habib and Sirigu,1987; Farah, Levine, and Calviano, 1988; Neal,1988 2 These were all patients who experiencedglobal cessation of dreaming as a consequence of neurological insult, regardless of the lesion site or type(see Table 1 This sample included 34 males 55.70/0 ,20 females (32.8 ), and 7 cases in which the sex wasnot specified (11.5 ). The average age was 47 years(s.d. 14.13, min. 18, max. 74).

able 1Neuropathology in S ampl e 1 (N = 61)

Pathology requency

Cerebrovascular Disease 34 55.7Tumor 9 14.8Infection 1 6Trauma 5 8.2Leukotomy 6 9.8Toxic Disease 1.6Missing Data 5 8.2Total 61 100

Sample 2: Solms s Original T a nd M R Records

Sixty-four clinical cases first reported in So lms s(1997) monograph constitute the second sample, comprising 36 (56.3 ) male and 28 (43.8 ) female patients. 3 These, too, were all patients who experiencedglobal cessation of dreaming as a consequence of neurological insult, regardless of the lesion site or type(see Table 2). Mean age is 40.8 (s.d. 17.77, min. 10, max. 77).

2A complete tabulation of these cases is archived at http://www.neuropsa.com/archive

am grateful to Dr. Solms for making this raw data available to me.


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Neuroanatomical Correlates of Dreaming 49

Table 2Neuropathology of Sa mp le 2 (N = 64)

Table 3Methods Used i n Sample 3 (N = 118 Ss)

Procedure and Materials

The locations of the lesions in samples 1 and 2 werecoded as precisely as possible, using the cytoarchitectonic maps of Brodmann (1909) and the templates ofDamasio and Damasio (1989), and the original descriptions and illustrations in sample 1 and the originalCT and MRI scans in sample 2. Among the 61 casesin sample 1 only 8 cases were suitable for such preciselocalization, since most of the original descriptions

The third sample consisted in PET data drawn fromnine previous studies, involving a total of 118 healthysubjects (Heiss, Pawlik, Herholz, Wagner, and Wienhard, 1985; Maquet, Dive, Salmon et aI., 1990; Madsen, Holm, Vorstrup et aI., 1991a; Madsen, Schmidt, i l d s h i ~ d t zet aI., 1991b; Hong, Gillin, Dow, Wu,and Buchsbaum, 1995; Maquet, Peters, Aerts et aI.,1996; Nofzinger, Mintun, Wiseman, Kupfer, andMoore, 1997; Braun, Balkin, Wesensten, Carson etaI., 1997; Braun, Balkin , Wesensten, Gwadry et aI.,1998). Ninety-one of these subjects were male(77.1 ) and 18 were female (15.3 ). The sex of 9

subjects was not mentioned in the original studies(7.6 ).The methods employed across the nine studies,

though similar, were not identical (see Table 3). Honget aI. 's study (1995), for example, instead of comparing the cerebral activity in dreaming states against thatof wakefulness, correlated the cerebral metabolic ratewith the number of REMs during dreaming sleep.Two methods of measurement, cerebral blood flow(CBF) and cerebral metabolic rate (CMR), were usedin these PET studies. Only in one study were bothtechniques employed (Madsen et aI., 1991b).

Frequency PE T Study Measure REM State No. Sex of Subjects

Compared toHeiss et al. rCMR Glu Wakefulness Experimental: 1 M(1985) Contro l: 5 MMaquet et al. rCMR Glu Wakefulness Experimental: 10 M, 1(1990) F

Contro l: 9 MMadsen et al. rCBF Wakefulness 6 M F(1991a)Madsen et al. gCBF Wakefulness 8 M 6 F

(1991b) gCMRo 2Hong et al. rCMR Glu Correlate with No. of Experimental: 9(1995) REM Control: 6Maquet et al. rCBF Wakefulness & SWS 19 M(1996)Nofzinger et al. rCMR Glu Wakefulness 6 F

(1997)Braun et al. rCBF Wakefulness & SWS 37 M(1997)Braun et al. rCBF Wakefulness & SWS 1 M(1998)

r = regional, g = global, CMR = Cerebral Metabolic Rate, CBF = Cerebral BloodFlow, Glu = glucose, 2 = oxygen

Results

were either not concrete enough or lacking in illustrations suitable for accurate coding. Likewise, only 35of the 64 patients in sample 2 could be traced usingthis precise method (principally due to curren t un

availability of the original records).The PET data (sample 3) was similarly coded,adopting Damasio and Damasio's (1989) method. TheBrodmann-coded brain lesions of the patients fromthe first and second samples and the Brodmann-codedlocations identified by the PET data of REM 'dreaming sleep were then analyzed and compared.

Neuroanatomical nalysis of linical ases fromthe Literature

Posterior cortical lesions were prominent in the 61cases reported in the clinical literature (38 cases) and

This section is divided into three parts correspondingto the three samples and it clarifies which posteriorcortical structures are actively necessary for dreamformation and which are not. The supramarginal gyrusis, as mentioned previously, at the heart of thequestion.

26.61.6

3.132.829.7

1.64.7100

171

22119

13

64

Sample 3: Published T Data

Pathology

Cerebrovascular DiseaseCongenitalMalformationBenign CystTumorTraumaDegenerative DiseaseInfectionTotal


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50 Calvin Kai-ching Yu

Table 6Traceable Cytoarchitectonic Data i n Sa mp le 1 N = 8)

Neuroanatomical Analysis Solms s OriginalRecords

was therefore circumscribed to area 40 in only onecase (case 5 Lyman et aI. s 1938 case of parietaltumor).

Case number refers to the table archived at http://www.neuro-psa.com/archiveBA37 = inferior temporal gyrus, BA37 + BA36 = temporo-occipital junction, BA37+ BA27 = hippocampal-parahippocampal regions, BA37 + BA19 = extrastriatecortex, BA28 + BA36 = amygdala and hippocampus; R = Right; L = Lef t; B= Bilateral.

23

2

2

2133521

4

65

FrequencyA Laterality Case No.

4 R586 B589 L58

44 L5845 L5846 L58

5 L5, L587 L5, L45, R58

39 L5, B5840 L5, B58

22 R30, L5827 R4628 L37, L45, R4636 L37, L45, R4637 R30 L37 L45 R46 L4723 L45, L58

Insula R30

17 Rl R30, L45, L4718 Bl R30 L37 L45 L47 L5819 R30 L37 L45 L47 B58

Lobe Involved

Frontal

Occipital

Temporal

Lesions Include Frequency

Frontal Lobe 22 36.1 ParietalParietal Lobe 25 41.0Temporal Lobe 28 45.9Occipital Lobe 24 39.3

Localization Frequency

Frontal 10 16.4Parietal 6 9.8Temporal 4 6.6Occipital 6 9.8Frontal-Parietal 3 4.9Frontal-Temporal 3 4.9

Parietal-Temporal 5 8.2Parietal-Occipital 5 8.2Temporal-Occipital 10 16.4Frontal-Parietal- 3 4.9TemporalLeft Hemisphere 3 4.9Pure Centrencephalic 3 4.9Total 61 100

pIe; see Table 4). The most common combination oflesion sites was temporo occipital (10/61 cases; 7/8

Table 5Neuroanatomical Characteristics of th e Clinical Cases Re

ported i n t he Literature (2) N = 61)

These lesion sites are not exclusive.

in the 8 cases from which more precise anatomicaldata were available (all 8 cases). The lesions involvedthe temporal lobe more than any other (28/61 cases

in the total sample; 6/8 cases in the detailed subsam-Table 4

Neuroanatomical Characteristics of t he Clinical Cases Reported i n th e Literature (1) N = 61)

cases; see Table 5). Looking in more detail at the cytoarchitectonic areas involved in the 8 traceable cases(Table 6), the most common lesion sites were in areas18 (6 cases), 19 5 cases), and 37 5 cases). Area 40was affected in only two cases (cases 5 [tumor] and58 [cerebrovascular disease])4. In one of these cases(Michel et aI., 1965, case with multiple vascular lesions; case 58 in the table archived at http:/ /www.neuro-psa.com/archive) the lesion was widelydistributed and therefore difficult to interpret in localizationist terms. Significantly, this patient also had pathology in the temporo-occipital area, and inBrodmann s areas 18 and 19 in particular. The lesion

4These case numbers refer to the table archived at http://www.neuropas.com/archive

At first glance, the distribution of the lesions inSolms s clinical series appears to be quite differentfrom and even incompatible with that in the previousliterature (Table 7). Posterior lesions predominate

once again. However, in stark contrast to the prevalence of temporo-occipital lesions in the nondreamingpatients from the literature, parietal lesions seem to bepredominant in Solms s series (27/35 cases 77.1

This number significantly outweighs the incidence rates of lesions in the other three lobes X 2 11.64, df 3 P < 0.01). Consistent with Solmss(1997) hypothesis but in striking contradiction to theresults drawn from the previous literature (pp. 49-50and the PET data (p. 52), this data seem to supportthe hypothesis that parietal lesions are a significantneuroanatomical correlate of cessation of dreaming.


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Neuroanatomical Correlates of Dreaming

Table 7Traceable Gross Lesion Data in S am pl e 2 (N = 35)

Localization Frequency

Frontal 4 11.4Parietal 3 8.6Temporal 1 2.9Occipital 0 0Frontal-Parietal 8 22.9Frontal-Temporal 0 0Parietal-Temporal 7 20.0Parietal-Occipital 2 5.7Temporo-Occipital 3 8.6Frontal-Parietal-Temporal 5 14.3Frontal-Parietal-Occipital 1 2.9Parietal-Temporal-Occipital 1 2.9Total 35 100

Seventeen cytoarchitectonic regions of interestwith reference to Solms s series are listed in Table 8

Table 8Traceable Cytoarchitectonic D at a i n Sample 2 = 35)

Lobe Substructures Left Right Bilateral Total

Frontal BA8 1 2 0 3 8.6BA9 3 6 0 9 25.7BAIO 2 3 0 5 14.3 il 1 3 0 4 11.4BA45 3 6 I 10 28.6BA46 2 3 1 6 17 1BA47 2 1 0 3 8.6

Parietal BA39 3 6 10 28.6BA40 8 12 21 60

Temporal BA20 4 4 0 8 22.9BA21 7 6 0 13 37.1BA22 10 II 0 21 60BA37 6 8 0 14 40

Occipital BA17 3 0 0 3 8.6BA18 3 1 0 4 11.4BA19 5 3 0 8 22.9

Subcortical Thalamus 5 5 0 10 28.6

These 17 regions are not all the Brodmann areas damaged in the nondreaming patients, but all are relatedto the controversy at issue here. Consonant with theimpressive incidence of the parietal lesions notedabove, the supramarginal gyrus (BA40) is also themost frequent cytoarchitectonic site of lesion (60 ).However, the same rate of occurrence was found inthe superior temporal gyrus (BA22). An area that appeared significant in our analysis of the cases in theprevious literature (pp. 49-50) also demonstrated rela-

51

tively high frequencies in Solms s series (40 ),namely, the temporo-occipital junction (BA37). Thesame cannot be said for areas 18 and 19 (frequency

11.4 and 22.9 respectively).Although BA40 lesions were common in comparison with the other regions of interest in this series,cessation of dreaming in the cases with BA40 lesionsis nevertheless not necessarily the result of BA40 lesion alone. Rather, i t may be the consequence of neuropathology concurrently affecting other crucialcomponents of the functional architecture of dreamingin the same patients. In this regard, areas 22 and 37appear to be of particular interest. If nondreaming patients with BA40 lesions also sustained injury to BA22or BA37, the role of BA40 in the neural network of

dreaming is more questionable.A significant positive correlation between BA40and BA22, which is located immediately inferior toBA40, was found (Pearson s X 2 5.73, df 1 P 0.1), a considerable number of patients sustained both lesions, that is, half of the patients whohad BA40 lesions also sustained BA37 lesions. Thesame applies to the thalamus, which may be importantin this connection due to its function of relaying information to various cortical areas. Further, despite thesmall number of cases with occipital pathology in thissample, 23.8 of BA40 patients had lesions in BA19.

Only three of the 21 cases with BA40 lesions(14.3 of cases with BA40 lesions) were entirely freeof lesions in BA37 and 22 or the thalamus. In otherwords, 85.7 the cases with BA4 lesions also sus-tained injuries to these three other cytoarchitectonicregions interest The three exceptional cases withBA40 lesions but intact BA37, BA22, 19 and 18 andthalamus (cases 17 [Solms s case 143 with right parietal infarct], 29 [Solms s case 244 with left par ietal


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Neuroanatomical Correlates of Dreaming 53

P T Study BAS BA7 BA22 BA37 BA19 BA23 BA31 Insula

Table Activation of Regions Surrounding BA40 in REM Sleep

S (supplementary sensory area), 7 (high-order somatosensory system): superiorparietal cortex (precuneus), superior to BA40; BA22: superior temporal cortex, inferior to BA40; BA37: inferior temporal lobule, inferior and posteriorto BA40; BA19:extrastriate cortex, caudal to BA40; BA23, 31: medial parietal-limbic regions (posterior cingulate), behind BA40; Insula: medial tempo-parietal cortex, behind BA40. I:

increase, decrease, NS: nonsignificant, Empty cells: no change or no mention inoriginal study, R: significant on right side only, L: significant on left side only, Ant:anterior, Post: posterior.

cations for the Freudian dream theory in the contextof neuroscience. It should be made clear at the outsetthat the discrepancy between the distribution of thefirst two samples (i.e., the preponderance of temporooccipital lesions in the previous literature as opposedto parietal lesions in So lms s cases) might be due tothe fact that Solms s cases were an unselected continuous clinical series, whereas the cases in the literaturewere selected for publication by virtue of the fact thatthey presented with interesting visual disorders (ratherthan cessation of dreaming). This is likely to haveresulted in a disproportionately high incidence of tem

poro-occipital lesions in the latter group.The PET findings, too, may be potentially biased

(and the role of BA40 in dreaming may accordinglybe rejuvenated) in view of the increasingly apparentfact that REM sleep is not equal to dreaming sleep(Solms, 2000). The fact that the inferior parietal lobuleis not consistently activated in REM sleep does notexclude the possibility that it is consistently activatedin the dreaming portion of both REM and NREMsleep. A critical test of this possibility must await thefindings of fMRI studies (which permit more precise

Pathways of Topographical Regression

temporal resolution than PET studies). Such studiesare currently still in the planning stages. In the presentstate of our knowledge, however, the discrepancy between Solms s findings and the available functionalimaging findings are best interpreted as follows. It isunderstandable that Solms (1997) privileged the finding in his own unselected continuous clinical seriesof a high correlation between inferior parietal lobulelesions and cessation of dreaming over the previousliterature (cases selectively published for unusual visual disorders), which demonstrated the preponderance of occipito-temporal lesions. However, in lightof the subsequent functional imaging (PET) findings,unless and until fMRI findings reveal a high correlation between inferior parietal activation and dreamingsleep it is more reasonable to reinterpret Solms sfindings in light of the consistent finding in the previ0us literature an d the PET literature to the effect thattemporo-occipital structures and not the inferior parietal lobule are implicated in dreaming (or at leastREM) sleep. This brings new significance to the factthat areas immediately surrounding BA40 and 39 (i.e.areas BA22, 19 and 37) were contiguously lesioned inmost of Solms s cases. These areas are also implicatedin both the previous clinical literature and the existingfunctional imaging studies. In other words it now appears more likely that i t was the contiguous occipito-temporal component of the lesions in Solms s cases

that was responsible fo r the cessation of dreaming.

Solms (1995, 1999,2000) found a bridge between motivational systems (i.e., the limbic core) and the perceptual hallucinatory apparatus (i.e., the visual cortex)in the inferior parietal lobule (supramarginal gyrus,BA40). He linked this with the Freudian theory ofdream formation and topographical regression. Therole of the inferior parietal lobule, however, wasshown to be questionable in the present study whereoverlapping results did not provide compell ing evidence for its active involvement in dreaming.

The supramarginal gyrus is part of the associationcortex of the posterior cerebrum (BAS, 7, 40, 39, and 37), a zone of overlapping within the corticalend of the various perceptual analyzers that enablesthe different modalities to work in concert (Luria,1973). This work of the associative zones of the posterior cort ical regions is essential , not only for the successful integration of in format ion reaching manthrough his visual system, but also for the transition

I (L)

(Ant)D (post)

I (NS)

DPosCingu

DPosCingu

I (Post)I

I (NS) I (L) I (L)

I (R) I (R) I

D

Braun e t al.(1998)

Heiss et al.(1985)Maquet e t al.(1990)Mad sen e t al.(1991a)Madsen et al.(1991b)Hong et al.(1995)Maquet et al. D(1996)

of zingeret al.(1997)

Braun e t al.(1977)


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from direct, visually represented synthesis to the levelof symbolic processes. BA40 performs critical functions in associating and organizing cross-modal per

ceptions and visuospatial activities and, in the lefthemisphere, in operations with word meanings, withcomplex grammatical n logical structures with systems of numbers and mathematical relationships.

A theoretical question arises as to whether suchfunctions are necessary for dream formation. The answer is: almost certainly not. First, visuospatial cognition is indispensable for dreaming not simply becausethe visual content of dreams necessarily comprisesconcrete space with coordinates that presumably require a minimal level of objective frames of reference,but rather because they involve objects in the psychoanalytic sense. Second, as regards the logicogrammatical functions of the left inferior parietal lobule,the basic quality of dreaming is not logicogrammatical, but rather elusive and paralogical. This, however,leads to two further problems.

First, does the inferior parietal lobule never takepart in dream formation? The probable answer to thisquestion (which can only properly be answered byfurther research) is that it most likely depends on thekind of dreaming (i.e., the nature of the representations) an d the quality of the dreams in question. Relatively complex dreams made up of sophisticatedspatial and verbal elements, which surely obligate the

functions of spatial orientation and grammatical organization, may recruit the involvement of this importanttransmodal cortex. In such dreams significant variances in content and representation are found amongdifferent populations (Foulkes, 1982, 1999; Domhoff,2000). Children s dreams, for example, the most primal and simple ones, tend to be more visually basedthan adults dreams, as verbal linguistic skills and thuscomplicated verbal linguistic elements do not play arole until dreaming is fully developed around ages to 3 (Foulkes, 1982, 1999). Also, it is an undeniablefact (as shown in the Results section of this study) thatsome patients do lose the capacity to dream after pureparietal insults, and, therefore, attention may need tobe given to a certain level of individual difference ordreaming style.

So, if it is accepted that the inferior parietal lobuleis not normally essential to connect the motivationalsystems and the visual cortex in the way that Solms(1997) hypothesized, how might the dream work ofregression be performed? The findings of this studysuggest another pathway for the formation of dreaming in typical cases, namely, the inferior mesial temporal lobe (BA37), which has been identified by this

Calvin Kai-ching Yu

research as one of the most crucial structures indream formation.

The anatomical situation of BA37 equips it with

compact neuroanatomical and functional associationswith the occipital cortex (BA19 and 18) on the onehand, and the paralimbic and limbic structures (BA23,27, 28, and 36) on the other. Hippocampal and parahippocampal regions (BA37, 36, and 27) are centerswhich participate centrally in the encoding and retrieval of memory. The amygdala in anterio r BA28and 36, which serves as a neural substrate of emotionalbehaviors and motivation, is intimately connectedwith the hippocampus, hypothalamus, cingulate gyrus,and basal forebrain. The functions subsumed by allthese structures embody basic characteristics of, andprobably necessary preconditions for, dreaming.

Ample evidence supports the suggestion that theinferotemporal cortex is a ridge between the visual cortex and the limbic system, which has intenseafferent and efferent connections with both regions(e.g., amygdala, hypothalamus, entorhinal area, andfusiform gyrus) (Whitlok and Nauta, 1956; Akert,Gruesen, Woolsey, and Meyer, 1961; Prelevic, McIntyre-Burnham, and Gloor, 1976; Turner, Mishkin, andKnapp, 1980; Creutzfeldt, 1995). Moreover, specificthalamic afferents to the inferotemporal cortex arrivevia Arnold s bundle from the nucleus inferior of thepulvinar (thalamus), which in turn receives its afferents from the tectum and the pretectum, as well asfrom BA17 and 8 A similar situation also applies toits connection with the amygdala. Conversely, descending efferents from the temporal cortex project tothe optic tectum, the putamen, and the claustrum (inexternal capsule), in addition to the corticofugal reciprocal connections with the pulvinar (Whitlok andNauta, 1956).

These connections, furthermore, are consistentwith Braun, Balkin, Wesensten, Gwadrey et al. s(1998) finding that the extrastriate activity of BA37and BA19 is associated with concomitant activationof the limbic and paralimbic regions. Therefore, lesions here would imply that the intercurrent activityof this way station is blocked. It is therefore highlyplausible that BA37 constitutes the inferomesio tem-poro Limbic occipital pathway fo r topographical re-gression and thus for the formation of dreaming, byconnecting motivational and perceptuo-hallucinatorysystems. This pathway is more primitive than the relatively sophisticated pathway constituted by the supramarginal gyrus, but no less capable of performing therequisite functions.


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Neuroanatomical orrelates reaming

Representation

Interestingly, though unsurprisingly, according toFrackowiak, Friston, Frith, Dolan, and Mazziotta(1997), the ability to represent things in mind even inthe absence of direct perception of such things (e.g.,imaging, active memory) is contributed by a neuralnetwork including the posterior brain. However, thelocation of the coactivated posterior brain regions inquestion is dependent upon the nature of the representation. As Frackowiak et al (1997) underscored, research findings consistently indicate relativefunctional specialization in the parietal cortex for spa-tial representations and the inferior temporal cortexfor object representations. The activation of the inferotemporal cortex also provides relatively coarse andimprecise representations of visual objects. Inferotemporal representation is therefore mainly driven by complexity rather than specificity (Creutzfeldt,1995, p 418). More importantly, the inferotemporalcortex plays a role in categorization, specifically inthe classification of visual stimuli into certain behaviorally meaningful categories, and therefore, forgesconnections between visual experience, complex orsequential behavioral patterns, and temporal emotionalexperience (Weiskrantz, 1974; Creutzfeldt, 1995).

In analogy to the parietal association cortex, where

the relationship between visual and somatosensorysignals to the body and the extracorporal space ofaction is represented, one could say that in the tempo-ral neocortex the reference auditory, visual, andvisceral signals to a more subjective space expe-rience, emotion, and attention s represented, relatingthem to behavior as it is controlled by limbic andhypothalamic mechanisms [Creutzfeldt, 1995, p 419;emphasis added].

These bidirectional anatomical pathways seem to signify the qualitative aspect of what most dreams are;in o ther words most dreams are complex but vaguerather than specific, object rather than space dominated, oriented in subjective space rather than in objective space, visceral and emotional instead ofexternal and rational. All these factors cover the essential attributes of dreaming, and seem to resonate withthe Freudian (1914) assertion that the absolute narcissism of the state of sleep implies a withdrawal of cathexis from the ex ternal world of real objects backinto the subjective space of the self. W e know thatdreams are completely egoistic and that the personwho plays the chief part in their scenes is always to

be recognized as the dreamer (Freud, 1917, p 223).Perhaps, in agreement with the current neuroscientificfindings, this statement can be fine-tuned; dreams arerepresentations of emotionally charged object-relationships in an egoistic context, in which objectivereality and external constraints are relatively disregarded.

Primary Process: Temporal Regression,Condensation, and Displacement

Intriguingly, it is well known that abnormal excitationof the temporal lobe alone during an epileptic attackor exploratory electrical stimulation during surgerycan lead to hallucinations or dreamlike states, termed experien tial hallucinations a n d interpretative illusions by Penfield (1958). Stimulation of the cerebral cortex produces perceptual i llusions only in thetemporal regions and perhaps extending somewhatinto occipital cortex (Penfield and Rasmussen, 1955,p 173).

As reviewed and delineated by Luria (1973), various kinds of visual-verbal and even spatial hallucinations involve temporo-occipital stimulation, especiallyof the inferior regions; for instance, BA18 for elementary visual hallucination, BA19 and 37 for complexvisual hallucination, BA37 for complex spatial dis

placement, BA22, 41, and 42 for acoustico-verbal hallucination, and BA20 for lingual hallucination. Luria(1973) described all these hallucinations as reflectingthe subject s previous experience.

The experiential hallucinations comprise elements ofthe individual s previous experience drawn together.They can appear to him so unfamiliar that he describes them as dreams, but after careful analysisthese hallucinations can be broken u into shorter orlonger sequences earlier experiences. The patientrelives an episode from the past, although he is awareof the fact of being in the present. All the elementsof the earlier state of consciousness appear to be thereagain; l ight impression, sounds, explanations andemotions 8 In the case of an illusion of interpretation, there is sudden false explanation or a changedexplanation of the meaning of a current experience.Things which one has just heard or seen appear suddenly familiar (deja vu already seen, deja vecu

already experienced) or they may, in contrast, appearstrange or nonsensical. They appear to be larger or

Note the multimodal character of these experiences (vide infra).


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smaller, to come closer or go further away [Penfield,1958, pp. 23-24; emphasis added].

A few words seem to paraphrase and reiteratewhat Freud set forth about dream work and temporalregression. The experiential hallucinations caused byexcitations of the temporal cortex appear to be unfamiliar, strange, and senseless, but after analysis c anbe broken up into shorter or longer sequences of earlierexperiences. This is similar to what Freud referredto as condensation. In Freudian theory, any eventof incoherent, accentuated, or diminished intensity occurring in dreams is ascribed to the effect of displacement (transvaluation). This too, it seems, can betriggered by the stimulation of the temporal cortex:Things suddenly become familiar or, by contrast, appear strange or senseless; they appear to be larger orsmaller, to come closer or go further away. In thissense, Penfield s experiential hallucinations and illusion of perception and interpretation, whichmakes things strange and incomprehensible, or dramatically change their original appearances, are homologous to Freud s dream distortion.

It is worth noting that these hallucinations provoked by the temporal lobe excitations, according toPenfield (and highly congruent with Freud s theory),are recollections of the unconscious past, which allowreliving of previous experience that is not normally

accessible to consciousness when awake. To put it inFreud s words, t he unconscious material forces itsway into the ego (Freud, 1940, p 47).

In such repetitions of previous experience perceptionsare largely auditory, or visual, or both. Time seemsto unroll at its normal tempo. The return of the content of consciousness thus evoked, is quite at random,except that there is some evidence of cortical conditioning. The evolving detail is f r greater than memories which can be summoned voluntarily Thisdemonstrates the existence of a functional system devoted to subconscious recall ofp st experiences [Penfield and Perot, 1963, p 692; emphasis added].

Memory is far more comprehensive in dreams thanin waking life [Freud, 1940, p 166].

Multiple Pathways to Regression

BA22, albeit an auditory association area, may provide a potent contribution along the path of the dreamformation by transforming abstract thoughts into theconcrete acoustic or visual content of dreams (e.g.

Calvin Kai-ching Yu

, dream thoughts might, perhaps, first pass throughBA22 before being processed by BA37 and eventuallyarriving at BAI9).

Two patients reported by Solms (1997) sustainedlesions to BA37 but instead of a total loss of dreaming,they reported a cessation of visual dream imagery andcontinued to dream with other channels. The incidenceof this kind of disorder is extremely low (1.1 ) andp r contra a considerable number of negative caseswith the same lesions experienced a global cessationof dreaming. Also, BA37 in these two cases was notcompletely destroyed; rather the lesions involvedmerely a relatively small portion, that is to say, theventromesial aspects of BA37. The lateral aspects ofBA37 were almost completely spared in these cases.Perhaps the degree to which auditory material predominates in dreams or individual dreamers is determined by the extent to which this channel is reliedupon in any given case.

Other ontroversial Issues

Braun (2000) argues that the dream w ork requiresconsiderable mobilization of the reflective and otherexecutive functions of the dorsolateral frontal convexity, which is unequivocally deactivated during dreaming (Braun, et aI 1997; Solms, 1997). I take an

opposite point of view (Yu, 2000): The pervasive deactivation of all association cortex apart from BA37(which strongly implies a dissociation of cerebral activity and thereby explains the bewildering effect ofmost information processing during dreaming), underscores what Freud pu t forward as regards the dreamwor k The dream work and dream distort ion may,accordingly, not only be facilitated by the deactivationof dorsolateral prefrontal cortex and other associationareas (including BA40) but also positively caused bythe activation of BA37 and related occipito-temporalstructures.

Partly contradicting another controversial argument posed by Hobson (2000), these neuroscientificfindings seem to justify the Freudian view of the distinction between the manifest and latent content ofdreams. Although dream dis tortion seems not to bedirectly related to (or a direct product of) censorship,so long as dream distortion exists, there is necessarilya demarcation between the manifest and latent content. Hobson contradicts himself by insisting on theproposition that there is no real difference betweenthe manifest content and latent dream thoughts, andtherefore that dreams are transparent and can be read


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Department of Counselling nd PsychologyHong Kong Shue Yan CollegeBraemar Hill o d

North PointHong Konge-mail: [email protected]

11 neuroanatomical correlates of dreaming: the supramarginal gyrus controversy (dream work)

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