the role of the frontal lobes in the regulation

BRAIN AND COGNITION 20, 51-73 (1992)

The Role of the Frontal Lobes in the Regulation of Cognitive Development

ROBBIE CASE

Center for Educational Research at Stanford, School of Education, Stanford University

Between the ages of 1.5 and 5 years, and again between the ages of 5 and 10 years, a sequence of changes takes place in childrens behavior which indicates a fundamental reorganization of their attentional, executive, and self-reflexive processes. In the present article, these changes are summarized, and evidence is adduced to support the claims (1) that these changes are frontally mediated and (2) that the underlying mechanism that generates them is similar to the one that generates the changes in EEG coherence during the same time period. The psychological model that has been hypothesized to explain the cycles of cognitive development (Case, 1992) is then compared to the physiological model that has been proposed to explain cycles of EEG development (Thatcher, 1992). It is shown that the two models are complementary, both in the underlying developmental sequence that they postulate and in the recursive dynamic they propose for producing movement through this sequence. A number of implications and predictions are derived, which follow from the proposition that the two sets of changes are different manifestations of a common underlying process. c, IW2 Academic Press. Inc.

On the basis of the existing anatomical and neurophysiological data, as well as his own extensive data on brain-injured and normal adults, Stuss (1992) has concluded that the frontal system is responsible for controlling two of the functions that are most essential for high-level cognitive activity in humans, namely: (1) executive control of novel responses and (2) awareness of the self as an actor that has this sort of intellectual capability. Stuss has also reviewed data which suggest that the frontal cortex continues to develop, in a hierarchical fashion, for a good 20 years

I am endebted to Adele Diamond, Dan Keating, Anik DeRibaupierre, Juan Pascual- Leone, Sid Segalowitz, Donald Stuss, and Robert Thatcher for their comments on an earlier draft of the present article and to the McDonnell Foundation for supporting its preparation. 1 am also endebted to Wilma Strenk for her help in typing the manuscript and to Donald Hebb for planting the original seed. Address correspondence and reprint requests to Robbie Case, Center for Educational Research, Stanford School of Education, Stanford University, Palo Alto, CA 94305.

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52 ROBBIE CASE

after birth and that both of the foregoing functions continue to evolve throughout this time period.

On the basis of his work on the development of EEG coherence and phase, Thatcher (1992; see also Thatcher, in press) has presented a view of frontal lobe development that complements and extends the view proposed by Stuss. During the period between 18 months and 11 years, Thatcher has suggested that two cycles or waves of development may be identified, in which electrical activity in the frontal cortex is increasingly coordinated with electrical activity in other cortical systems in a dynamic fashion.

On the basis of these two general categories of data, and others like them (Matousek & Peterson, 1973; Hudspeth, 1985), both Stuss and Thatcher have implicitly endorsed the classical metaphor of the frontal system as an orchestra leader, whose function is to direct the activity of various other systems. What their work adds are the notions (1) that this role requires the frontal system to establish some sort of electro- physiological control of these other systems, in the course of ontogenesis, and (2) that the process by which this occurs is a hierarchical and dynamic one, which continues throughout the period of physical maturation.

If one were to stop at this sort of characterization, one would be on theoretical ground that is solid, in the sense that it is supported by the great bulk of data on normal and frontally impaired cognitive functioning in both adults and children. The characterization would also be supported by the great bulk of data on EEG patterning and anatomical change in the course of human and primate ontogenesis. Finally, the characterization would be congruent with the classical theoretical view of frontal functioning that was developed in the early 1960s (Luria, 1966; Milner, 1963; Teuber, 1964), as well as the refinements and reinterpretations of that view that have been generated since (e.g., Hudspeth & Pribram, 1990; Stuss & Benson, 1986, Thatcher, Walker, & Guidice, 1987).

While this neo-classical view seems correct in its broad outline, what I attempt in the present article is to move slightly beyond it, into an empirical and theoretical region that is more speculative. My motivation for doing so is that there is a striking similarity between the cycles of EEG coherence that have been documented by Thatcher and his colleagues and the cycles of cognitive growth that have been documented by contemporary investigators in the field of intellectual cognitive development (Case, 1985; Case, Kurland, & Goldberg, 1992; Fischer & Ferrar, 1988; Mounoud, 1986). Moreover, the cognitive cycles which have been studied most intensively appear to involve functions which are the developmental precursors of those that have been studied by Stuss in his work with frontal patients. By comparing Stusss and Thatchers data with the data on childrens cognitive development, then, it seems possible that a more integrated view of the development of the frontal system may be

REGULATION OF COGNITIVE DEVELOPMENT 53

obtained. It also seems possible that hypotheses may be developed which transcend any one of these fields of investigation and which may be used to inform further work of an integrative nature.

With these goals in mind, the present article has been organized in four sections. In the first, three sets of data are presented which bear on the development of childrens executive and self-reflexive capabilities in middle childhood; these data are then compared to the EEG data presented by Thatcher and shown to be similar in a number of important respects. In the second section, a similar set of data are oresented for the preschool period and once again shown to be similar to the EEG data presented by Thatcher. In the third section, the reasons for these similarities are explored, and a model is proposed that integrates the two different sorts of data. Finally, in the fourth section, several predictions are adduced from the model, for further exploration.

1. COGNITIVE DEVELOPMENT DURING MIDDLE CHILDHOOD

1. I Changes in A ttentional Capacity

The first function that Stuss attributes to the frontal lobes is the executive control of novel behavior. As even a casual analysis will reveal, one of the most distinctive characteristics of effective novel behavior is that it can only be generated once the available information has been scrutinized in the active fashion: certain items of information must be actively attended to, and others must be actively ignored, if subjects are to adapt their existing behavioral repertoire to the new situations that they encounter. It is because this sort of adaptation is necessary that, from the founding of cognitive psychology, the twin attentional functions of activation and inhibition have been regarded as essential to the exercise of the executive function (e.g., Baldwin, 1984; James, 1950).

As might be expected, these two functions have also remained of interest to contemporary theorists (Kahneman, 1973; Pascual-Leone, 1988; Stuss & Benson, 1986). In the developmental literature, a hypothesis that has been scrutinized with particular care is that children show a maturationally based increase in attentional capacity from 1 to 4 units during the period from 4 to 10 years of age and that this increase acts both to energize and to constrain the novel behavior they exhibit (Pascual-Leone, 1970). On a number of measures that were devised to test this hypothesis, what emerged was a strong linear increase from 1 to 3 units for the age range from 4 to 7 years, a decelleration which began at about the age of 8 years and an asymptote which began at about the age of 10 or 11 years (Case, 1972; Case, Kurland & Goldberg, 1982). Two measures which showed this trend quite reliably are the Counting Span, and the Spatial Span tests.

On the Counting Span test, subjects are asked to count a set of blue dots embedded in a field of yellow dots, touching each blue dot and

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enumerating it as they do so. They must then remember the total number of blue dots while they count the blue dots on a series of IZ - 1 further cards. Finally, they must recall each of the II totals they have computed and say them back to the experimenter in order. On the first block of trials, 12 is set at 1 (i.e., no subsequent card is presented). On each subsequent block, n is incremented by 1 unit. Eventually the point is reached where the subject can no longer remember all the totals for any trial: numbers from previous trials or from interpolated counting acts intrude, and the interference becomes too great for the subject to over- come. The number of card-totals that the subject can remember on the majority of trials within a block is then noted and referred to as his or her working memory for numbers.

On the Spatial Span test subjects are asked to inspect a 4 x 4 matrix and note which cell has been shaded. They are then shown a filler pattern, followed by a second, blank 4 x 4 matrix. When the second matrix appears, subjects must point to the cell which corresponds to the one that was shaded on the first matrix. Several blocks of trials are then presented, in which the number of cells shaded (n) is increased by 1 unit for each block. Again, a point is eventually reached where the subject can no longer remember all the positions successfully on the majority of trials within a block, due to the interference from prior and/or interpolated activity. The number of cells whose position can be recalled is referred to as the subjects working memory for grid positions (Crammond, 1992).

The specific operations that these two working memory tests require are of course quite different. What is common is that-within each test- subjects must (1) execute a series of highly similar operations, (2) store the products of these operations under conditions of strong interference, and (3) output these products in sequence. In Stuss and Bensons (1986) framework, as in Pascual-Leones (1970, 1988), what this means is that subjects must exercise both of the functions that are normally included under the rubric of executively mediated attention, namely (1) sustained activation of one set of units and (2) inhibition of a potentially competing set of units.

The sort of data that result when these tests are administered are illustrated in Table 1. Elsewhere, I have interpreted such results as providing strong support for Pascual-Leones theory. What is important in the present context, however, is their fit to Thatchers second cycle of EEG coherence. Although the two different sorts of data are hard to place on a common scale, a global comparison of their timing and shape is possible, by computing annual increments in span and comparing them with data on rate of EEG change. Such a comparison is presented in Fig. 1. The span data are from a meta-analysis of 12 developmental studies, each of which sampled cross-sectionally across a 6- to &year age range and assessed at least 80 children on one or both of the measures described


TABLE 1 MEANS AND (STANDARD DEVIATIONS) OF Two DIFFERENT ATTENTIONAL SPAN MEASURES

SCORES FOR AGE GROUPS

Span measure Age group ___-~____- mean (years) Counting 4 x 4 Matrix --__- ~__ __-. .~ _---.~ 4.61 (0.27) 1.07 (0.15) 0.96 (0.39) 6.62 (0.13) 2.08 (0.64) 1.95 (0.62) 8.57 (0.17) 3.13 (0.44) 2.88 (0.79)

10.56 (0.20) 3.41 (0.47) 359 (1.08) 15.10 (Sl) 3.83 (64) 3.79 (.4X)

-. ..~. ~-.-. Data from Crammond (1992). Data from Menna (1989).

4 45 5 5.5 6 61 T 75 8 85 9 9.5 Age I Years

FIG. 1. (A) Rate of growth of EEG coherence between frontal and posterior lobes during middle childhood (FI-PJ). (Source: Thatcher, 19Y2). (B) Rate of growth of working memory (counting span and spatial span) during the same age range.

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above. The EEG data are taken from Thatchers work, which is reported in this volume.

As will no doubt be apparent, there is an approximate correspondence in the shape and position of the two curves, which suggests that the two sets of data may be indexing a common underlying set of changes. Further evidence which bears on this interpretation comes from a study on frontal development by Segalowitz, Wagner, and Menna (1992). As part of this study, electrodes were placed on the central vertex (Cz) and frontal pole (Fpz), and contingent negative variation (CNV) was measured. The two measures of attentional capacity that were described above were also administered and shown to correlate significantly with frontal CNV (r = .40 and .44, for the Counting and Spatial Spans, respectively). Combining these data with those illustrated in Fig. 1, it seems reasonable to suggest that the growth of attentional span depends in some fashion on the functioning of the frontal lobes and/or changes in the extent to which frontal activity is coordinated with activity in other cortical systems.

1.2 Changes in the Power and Flexibility of the Executive Function

Although attentional activation and inhibition constitute two important components of childrens executive functioning, they are of course not all there is to this functioning. One of the best known tasks that has been used for studying childrens executive functioning more directly is Inhelder and Piagets (1958) Balance Beam task. This is a task in which children are shown a balance beam, allowed to play with it, and then asked to make predictions concerning which side will go down on a series of trials of increasing complexity. After each trial feedback is presented, so that children can see whether they are correct. Under these conditions, 4- year-olds tend to focus exclusively on the global perceptual appearance of the objects on each side in making their predictions and to perseverate on this variable, even in the face of negative feedback. Thus, they succeed on trials where a large stack of objects is on one side and this side happens to go down, but fail on all others (Case, 1985, p. 96.; Liu, 1981; Marini, 1992). Six-year-olds take account of the number of objects on each side as well, but perseverate on this dimension when feedback indicates that it is insufficient (Siegler, 1976; Furman, 1981). Finally, S-year-olds take account of the additional dimension that is of relevance, namely distance from the fulcrum (Siegler, 1976).

There is a clear relationship between childrens progression through this sequence and the development of their working memory on the measures described in the previous section. Children whose working memory development is delayed or accelerated show a corresponding acceleration

For further evidence on this point, see Howard and Pollich (1985); Pascual-Leone, Hamstra, Benson, Khan and England (1990).


or delay in their balance beam performance. Moreover, any direct ma- nipulation of attentional capacity produces a corresponding effect on level of functioning on the balance task (Case, 1985, ch. 16).

Although the specifics are quite different, similar findings have been obtained on a version of the Raven Matrices for which training is provided (Wagner, 1981; Case, 1985, p. 201). Four-year-olds can only succeed on matrices where the correct answer can be arrived at by a strategy of perceptual pattern recognition. Six-year-olds can focus their attention on one particular dimension, (e.g., shape) and complete patterns of the form: square A goes with triangle B, square B goes with -? Eight-year-olds can focus on a second dimension and thus succeed on a more standard sort of matrix item such as small square A goes with big square A; small triangle B goes with ---? Finally, progression through this sequence is strongly related to the development of working memory, as assessed by the measures described above.

One more set of results is worth mentioning. On the standard test of concept acquisition (Gholson & Beilin, 1979; Stevenson, 1968), children are presented with a sequence of card pairs, for each of which they must guess which of the two cards is correct. The cards vary in their size, shape, and color, and for any block of trials one particular dimension and value (e.g., shape-triangle) is established as the correct concept by the experimenter and is rewarded. What happens under these conditions is that 4-year-olds tend to focus on the global perceptual properties of the first object that is classified as correct (e.g., a large triangle). They then use these properties as a guide for guessing which stimulus will be correct on subsequent trials, and if they are incorrect they either perseverate on these characteristics or adopt some sort of positional guessing strategy (e.g., the one on the left is always correct).

By contrast, 6-year-olds begin to use their ability to classify along various dimensions to aid them in their hypothesis about which card is correct. Thus, they now focus consistently on the rewarded dimensions (e.g., shape) from the outset and on the particular value along this dimension (e.g., triangle). If they happen to be incorrect in their first hypothesis (or if the underlying rule is changed), they reverse the value of the dimension and start picking the square instead of the triangle. This is of course fine if the experimenter happens to pick this as correct. If he does not, however, it is not a good strategy, and in fact 6-year-olds then do very poorly, as they tend to perseverate on the first dimension.

Finally, by the age of 8, childen show the ability to shift to a totally different dimension (e.g., color) if the first dimension they select yields an inconsistent pattern or if the rule is changed. In the literature on childrens concept acquisition, this latter strategy is referred to as a non- reversal shift (Stevenson, 1968)

A detailed model of the executive control structures that are necessary

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to respond successfully to each of the above three tasks in a flexible fashion has been presented elsewhere (Case, 1985, chap 9). What is important in the present context is (1) all the foregoing tasks require subjects to orchestrate their existing perceptual capabilities, in the presence of feedback, in order to attain a novel goal and (2) the general pattern of development that is obtained in each case is one that parallels the development of childrens working memory. One piece of clinical data is also relevant. This is that the foregoing tasks all utilize materials and task formats which bear a strong resemblance to those used on the Wisconsin Card Sort Test, which is one of the standard clinical markers for frontal lobe dysfunction. Not only are the requirements of the tasks similar to those of the Wisconsin Card Sort, but the age range in which the most rapid improvement is observed on these tasks is similar as well (Chelune & Baer, 1986). There is also a similarity in the form of childrens errors. For example: one of the standard problems for frontal patients on the Wisconsin Card Sort is a dissociation between what they state they will do and what they actually do. In my experience, this is exactly what occurs with young children: Although they may state that they will change the basis of their response, in fact they have great difficulty doing so and often continue to select the same stimulus dimension on later trials as on early ones.

In summary: childrens problems on all the foregoing tests are dual ones, which involve paying attention to one or more new dimensions on the one hand and inhibiting their response to a previously rewarded dimension on the other. These problems are empirically associated with low functioning on the tests of working memory, which were described in the previous section, and which-in addition to sharing these same requirements-are known to correlate with frontal CNV. The problems children exhibit on these tasks when they fail also bear a pronounced resemblance to the difficulties exhibited on the standard marker for frontal lobe functioning by subjects who are either developmentally immature or frontally impaired. Putting these facts together, it seems reasonable to suggest that the wave-like cycle of growth which is observed on these behavioral tasks is dependent on the same underlying set of frontally mediated changes as those which produce the EEG coherence waves that Thatcher has documented.

1.3 Changes in Self-Awareness and Emotional Regulation

The level three function that Stuss ascribes to the frontal lobes is that of metacognition or self-regulation. Interestingly, children have also been found to show substantial improvements on these functions during theis same age range (Biemiller & Meichenbaum, 1989). One way in which these changes are reflected is in childrens increased awareness of their own mental activity when they are shown a videotape of them-


selves in their preschool classrooms. Under these conditions, 4-year-olds can identify themselves (often because they recognize their own clothing!). However, they do not show either the capability or the inclination to suggest what was going on in their minds at the time the videotape was made. By contrast, 6- and S-year olds are capable of providing rich accounts of what they were thinking or planning during the videotaped session, and these accounts correspond quite well to the sorts of spon- taneous verbal comments that they make in other, similar situations (Biemiller & Meichenbaum, 1989; Griffin, 1986).

A parallel set of data have been gathered for emotional awareness and regulation. Four-year-olds show very little understanding of emotions that are related to self-evaluation (such as pride or embarrassment), whereas 6- and 8-year-olds show increasing sophistication in this regard (Griffin, 1989, 1992). In addition, 4-year-olds show relatively little ability to delay gratification (Meichenbaum & Goodman, 1971) or to inhibit emotional expressions of sadness or anger in social situations in which these are deemed inappropriate by their culture. By contrast, 8-year-olds are once again quite sophisticated in this regard (Izard & Malaetesta, 1984). This is also the same age range as the one in which, in studies that have been conducted in the sociohistoric tradition (Diaz, Neal, & Williams 1991), internal speech is believed to assume control over childrens self-regulation. Finally, as Eslinger, Damasio, Dasio, & Grattan have shown (1989; see also Grattan & Eslinger, 1992), developmental lesions in the frontal lobes which are sustained during the 6- to g-year-old period produce decrements in the regulatory function that normally emerges during this age range, as well as in those that normally emerge at subsequent points in development.

Although the above set of data does not come exclusively or even primarily from our own research group, we have attempted to model them using the same approach as we have employed for our models of novel problem solving and to examine their relationship to the data already mentioned (Case, 1991). Our conclusion is that they show the same general pattern of growth during the elementary school years and are dependent on the same underlying processes. Although the evidence is not quite as strong for self-reflection as it is for attention and executive functioning, it seems reasonable to suggest that the cycle of behavioral growth and the cycle of EEG growth are dependent on a similar set of underlying changes, which are frontally mediated.

2. COGNITIVE DEVELOPMENT DURING EARLY CHILDHOOD

As developmental psychologists are all too aware, the age norms that one obtains on most cognitive-developmental measures can be radically altered, either by simplification of the measures or by the addition of some extra complexity. As it happens, a number of measures have been

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designed which tap the same general functions as those which were described in the previous section, but which are less complex and can there- fore be assumed to require a lower level of processing (Craik & Lock- hart, 1972).

2.1 Changes in Attentional Capacity

The steps that are required in order to create a simple measure of working memory are: First, subjects must be asked to execute a simpler operation, whose product would normally be a prerequisite for executing one of the more complex operations that are tapped by measures such as the Counting or Spatial Spans. Next, subjects must be asked to execute a series of highly similar operations and recall the entire string of results that they generated when they did so. In fact, such measures have been created for both numerical and spatial operations. For example, on one such measure subjects were asked to access a series of number names (which of course is a prerequisite for counting). On another, they were asked to place a series of objects in some particular spatial orientation to the background on which they were situated (which is a prerequisite for indicating the spot where a dot is to be found in a spatial grid). Both measures were converted to a standard working memory format: i.e., a format in which several operations were executed in a row, and their products had to be recollected.

The sorts of data that were obtained under these conditions are presented in Fig. 2. In the same figure the EEG data obtained for this age range by Thatcher (in press) and by Matousek and Peterson (1973) are presented. As may be seen, the pattern is once again quite similar across all three sets of data.

Lest these parallels be dismissed as coincidental, it is once again important to mention that data exist which tie performance on simple preschool memory measures such as these more directly to frontal lobe activity. In studies using single cell recording in monkeys, Goldman-Rakic (1989a,b) has demonstrated that the frontal system is essential for per- forming the working memory function on a delayed match to sample task. In a related series of studies, Diamond and her colleagues (1991) have shown that short-term memory measures that are mastered by preschoolers also have a strong frontal implication. Once again, then, it seems reasonable to suggest that the behavioral data and the EEG data show the same general developmental pattern because they are assessing a common underlying set of frontally mediated changes.

2.2 Changes in the Power and Flexibility of Executive Functioning Although the tasks and data are too complex to present in detail, it is

worthwhile to mention that other tests have been created which require


A: EEG: Relative Power [F - T] 5

B: EEG: Coherence [F2 - T6]

C: STM

Age in Years

FIG. 2. (A) Rate of growth of EEG coherence between frontal and temporal lobes during early childhood (FZ-T,). (Source: Thatcher, 1992). (B) Rate of growth of relative EEG power (F-T). [Source: Matousek & Peterson (1973) as reported by Hudspeth & Pribram (1985)]. (C) Rate of growth of working memory for consonants. [Primary source: Bleiker (1991). Secondary sources (for 1st data point (Liu, 1991) for last data point, Dempster

(1978))1.

preschool children to devote their attentional resources to the solution of novel problems. For example, on one such battery, children are presented with a simpler set of balance scale items than those described in the previous section (Case, 1985, chap. 6; Marini & Case, 1989). Once again, the growth curves for these other tasks correspond quite well to Thatchers waves of coherence. There is a rapid improvement from 1 r/2 to 2% years of age and a more gradual continued improvement from ages 2% to 5. The rate of this improvement is also strongly correlated with the rate of improvement in subjects short-term memory (Liu, 1981; Case, 1985, p. 315).

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2.3 Changes in Self-Control and Awareness

A similar pattern may also be found on tests which assess childrens self-awareness and self-regulation during this age range. At about the age of 20 months, children begin to pass the rouge test (Lewis, 1979). This is a test in which a bit of rouge is daubed on their forehead, and they are confronted with the result in a mirror. Prior to the age of about 20 months, children either do not notice the daub of rouge or point to it in the mirror only. By the age of about 20 months, they reach to their own forehead to explore the rouge directly, thus demonstrating that they un- derstand (1) that the image that the mirror shows is only a representation and (2) that what the image represents is their own person. Shortly after this time, children also acquire personal pronouns for referring to themselves and for differentiating themselves from others. Finally, during the period from about 3 to 4 years of age, children begin to show clear signs of referring to themselves with age- and gender-appropriate category la- bels, and of controlling their negative emotions, not because the emotions are socially inappropriate but simply because they dislike the experience (Knopp, 1982).

As Diaz, Neal, and Williams (1991) have pointed out, the foregoing developments are more aptly characterized as self-control than as self- regulation, Nevertheless, the changes represent an important precursor of self regulation, and one that is hierarchically related to it.

2.4 Summary

Each one of the frontal functions that Stuss has isolated on the basis of his work with adult frontal patients has a counterpart in measures that have been administered to young children. For each one of these functions, too, there is evidence of recursive, hierarchical growth, as children move to higher levels of cognitive processing. Finally, for each of these tasks there is some form of evidence+ither direct or indirect-that the frontal lobes are implicated in this growth in some manner. This being the case, it seems reasonable to suggest that the correspondence between the cycles of cognitive development and the cycles of EEG coherence is not coincidental. Rather, it seems likely that the two sets of curves are dependent on a common underlying process, which is frontally mediated.

3. TOWARD AN INTEGRATED MODEL OF NEUROLOGICAL AND PSYCHOLOGICAL DEVELOPMENT

Given the pattern of data that was described in the foregoing sections, the question that naturally emerges concerns the underlying process which generates these patterns and why it generates a wave-like rather than a linear change. One way to address this question is to examine, inde- pendently, the explanations that have been proposed to account for the


cycles of cognitive and EEG growth- then to see if any relationship can be found between them.

3.1 Explanations for Cycles of Cognitive Growth

The most common explanation that has been advanced for the cycles of growth in cognitive development is illustrated in Fig. 3. This is a visual representation proposed by Fischer (1980) for a form of developmental reorganization that a number of authors have documented (Case, 1978, 1985, 1991; Fischer, 1980; Fischer & Ferrar, 1988; Halford, 1982; Moun- oud, 1986)?

What the figure is meant to convey is this: (1) During the period from birth to adulthood, four major stages may be identified in childrens intellectual development, each of which involves a move to a higher level of processing. (2) Transition to each new level of processing takes place as a result of the differentiation, consolidation, and coordination of qualitatively different units from the previous stage (these units are symbolized in the figure by the letters A and B). (3) As children actually enter any new level the following sequence of further changes take place: (i) First, two qualitatively different units are integrated and used to construct some new form of mental unit. (ii) Next, the focus of childrens attention expands, and two or more (potentially conflicting) units of this new sort are differentiated. (iii) Next, as working memory expands further, there is a further expansion in the attentional field, with the result that two or more of the new units can be synthesized into a coherent system (thus potentially overcoming any conflict that may have been present). (iv) Finally, as children become capable of moving from one unit to another in the new system and back in a flexible and principled (reversible) fashion, an overall consolidation of the system takes place. This consolidation prepares the system to function as one of the two fundamental units from which the higher order structures of the next stage will be constructed.

3.2 Comparison of Cycles of Cognitive Growth with Cycles of EEG Growth

Figure 4 compares the cognitive changes that take place during the period from 1.5 to 11 years with the EEG changes that have been documented by Thatcher in the present issue of this journal (for 1.5 to 7 years) and elsewhere (for the period from 7 to 11 years). As may be seen, two formally identical cycles are apparent; in each of which there is a progression from left to bilateral to right hemispheric change. More- over, the match between the cycles of neurological and cognitive devel-

* The particulars of the figure (including the age ranges), differ somewhat from Fischers and derive from my own work.

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REGULATlON OF COGNITIVE DEVELOPMENT 65

:a A 9-11 Right Hemisphere : : : years 7-9 years

5- 6 years

STAGE II

FIG. 4. Visual representation of connections that are being formed among various cortical locations, as judged by data on EEG coherence. [Sources: Thatcher. (in press: 1992)j

opment is quite a close one. For each stage or substage in the developmental cycle, there is a corresponding stage or substage in the EEG cycle. Putting the two sets of changes together, the following tentative characterization may be suggested.

Substage 1: Operational coordination. At the beginning of each major stage, what the EEG data suggest is that new short-distance connections are formed between previously differentiated cortical units controlled by the frontal lobes and units in the left temporal, occipital, and parietal lobes (Thatcher, 1991, 1992). The psychological change is the creation of a new psychological function and/or the creation of a new psychological unit.

Recall that Thatchers use of the term connection is a general one and is meant to include axonal sprouting, synaptogenesis. expansion of existing synaptic terminals, presyn- aptic changes in the amount of neurotransmitter excreted, and changes in postsynaptic response to neurotransmitter. Another possible mechanism which Thatcher mentions (but does not favor) is myelinization.

In this connection. it is worthwhile to note that Halford (in press) has suggested that

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As the reader will no doubt be aware, the primary new function that emerges during the period from 1.5 to 2 years is the symbolic one, i.e., the use of linguistic, gestural, and image-generating capabilities that are already present in rudimentary form, in a voluntary, referential fashion. What may be less well known is that, during the period from 5 to 7 years, a new function emerges as well. In classical Piagetian terms, this function would be termed the logic of functions. One example of this sort of logic has already been mentioned: the one-way, quantitative logic, whose origin lies in the integration of preschoolers causal-analytic and numerical capabilities (Case, 1985). Another example is, in effect, a form of psycho- logic which results from the integration of preschoolers rudimentary theory of mind with their narrative capability: For the first time, events in a socially scripted sequence of behavior are given motivational or plan- based explanations as well as action-based ones (Goldberg, 1992; Bru- chowsky, 1992; McKeough, 1982; Griffin, 1992).

Substage 2:Bifocal coordination. During the second substage, the EEG changes that one begins to see appear to reflect the gradual formation and rotation of longer distance connections between the left frontal lobe and the other lobes and the formation of parallel long-distance connections in the right hemisphere (Thatcher, 1992). The psychological changes that take place include the creation of more complex executive structures for controlling the new functions that emerged during the previous substage and the emergence of voluntary shifts in focus between different exemplars of the new units that have been created (hence the term bifocal). In early childhood, the shifts in focus between 2.5 and 3.5 years of age tend to involve a move from one to two semantic relations or one spatial relation and one verbal relation (Case, 1985). In middle childhood, the shifts tend to involve movement between two psychological or logical dimensions, rather than exclusive focusing on one (recall that this sort of refocusing is required by tests such as the Wisconsin Card Sort).

Substage 3: Elaborated bifocal coordination. The cortical changes that take place during the third substage include the termination of left frontal changes and the formation of shorter distance connections in the right hemisphere. Thatcher (1992) has interpreted these new developments as indicating a differentiation and consolidation of functions that have already been integrated. In fact, this appears to be a good cognitive characterization as well. What happens during this substage, at least from a cognitive point of view, is that the flexibility that emerged at the previous substage is actively drawn upon in order to create well-consolidated and highly

the creation of a new psychological function can be modeled in a PDP framework by a function that maps one existing network onto another. The present analysis seems consistent with this suggestion.


differentiated units at the existing level of processing. Once assembled and consolidated, these new units then set the stage for the next wave of growth, as new short-distance connections are once again formed to the left hemisphere and a new level of processsing is entered.

Although space does not permit its consideration here, there is also considerable evidence that entry into any new level has new affective requirements as well and that the integration that is involved involves not only higher level control over posterior, cognitive structures, but also higher level control of emotional structures, which are very probably subserved by the limbic system (Case, Hayward, Lewis, & Hurst, 1987). Examples of this sort of regulation are provided by Davidson (1992) and Fox (1992).

3.4 In Search of a Metaphor Which Includes Structural and Functional Components

As anyone who is familiar with computer programming is aware, the sort of cyclic recursion that the foregoing description implies could be effected by a change in childrens intellectual software, without the introduction of any changes in hardware whatever. All one would need would be a system which was capable of taking entire programs at one level, once they were formed, and recoding them as single units, then utilizing these units as core elements in higher order programs.

What the neurological data and model suggest, however, and what is further supported by data on the cognitive functioning of other species, is that this is unlikely to be the full story. Rather, a better analogy might be the sort of change that often takes place in a growing industrial organization. As an industrial operation reaches a critical size and complexity (as happens in the final phase of any cycle), it is often the case that-in order to continue to grow and expand-its functions must be differentiated, and a vice president must be appointed to take charge of each. A new president can then be sought, whose primary role is to deal with the demands of coordinating the activities of each division, rather than with the daily demands of running either.

As this switch takes place in a business organization, the enterprise enters a new stage in its industrial life, and some further expansion in the physical units that house the enterprise must often take place as well. New quarters (undoubtedly more modern!) may also have to be found to house the new chief executive, and the new chief executive may also find that she needs to increase her office staff and to install a new communication system to link her office with those of her new vice presidents.

The foregoing set of changes may well constitute an appropriate metaphor to describe the changes that have taken place in the course of human evolution and that are in some sense recapitulated in a dynamic, self-organizing fashion (and with vital experimential input) in the course

68 ROBBIE CASE

of human ontogenesis. One need simply add the suggestions (1) that the space in which the increased executive function is located is the frontal lobes and (2) that every time an expansion takes place in this executive function, such that higher level units can be monitored and directed, it is also necessary to effect a more elaborated system of communication between the seat of the executive function (i.e., the frontal lobes) and the seat of the other, more specialized functions that the organism has developed in its day-to-day interaction with its environment.

The one question that this metaphor leaves unanswered is why the waves of frontal connection should move from left to right, as well as from short to longer distances. Here again, the psychological model may offer a possible explanation. Let us suppose that the requirements for the instrumental sequencing of a new A-B unit are different from those of differentiating and expanding the number of such units that can be considered and assembling them into a coherent system. With this idea in hand, we can make two further suggestions. The first is that the two cerebral hemispheres may be differentially specialized for these two different developmental functions, with the right hemisphere perhaps playing a stronger role in envisioning the functioning of an overall system and differentiating it from the functioning of other systems (Pascual-Leone, personal communication; Thatcher, 1992; Young, 1990). The second is that, since there is a functional dependence of one sort of change on the other, it might be more efficient to have the two functions operate in a recursive, two-stroke, fashion, rather than completely in parallel. Al- though I know of no direct evidence that this is the case, this sort of arrangement would certainly give development a dynamic quality, as the two sorts of changes could play off against and energize each other. And there is increasing evidence that development does have this dynamic property (Lautry, 1991; Thelan & Ulrich, 1991).

4. IMPLICATIONS FOR FURTHER RESEARCH

Although a number of implications of the foregoing developmental model and metaphor could be adduced, three will be considered before concluding.

The first concerns the possibility of cycles of development at other age levels. If the sequence of neurological changes illustrated in Fig. 4 is in fact what underpins the sequence of psychological developments illustrated in Fig. 3, then it follows that additional cycles of frontal EEG growth should be identifiable during each of the age ranges for which additional psychological cycles have been identified: namely, between the ages of 4 and 18 months, on the one hand, and between the ages of 11 and 16-18 years on the other.5 Given that the overall progression of these four cycles

For evidence with regard to the latter of these two periods, see Thatcher (in press).


approximates a normal growth function, it is also quite possible that a further cycle could be identified in the months prior to and immediately preceding birth, on the one hand, and during the years of full maturity on the other.

A second implication is that, if dynamic systems models are necessary to capture the nature of the cortical changes that take place during the preschool and elementary school period (as Thatcher has suggested), it is very probably the case that these sorts of models will be necessary to describe the cognitive changes that take place during these time periods as well. This suggestion is of course congruent with much of Piagets later work (Piaget & Garcia, 1983) as well as with recent work in general systems theory (Van Geert, 1991) and such specific content areas as motor development (Thelan & Ulrich, 1991). Its extension to the field of attentional, executive, and reflexive development thus seems likely to be prom- ising.

A final implication, and the most speculative one, concerns the consequences of asymmetrical frontal lobe injury. If an injury occurs early in development and the damage is to the left frontal lobes, then according to the psychological model, the injury should block subsequent developments that normally occur at the end of the cycle. On the other hand, the reverse would not necessarily follow. Since movement to a new level of development only depends on being able to coordinate two units from the previous level, it could conceivably occur even if the units that were being coordinated were not fully elaborated and differentiated. Thus, right frontal lobe injury might not necessarily block further development of a normal nature in the left frontal lobes. Of course, this argument is pred- icated on two admittedly controversial assumptions, namely (1) that certain psychological functions are differentially localized in the left vs. the right hemispheres, and (2) that these functions might be differentially involved at the beginning and end of the sort of growth cycle that has been postulated by cognitive theorists. Still, as a direction for future research, the possibility seems an intriguing one.

CONCLUSIONS

The present article was originally solicited as a commentary on the papers that were presented by Stuss and Thatcher in the symposium on which the present issue of this journal has been based. As the reader is by now aware, I have strayed rather far from the data that Thatcher and Stuss have presented in my effort to connect them in a sensible fashion.

Ages for these cycles have been suggested by H. White (personal communication). by fitting a mathematical curve to the existing stages and substages and extraplolating it. Data on adult cycles are also currently being analyzed by Thatcher (See Thatcher, in press. for a preliminary description).

70 ROBBIE CASE

Moreover, the account I have offered has been one that deals with the organization and flow of information, which is of course only one of many neurological functions. Still, the reason I have ventured this sort of description will hopefully also be apparent. It seems to me that the work with adult frontal patients and the work on childhood EEG patterns are part of the same general picture, but that we will not be able to grasp the full dimensions of this picture until we look at the data on cognitive development as well and attempt to build a model which somehow en- compasses all three. What I have tried to do in the present paper is to indicate the general sort of data that we will have to look at, and one possible manner in which these data might be organized, if we are to construct a model of frontal growth that has this sort of integrated nature.

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the role of the frontal lobes in the regulation

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