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Documente Profesional
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AND
COGNITION
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.
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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 electrophysiological 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
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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 overcome. 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 testsubjects 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 assessedat least 80 children on one or both of the measures described
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TABLE 1
MEANS AND (STANDARD DEVIATIONS) OF Two DIFFERENT ATTENTIONAL SPAN MEASURES
SCORESFOR AGE GROUPS
Age group
mean (years)
--__4.61 (0.27)
6.62 (0.13)
8.57 (0.17)
10.56 (0.20)
15.10 (Sl)
___-~____Counting
__-.
1.07 (0.15)
2.08 (0.64)
3.13 (0.44)
3.41 (0.47)
3.83 (64)
-.
~__
Span measure
.~
..~.
~-.-.
4 x 4 Matrix
_---.~
0.96 (0.39)
1.95 (0.62)
2.88 (0.79)
359 (1.08)
3.79 (.4X)
45
5.5
61
T 75
Age I Years
85
9.5
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, 4year-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
Hamstra, Benson, Khan and England (1990).
and Pollich
(1985); Pascual-Leone,
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or delay in their balance beam performance. Moreover, any direct manipulation 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 assessedby
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 nonreversal shift (Stevenson, 1968)
A detailed model of the executive control structures that are necessary
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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-
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DEVELOPMENT
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 therefore be assumed to require a lower level of processing (Craik & Lockhart, 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 performing 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
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C: STM
Age in Years
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.
FIG.
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and Awareness
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
PSYCHOLOGICAL DEVELOPMENT
AND
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, independently, the explanations that have been proposed to account for the
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Right
Hemisphere
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:a
A
:: :
9-11
years
7-9
years
STAGE II
5- 6
years
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, presynaptic 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 psychologic 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 planbased explanations as well as action-based ones (Goldberg, 1992; Bruchowsky, 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.
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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. Although 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
(in press).
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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 encompasses 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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