Executive control: balancing stability and flexibility via the duality of evolutionary neuroanatomical trends
ABSTRACT The concept of executive functions has a rich history and remains current despite increased use of other terms, including working memory and cognitive control. Executive functions have sometimes been equated with functions subserved by the frontal cortex, but this adds little clarity, given that we so far lack a comprehensive theory of frontal function. Pending a more complete mechanistic understanding, clinically useful generalizations can help characterize both healthy cognition and multiple varieties of cognitive impairment. This article surveys several hierarchical and autoregulatory control theories, and suggests that the evolutionary cytoarchitectonic trends theory provides a valuable neuroanatomical framework to help organize research on frontal structure-function relations. The theory suggests that paleocortical/ventrolateral and archicortical/dorsomedial trends are associated with neural network flexibility and stability respectively, which comports well with multiple other conceptual distinctions that have been proposed to characterize ventral and dorsal frontal functions, including the "initiation/inhibition," "what/where," and "classification/expectation" hypotheses.
- SourceAvailable from: Randall C. O’Reilly[Show abstract] [Hide abstract]
ABSTRACT: We use a biologically grounded neural network model to investigate the brain mechanisms underlying individual differences specific to the selection and instantiation of representations that exert cognitive control in task switching. Existing computational models of task switching do not focus on individual differences and so cannot explain why task switching abilities are separable from other executive function (EF) abilities (such as response inhibition). We explore hypotheses regarding neural mechanisms underlying the “Shifting-Specific“ and “Common EF“ components of EF proposed in the Unity/Diversity model (Miyake & Friedman, 2012) and similar components in related theoretical frameworks. We do so by adapting a well-developed neural network model of working memory (Prefrontal cortex, Basal ganglia Working Memory or PBWM; Hazy, Frank, & O’Reilly, 2007) to task switching and the Stroop task, and comparing its behavior on those tasks under a variety of individual difference manipulations. Results are consistent with the hypotheses that variation specific to task switching (i.e., Shifting-Specific) may be related to uncontrolled, automatic persistence of goal representations, whereas variation general to multiple EFs (i.e., Common EF) may be related to the strength of PFC representations and their effect on processing in the remainder of the cognitive system. Moreover, increasing signal to noise ratio in PFC, theoretically tied to levels of tonic dopamine and a genetic polymorphism in the COMT gene, reduced Stroop interference but increased switch costs. This stability-flexibility tradeoff provides an explanation for why these two EF components sometimes show opposing correlations with other variables such as attention problems and self-restraint.Neuropsychologia 01/2014; · 3.45 Impact Factor
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ABSTRACT: Sexual dimorphism in the brain and cognition is a topic of widespread interest. Many studies of sex differences have focused on visuospatial and verbal abilities, but few studies have investigated sex differences in executive functions. We examined two key components of executive function - response inhibition and response monitoring - in healthy men (n = 285) and women (n = 346) performing the Stop-signal task. In this task, participants are required to make a key press to a stimulus, unless a tone is presented at some delay following the initial stimulus presentation; on these infrequent trials, participants are instructed to inhibit their planned response. Response inhibition was assessed with an estimate of the latency needed to inhibit a response (stop-signal reaction time), and response monitoring was measured by calculating the degree to which participants adjusted their reaction times based on the immediately preceding trial (e.g., speeding following correct trials and slowing following errors). There were no sex differences in overall accuracy or response inhibition, but women showed greater sensitivity to trial history. Women sped up more than men following correct 'Go' trials, and slowed down more than men following errors. These small but statistically significant effects (Cohen's d = 0.25-0.3) suggest more flexible adjustments in speed-accuracy trade-offs in women and greater cognitive flexibility associated with the responsive control of action.British Journal of Psychology 05/2014; 105(2):254-72. · 2.37 Impact Factor
- Frontiers in Psychology 09/2014; 5:1104. · 2.80 Impact Factor
xecutive functions have enjoyed diverse defin-
itions, but most agree that these functions represent the
pinnacle of phylogenetic and ontogenetic development
within the brain. Many views of executive functions
equate these with the functioning of frontal lobe systems,
but changes in usage over the last few decades reflect
differences in research focus on component processes,
and the perspectives advanced in cognitive psychology
and cognitive neuroscience relative to those that were
the prior focus of clinical neuropsychology and neurol-
ogy. This article provides limited historical perspective,
summarizes several overarching theoretical views of
executive functions, and suggests that it is valuable to
focus on a fundamental functional distinction between
operations supporting stability and flexibility of neural
network activation states and associated cognitive rep-
resentations. This functional distinction is linked to a
fundamental duality in evolutionary cytoarchitectonic
trends that map onto dorsomedial archicortical and ven-
trolateral paleocortical neural systems. This perspective
may help align cognitive neuroscience research with
B a s i c r e s e a r c h
Copyright © 2012 LLS SAS. All rights reservedwww.dialogues-cns.org
Executive control: balancing stability and
flexibility via the duality of evolutionary
Robert M. Bilder, PhD
Keywords: executive function; cognitive control; frontal lobe; working memory;
neuroanatomy; cognition; neuropsychology
Author affiliations: Department of Psychiatry and Biobehavioral Sciences,
UCLA David Geffen School of Medicine, and Department of Psychology, UCLA
College of Letters & Science, Los Angeles, California, USA
Address for correspondence: Robert M. Bilder, PhD, Michael E. Tennenbaum
Family Professor of Psychiatry and Biobehavioral Sciences, David Geffen School
of Medicine at UCLA and Professor of Psychology, UCLA College of Letters &
Science, Room C8-849, 740 Westwood Plaza, Los Angeles, CA 90095, USA
The concept of executive functions has a rich history and
remains current despite increased use of other terms,
including working memory and cognitive control.
Executive functions have sometimes been equated with
functions subserved by the frontal cortex, but this adds lit-
tle clarity, given that we so far lack a comprehensive the-
ory of frontal function. Pending a more complete mecha-
nistic understanding, clinically useful generalizations can
help characterize both healthy cognition and multiple
varieties of cognitive impairment. This article surveys sev-
eral hierarchical and autoregulatory control theories, and
suggests that the evolutionary cytoarchitectonic trends
theory provides a valuable neuroanatomical framework
to help organize research on frontal structure-function
relations. The theory suggests that paleocortical/ventro-
lateral and archicortical/dorsomedial trends are associated
with neural network flexibility and stability respectively,
which comports well with multiple other conceptual dis-
tinctions that have been proposed to characterize ventral
and dorsal frontal functions, including the “initiation/inhi-
bition,” “what/where,” and “classification/expectation”
© 2012, LLS SASDialogues Clin Neurosci. 2012;14:39-47.
functional distinctions that have clearer neuroanatomi-
cal bases, help us understand clinical impairments of
executive control, and ultimately provide new clues to
more effective treatments.
a rose is a rose is a rose; or is it?
The concept of executive functions and the links of these
functions to frontal lobe systems have rich legacies, with
roots dating back to the mid-19th century and continued
widespread use in the modern literature. Some early
uses of the concept are found at least by 1861, when
Gratiolet referred to the frontal lobes as the site of the
“regulating mind” or the “supreme organ of the brain.”1
Luria also credits Broadbent2,3and Jackson4,5with early
development of concepts regarding the importance of
the frontal lobes in the hierarchical regulation of behav-
The actual use of the term “executive function” to refer
to frontal lobe function has been credited to Karl
Pribram, who wrote in 1973: “… the frontal cortex
appears critically involved in implementing executive
programs when these are necessary to maintain brain
organization in the face of insufficient redundancy in
input processing and in the outcomes of behavior”6(p
312). Pribram’s usage here was tied to then-current com-
puter terminology referring to “flexible noticing order
programs” that were applied in the sequencing and
tracking of routines in a context-sensitive manner, and
in this way he distinguished such control processes from
strictly hierarchical programs which are context-free.
The term “working memory” (a coinage attributed to
Miller, Galanter, and Pribram7) developed its own niche
role as one of the components of “executive function.”
This may be attributed at least in part to the widespread
uptake of the term in cognitive psychology following its
use in influential works by Alan Baddeley and col-
leagues.8Many of these cognitive works assiduously
avoided attributions to specific brain mechanisms,
despite knowledge that the frontal lobes were critical for
delayed response task performance.9Later experiments
provided considerably greater detail about the specific
nature of the deficit produced by frontal versus poste-
rior cortical lesions on these behaviors, documenting fir-
ing patterns of prefrontal pyramidal cells during delay
periods, and using selective lesions to reveal the roles of
reciprocal connections between frontal and posterior
cortical regions, the relations of these transmissions to
graded electrical potential changes over relevant corti-
cal or scalp regions (reviewed by Pribram and
McGuinness10,11), and then linking these sustained acti-
vation patterns to specific pharmacological manipula-
tions, particularly of dopamine (DA) neurons.12,13Today
this work has progressed to include biophysically
detailed models of mechanisms responsible for stabiliz-
ing and introducing flexibility into sustained activation
states of these neural networks.14-16
To highlight how construct labels may impact science,
however, it is exemplary to consider what happened to the
term “executive functions” in the project—Measurement
and Treatment Research to Improve Cognition in
Schizophrenia (MATRICS). Considerable research
already had documented impairment on multiple tasks of
executive function, and many reports highlighted the
impairments of executive control as among the most
severe deficits in people with schizophrenia,17-19and
showed that these were important in functional impair-
ment,20leading to hypotheses that developmental dys-
functions affecting frontal lobe systems may be central to
the pathophysiology of schizophrenia.21-25But in consen-
sus meetings and reviews of factor analytic studies it was
determined that the term “reasoning and problem solv-
ing” had the “advantage of distinguishing this domain
from working memory.” 26Armed with these revised con-
cept labels the team identified tests to measure this con-
struct, but some tests upon which the original factor ana-
lytic studies were based were not evaluated further for
various good reasons (eg, the Wisconsin Card Sorting Test
had figured heavily in prior research, but is ill-suited for
application in clinical trials). Then several tests were pro-
posed that had not been used in the factor analyses, and
which are quite reasonably considered tests of “reasoning
and problem solving” but would less likely be selected as
measures of “executive functioning” and almost certainly
would not be selected as measures of “frontal lobe func-
tions.” For example, a maze-processing test was selected
for the MATRICS final battery, even though no maze test
was used in the original factor analytic studies, and while
most scientists would agree that frontal function is impor-
tant for maze performance, the contributions of non-
frontal systems are profound. Thus the construct label
executive functions (associated with frontal system
integrity), was split into working memory and reason-
ing/problem solving, the latter of which was untethered
from its “frontal” system anchor. This highlights how
B a s i c r e s e a r c h
breaking a construct into subcomponents can have unin-
tended consequences, and in general shows that cognitive
construct labels may be misleading. Indeed, it only
becomes clear what the labels really mean when these are
specified with respect to the actual test variables used to
measure the construct. These issues are discussed in
greater detail elsewhere, along with other examples show-
ing how construct labels may reflect fashion more than
science, and calling for routine specification of constructs
at the measurement level.27-29For example, in one litera-
ture-mining exercise the term “cognitive control” was
defined completely at the measurement level by a set of
four other labels including: working memory, response
selection, response inhibition, and task switching/set shift-
ing. Thus, the term “cognitive control” was used increas-
ingly in the literature to describe results from the same
tests that were previously branded with other labels.
By the time Pribram had offered the coinage of execu-
tive functions and participated in the coinage of working
memory, substantial progress had been made in recog-
nizing key aspects of frontal lobe organization based on
both clinical and basic research by Jacobsen, Halstead,
Teuber, Luria, Fuster, Mishkin, Sanides, Stuss, Benson,
and others.1,9,30-40Among these contributions I single out
for its elegance and simplicity the formulation of Luria1,41
as elaborated by Goldberg.42This provides an overall
functional framework within which the processes of
executive function take place. Next I turn to characteri-
zation of the nature of control exerted by the frontal sys-
tems, relying here on formulations articulated by
Pribram and McGuiness,10,11,43Fuster,44and Goldman-
Rakic.45Finally, I attempt to show how the fundamental
principles of frontal executive control mechanisms may
operate to subserve stability and flexibility operations
(which are a critical component particularly of Pribram’s
concept of frontal function) via an anatomic organiza-
tion that has evolved specifically to provide autoregula-
tory control over stability and flexibility, based on the
original work of Friedrich Sanides37as elaborated by
Pandya and his colleagues.46-49
The Luria/Goldberg hierarchical
and gradiental theories
Among the most successful and enduring general theo-
ries of frontal lobe functioning are the hierarchical mod-
els that were developed by Luria in the 1960s and elab-
orated and extended by others, including Joaquin Fuster
and Luria’s student Elkhonon Goldberg. A major
premise of these models is that the frontal lobes are
organized in a hierarchical fashion, which Luria referred
to as primary, secondary, and tertiary divisions of the
frontal cortex. These primary, secondary, and tertiary
divisions approximate the cytoarchitectonic divisions
referring to the primary motor cortex, the premotor cor-
tex, and the prefrontal cortex, respectively. Syndrome
analysis of patients with discrete lesions showed sys-
tematic increases in the complexity of behavioral dis-
ruptions paralleling the cytoarchitectonic progression.
In brief, discrete lesions in the primary motor cortex
cause loss of motor control (paralysis or paresis), at the
level of individual motor units, with relatively little
impact on other non-motor functions, and the dysfunc-
tion is well defined by a somatotopic representation
mapped as a motor homunculus on precentral gyrus. In
contrast, lesions to the premotor regions yield hierar-
chically “higher-order” functional deficits, impacting the
combined activation of units in the primary motor
regions, and preferentially affecting the spatially and
temporally organized sequencing of motor movements;
however, the capacity to execute elementary movements
of individual motor units may be spared. While the
impact of lesions in these premotor or secondary divi-
sions continues to be predominantly motoric in charac-
ter, and maintains elements of somatotopic representa-
tion, the “projective fields” are larger, involving multiple
motor units. Finally, lesions to the prefrontal cortex are
seen as hierarchically higher still, impacting the coordi-
nation of premotor activation and thereby regulating the
organization of complex actions and plans for behavior.
These prefrontal lesions may cause no obvious impact
on motor control at all, and there is no clear relation to
This basic scheme has enormous explanatory power,
and, with some refinements and elaborations, has been
used to help understand wide-ranging lesion effects
including not only elementary and complex motor syn-
dromes, but also diverse deficits in expressive language,
conceptual disorganization, and thought disorder, and
more generally problems in the initiation and regulation
of complex behavior. For example, the classic effects of
ventrolateral prefrontal and premotor lesions on expres-
sive speech (ie, “Broca’s aphasia”) may be more readily
appreciated as breakdowns in the regulation of sequen-
tially organized actions in regions that are somatotopi-
cally mapped to the motor control of the articulatory
Executive control via dual neuroanatomical trends - BilderDialogues in Clinical Neuroscience - Vol 14 .No. 1 .2012
apparatus (mouth, tongue, larynx, and pharynx), and this
system better explains how some (more posterior
frontal) lesions have greater effect on articulatory agility
and buccolingual praxis, while other (more anterior)
lesions leave the motor regulation of speech intact but
nevertheless yield alogia or other higher-order speech
impairments. Goldberg provides many examples, and
also an elegant explanation of how agnosias emerge as
a cardinal consequence of lesions in the secondary divi-
sions of posterior cortical regions, and how analogous
disruptions in the classification of behavioral programs
may result from premotor cortex dysfunction.42
Some difficulties for these theories include: (i) the obser-
vation that the secondary divisions of the cortex (ie, pre-
motor cortex) are actually phylogenetically older and
less differentiated than either tertiary prefrontal cortex
or primary motor cortex, which appear to have evolved
more recently (see refs 50,51); (ii) a lack of specification
about the nature of regulatory influence expressed by
the frontal cortex in its connections to posterior cortical
regions; and (iii) while the hierarchical theories account
well for diverse motor and planning phenomena, they
often pay less attention to the importance of frontal sys-
tems as regulators of the limbic, diencephalic, and brain
stem systems, and thereby offer less insight into how
frontal systems regulate visceral and autonomic function.
The Pribram-McGuiness hypothesis and
other autoregulatory control theories
In his classic paper “The riddle of frontal lobe function
in man,” Hans-Lukas Teuber31highlighted dilemmas
faced by the field in its attempts to identify a unitary the-
ory of frontal lobe functions, and he focused on taking a
“180-degree” shift in thinking by examining the impact
of frontal systems on the rest of the brain including sen-
sory cortices. Teuber’s emphasis on “corollary discharge”
anticipated interpretations that focused on the role of
frontal projections in biasing the processing of other cor-
tical systems to “prepare” for engagement in task-rele-
vant activity, thereby providing representation of “expec-
tation” and “context based on prior memory.” 52These
ideas are similar to later theoretical contributions that
attribute to frontal systems a unique role in guiding
behavior via context.53But Teuber and others also rec-
ognized that part of the “riddle” of frontal function was
likely posed by its structural heterogeneity.54Benson and
others had established a dichotomy widely used in neu-
rology and neuropsychology, distinguishing dorsolateral
from orbitofrontal syndromes, with the former marked
by cognitive inertia, planning and organization problems,
and the latter marked by pseudopsychopathy and disin-
hibitory psychopathology.55Luria distinguished three dis-
tinctive frontal syndromes, with a dorsomedial syndrome
marked by “oneiroid” (dreamy) states, in addition to the
dorsolateral and orbitofrontal/basal variants.1Pribram
had earlier focused on the unique relations of frontal
regions not only with the motor system but further with
the visceral and autonomic nervous system (see discus-
sion in ref 9), and subsequently refined these ideas in a
grand theory of attention regulation.10,11,43,52,56
The Pribram-McGuinness hypothesis states that frontal
systems contribute critically to integrated “arousal” and
“activation” functions that have primary roles in regu-
lating the flexibility and stability of brain activation
states. This conceptualization extended from the early
experiments of Morruzi and Magoun57and their follow-
ers, which revealed a fundamental duality in that elec-
trographic desynchronization and “alerting” responses
could be triggered not only via stimulation of the
ascending reticular activating system (ARAS), but also
by forebrain stimulation. Of particular importance, the
ARAS stimulation resulted in phasic arousal, while the
forebrain stimulation resulted in more enduring tonic
activation. Pribram and McGuinness recognized the
relation of the phasic arousal system to novelty detec-
tion and the orienting response, and of the tonic activa-
tion to maintenance of readiness to respond and the
preparation of other cortical regions to engage in pro-
cessing. An electrocortical representation of this tonic
activation process was observed in the contingent nega-
tive variation (CNV) observed over the vertex in scalp
EEG recordings selectively during the delay interval of
delayed response tests; it was noted further that depth
recordings revealed transcortical negative variations
which occurred within those sensory regions that were
about to be engaged in processing, and that both the
CVN and TNVs could be obliterated by lesions in
frontal or striatal components of the tonic activation sys-
tem, thus confirming a frontal system contribution to
preparation for processing elsewhere in the brain.
Several decades later, elegant experiments by Patricia
Goldman-Rakic and colleagues would corroborate and
extend these studies, revealing the exquisite organiza-
tion of reciprocal fronto-posterior projections and high-
lighting the sustained activity of prefrontal pyramidal
B a s i c r e s e a r c h
neurons in the maintenance of activation states in task-
relevant posterior cortical regions. It was at this point
that the processes of working memory received greater
attention, referring particularly to those elements of
tonic cortical activation previously labeled by Pribram
and McGuinness as activation.
Other distinctions have been put forward to help under-
stand the heterogeneity of frontal lobe function. Fuster
has emphasized the role of more dorsal frontal systems
in initiation of action and the more ventral systems in
the inhibition of action.44,58Following elegant experi-
ments that segregated the “what and where” functions
of ventral and dorsal visual streams, respectively, one
theory suggests this distinction is carried forward in
frontal system function.59A similar theory suggests this
distinction is better characterized as “what versus how.”60
Exploration and exploitation have been seen as a crucial
dichotomy in both business systems and frontal function,
though the anatomic attributions of these models do not
always converge (ie, Cohen and colleagues have sug-
gested that “exploration” is more mediated by fron-
topolar and dorsal systems that are engaged to over-
come prepotent response tendencies).61-63Another recent
review suggested that existing evidence is more consis-
tent with the idea that dorsal frontal systems are associ-
ated with “expectation” while the ventral systems are
more engaged in “classification.” 64Is there a way to rec-
oncile these ostensibly different views of frontal system
The dual evolutionary cytoarchitectonic
It has been said that in biology, function is always dic-
tated by structure (see ref 65), so our understanding of
functional distinctions in brain might best follow an
analysis of its structure. Comparative anatomic studies
going back to the 1930s highlighted a duality in the ori-
gins of the cerebral cortex, with one anatomic source
originating from a laterally positioned cellular pri-
mordium comprising the primitive olfactory cortex (pale-
ocortical trend) and another anatomic source derived
from a medially positioned cellular primordium com-
prising the primitive hippocampal formation (archicorti-
cal trend).66-68In the phylogenetic progression from fish
through reptiles to mammals and primates, this funda-
mental duality has been preserved as the cortex evolved
progressively from three to six layers, with the most
recently evolved representation of the paleocortical trend
apparent in the most ventral and lateral aspects of neo-
cortex, and the most recently evolved representation of
the archicortical trend in the most dorsal and medial
aspects of neocortex.69This duality in origins of the entire
cortical mantle is reflected in both distinctive patterns of
local cytoarchitectonic development and long-range pat-
terns of connectivity in both posterior and frontal
regions. The posterior paleocortical progression includes
parainsular cortex, from which further development of
six layered isocortex emphasized granular cells and led
to development of the primary sensory areas for the face,
head, and neck, and to the central visual component of
primary visual cortex, and to primary auditory cortex.
The archicortical progression includes paralimbic cortex,
from which isocortical developments included an empha-
sis on pyramidal cells and somatosensory representations
of the limbs and trunk, and to cortical regions represent-
ing the peripheral visual fields. In frontal regions70there
is a similar duality expressed in the elaboration of gran-
ular and pyramidal cells in the paleocortical and archicor-
tical trends, respectively, and a parallel emphasis on the
trends’ respective representations of motor control of the
face/head/neck versus limbs and trunk. Linking these
observations to the theories described above, the hierar-
chical view is reinforced by the documented short-range
projections from each region to nearby regions of both
greater and lesser degrees of differentiation. Reinforcing
the topographically organized patterns of frontoposte-
rior projections described above, it is further important
to note that these patterns of long-range projections
honor the level of cytoarchitectonic differentiation across
comparable anterior and posterior developments within
each trend, and also connect similarly evolved regions
between paleocortical and archicortical trends. These
relationships have been summarized elsewhere,71,72and
are further detailed and depicted elegantly in multiple
works by Pandya and colleagues (for a recent update, see
Several functional distinctions map either explicitly or
implicitly onto this neuroanatomical duality (Table I).
For example, the paleocortical and archicortical trends
have been seen as the potential substrate of object ver-
sus spatial processing, respectively,46following the “what
versus where” distinction noted above. Randall
O’Reilly73argues that this distinction may better be
broadened to consider “what versus how” processing,
similar to the hypothesis of Goodale and Milner.60
Executive control via dual neuroanatomical trends - Bilder Dialogues in Clinical Neuroscience - Vol 14 .No. 1 .2012
Petrides sees the dorsolateral (archicortical) system as
more critically engaged in “monitoring of information in
working memory” while the ventrolateral (paleocorti-
cal) system is more involved in “…active judgments on
information held in posterior cortical association regions
that are necessary for active retrieval and encoding of
information…” (p 793).74Gary Goldberg suggested that
the paleocortical system mediates “responsive” control
over action, while the archicortical system mediates
“projectional” control over action,75and this idea is
highly compatible with the distinction that Frith and
Done76made between “stimulus intentions” and “willed
intentions” in describing two distinct routes to action
(which incidentally can help explain both unusual phe-
nomena such as the “alien hand sign” seen rarely with
lesions to the archicortical divisions of the premotor sys-
tem, and certain hallucinatory behavior in syndromes
like schizophrenia). Further compatible with these views
is the recent hypothesis of Borst and colleagues, sug-
gesting that the dorsal/ventral distinction in frontal func-
tion is best captured by dimensions of “expectation” ver-
sus “classification.” 64
Key elements from each of these suggestions should
probably be accounted for in a mature model of frontal
lobe function. In prior work it was suggested that inte-
grating the evolutionary cytoarchitectonic trends model
with the Pribram and McGuinness theory of attentional
control might have merit.70,71,77-83Specifically, it has been
argued that the dorsal and medial archicortical systems
may emphasize the stabilization of behavioral programs,
thus subserving what Pribram and McGuinness referred
to as “tonic activation”—and this would be consistent
particularly with roles in mediating “projectional con-
trol,” “willed intentions,” “monitoring of information in
working memory,” and “expectation” as invoked above.
In contrast, it was suggested that the ventral and lateral
paleocortical system is biased towards flexibility and is
engaged in mediation and moderation of “phasic
arousal”—and this would be compatible with the ideas
espoused above regarding “responsive control,” “stimu-
lus intentions,” and elements of “retrieval and encoding”
particularly those that demand or are triggered by per-
ceptual “classification” processes. This functional dis-
tinction is also likely linked to both neurochemical dis-
tinctions and differences in cellular signaling pathways
that are under strong genetic regulation. For example,
this distinction between maintaining the stability
(through tonic dopaminergic activation) or introducing
more flexibility (through phasic dopaminergic arousal)
in corticostriatal networks was seen as a key mechanism
through which genetic variation in the catechol-O-
methyltransferase (COMT) gene may impact diverse
cognitive functions.83The putative identification of these
features and characteristics with paleocortical and
archicortical trends is summarized in Table I.
Modern neuroimaging studies, particularly those using
functional magnetic resonance imaging (fMRI), have
B a s i c r e s e a r c h
Derivative from primordial cellular moiety
Intermediate (allocortical and periallocortical) representation
Neocortical representation in frontal lobes
Route to action
Relations to visual streams and posterior cortical processing
Relation to memory and working memory processes
Ventrolateral and orbitofrontal cortex
Face, head, neck
Promote active retrieval and encoding
Medial and dorsal frontal cortex
Promote maintenance and
monitoring of working memory
Orientation with respect to input-output processing
Information processing bias
Mode of dopaminergic transmission
Table I. Summary of neuroanatomical progressions within paleocortical and archicortical trends and their putative functional characteristics.
already produced an enormous amount of evidence that
remains to be well integrated with our understanding of
connectional anatomy and with functional anatomic
hypotheses that are constrained by structural anatomic
architecture. It is hoped that data emerging from the
human connectome project will help advance applica-
tion of these anatomic constraints to functional models.84
Surging interest in the “default mode network”85may
also help by increasing understanding of functional net-
work activation free of the constraints of specific cogni-
tive hypotheses that may lead to reification of certain
functional networks because these are dictated by the
experiments. In the same way that genome-wide associ-
ation studies may provide an “agnostic” and unbiased
approach to the study of genetic association, future stud-
ies of brain activation may benefit from adopting a “cog-
nome-wide” strategy that samples brain function
broadly, and with fewer preconceptions.86Meanwhile, the
field is witnessing a burgeoning of intriguing new “mod-
ular” hypotheses about frontal regions and their puta-
tive roles in mediating discrete cognitive operations.87
Some aspects of these new theories already appear con-
sistent with the evolutionary cytoarchitectonic trends
hypotheses (for example the role of frontal pole region
10 as reflecting a merger zone with influences on both
dorsal and ventral trends), but a high future priority will
be fuller integration of current concepts of reward-sys-
tem function with cognitive process hypotheses.
Research that will enhance understanding of functional
links between frontal systems and deeper limbic, sub-
cortical and axial systems may be among the most
promising directions, and may help to fulfill the legacies
seeded more than 50 years ago by the pioneers of frontal
lobe territories. ❏
Acknowledgements: Preparation of this article was supported by the
Michael E. Tennenbaum Family Center for the Biology of Creativity, and
the Consortium for Neuropsychiatric Phenomics (NIH Roadmap for
Medical Research grants UL1-DE019580). I also thank William Barr and
Elkhonon Goldberg for historical notes and comments.
Executive control via dual neuroanatomical trends - BilderDialogues in Clinical Neuroscience - Vol 14 .No. 1 .2012
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estabilidad y flexibilidad a través de la
dualidad de las tendencias neuroanatómicas
El concepto de funciones ejecutivas tiene una rica
historia y se mantiene vigente a pesar del incre-
mento del empleo de otros términos, incluyendo los
de memoria de trabajo y control cognitivo. Las fun-
ciones ejecutivas algunas veces se han identificado
con funciones dependientes de la corteza frontal,
pero esto no aclara mucho, dado que a la fecha se
carece de una teoría comprensible de la función
frontal. Mientras se espera una comprensión meca-
nicista más completa, las generalizaciones de utili-
dad clínica pueden ayudar a caracterizar tanto la
cognición normal como múltiples variedades del
deterioro cognitivo. Este artículo revisa algunas teo-
rías que incluyen el control jerárquico y la autorre-
gulación, y sugiere que las tendencias de las teorías
evolutivas de la citoarquitectura aportan un valioso
soporte neuroanatómico para ayudar a organizar
la investigación de las relaciones entre función y
estructura frontal. La teoría sugiere que las vías
paleocortical/ventrolateral y arquicortical/dorso-
medial están asociadas con la flexibilidad y la esta-
bilidad de la red neural respectivamente, lo que
concuerda bastante con otras múltiples distinciones
conceptuales que se han propuesto para caracteri-
zar las funciones frontales ventral y dorsal, inclu-
yendo las hipótesis de “inicio/inhibición”,
“qué/dónde” y “clasificación/expectación”.
Contrôle exécutif : équilibre entre stabilité
et flexibilité via la dualité des tendances
Le concept de fonctions exécutives a une histoire
riche et reste actuel malgré l’utilisation accrue
d’autres termes, comme la mémoire de travail et le
contrôle cognitif. Les fonctions exécutives ont par-
fois été assimilées aux fonctions favorisées par le
cortex frontal, ce qui éclaire peu le sujet, car nous
manquons jusqu’à maintenant d’une théorie com-
plète de la fonction frontale. Dans l’attente d’une
compréhension mécaniste plus complète, des géné-
ralisations cliniquement utiles peuvent aider à
caractériser à la fois une cognition saine et des
variétés multiples de déficits cognitifs. Cet article
passe en revue plusieurs théories de contrôle hié-
rarchique et d’autorégulation, et suggère que la
théorie des tendances cytoarchitectoniques évolu-
tionistes apporte un cadre neuroanatomique très
utile pour aider l’organisation de la recherche des
relations structure-fonction frontales. La théorie
suggère que des tendances paléocorticales/ventro-
latérales et archicorticales/dorsomédiales sont asso-
ciées respectivement à la stabilité et à la flexibilité
du réseau neuronal, ce qui concorde avec de nom-
breuses autres distinctions conceptuelles proposées
pour caractériser les fonctions frontales dorsales et
ventrales, comme les hypothèses d’« initiation/inhi-
bition », de « quoi/où », et de « classification/anti-
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