The Frontal Lobes Revisited

Ellen Perecman

• Publisher: Psychology Press
• Year: 2019
• ISBN:
  9781317728115
• Edition: 1
• Topic: Psychology
• Subtopic: History & Theory in Psychology
• Index: Psychology

Experts in neuropsychology examine key issues in research involving the frontal lobes.

1
Consciousness and the Meta-Functions of the Frontal Lobes: Setting the Stage

Ellen Perecman

Introduction

The frontal lobes of the brain are presumed to be involved in the highest level of goal-directed acts including complex sequencing, the creation of long-and short-term plans, and the internal manipulation of representational systems. They have, furthermore, come to be associated with behaviors that are bound up with consciousness and its manifestations: self-awareness, self-regulation, intentionality, etc. Indeed, Luria (1973) argued that the frontal lobes play a fundamental role in constructing and maintaining human conscious activity.

Consistent with this notion of the frontal lobes as the "seat of consciousness" is the fact that they are most recent in the phylogenetic development of the brain; they are hardly visible in lower animals, are considerably larger in primates, and occupy up to one-fourth of the total mass of the cerebral hemispheres in man. Moreover, on the ontogenetic time scale, the frontal lobes do not mature until a child is between 4 and 7 years old (Luria, 1973, p. 183).

Clinical as well as experimental studies of focal brain damage have indicated that a lesion in the prefrontal cortex of humans (Milner, 1964, 1971), as well as monkeys (Fuster, 1980) and rats (Kesner, 1985), results in a number of intellectual and behavioral deficits. Thus, changes in social behavior, affect, and behavioral initiative and spontaneity are associated with damage to the orbitofrontal region, while disorders of cognitive function, such as memory for the temporal sequence of events, spatial orientation, and poor control of movement, are typically seen with dorsolateral lesions.

Note that each of the functions in question refers not to a particular behavior per se, but to the regulation of that behavior, to the integration of that specific behavior into some larger scheme of behavior. This is not surprising in view of the extensive connections of the frontal cortex with subcortical and cortical sensory, motor, and limbic systems.

In the present volume, Deepak Pandya and Clifford Barnes (Chapter 3) focus on the connectional relation of the frontal lobes with other areas of the brain. They set out to elucidate the afferent and efferent connections of the monkey frontal lobe with other cortical and subcortical regions, as an "indispensable prerequisite to any consideration of frontal lobe function," explaining how, in addition to limbic, thalamic, and hypothalamic input to the frontal lobe, successive parasensory association areas for all three major modalities of sensation send projections progressively to premotor, prefrontal, orbital, and medial cortices of the frontal lobe. They also identify an anatomical convergence of different sensory afférents in the frontal lobe that may be the basis for intermodal and cross-modal exchange of information. It is in fact such delineation of the connectional anatomy which has led to the conclusion that the frontal cortex "constitutes an essential anatomic substrate for functional unification of the higher mental processes" (Thatcher & John, 1977, p. 24).

An Overview

Spatial Processing and the Frontal Lobes

In Chapter 4, John Stamm offers a historical review of research on frontal lobe function in monkeys, cats, and dogs, using delayed-response (DR) and delayed-alternation (DA) tasks. He discusses experimental work that supports the view that kinesthetic cues are important in guiding delayed-alternation responses and in identifying two distinct forms of behavioral impairment: (1) spatial response differentiation in the absence of exteroceptive cues and (2) inhibition of interfering response tendencies. Stamm concludes that principalis cortex plays a role in the formation of self-regulating kinesthetic processes that guide its subsequent choice responses, and that the solution to the riddle of the monkey's delayed-response deficit lies in the principalis cortex.

Karl Pribram (Chapter 2) questions the kinesthetic hypothesis as the basis for the spatial aspect of the frontal deficit, suggesting instead that kinesthetic cues relate more to the temporal than to the spatial deficit that follows anterior frontal lesions and that the difficulty with "spatial" problems is due to an increase in sensitivity to distraction under certain specifiable conditions.

Pribram distinguishes between lesions that interfere with classic delay tasks and lesions that interfere with object alternation. He identifies a gradient of relationships of delay problem performance in sensory mode reaching from a periarcuate auditory and visual to a more anterior kinesthetic location and argues that "these relationships fit with the general hypothesis that the function of the anterior frontal cortex is to relate the processes served by the limbic forebrain to those of the somatosensory motor systems."

It is precisely the role of sensory modality in delineating zones within the periarcuate region which is the focus of Chapter 5 by Michael Petrides. Petrides reviews work on the effects on conditional learning in spatial tasks of selective lesions of the periarcuate region in humans and nonhuman primates that shows the degree to which this region may be divided into anatomically distinct zones mediating conditional responses as a function of the sensory modality through which stimuli are presented and the type of responses that must be produced. Petrides reviews experiments on conditional learning and presents an explanation for why monkeys with periarcuate lesions will often perform normally on many of the tasks used in these studies.

Temporal Integration and the Frontal Lobes

Joaquin Fuster (Chapter 6) focuses on the role of the prefrontal cortex in temporal processing. He argues that the three cognitive functions assigned to various parts of the prefrontal cortex, namely, short-term memory, anticipatory preparation for action, and inhibition or control of interference, all subserve a superordinate function essential for the organization of goal-directed behavior in the temporal domain: the "mediation of cross-temporal contingencies," or "the structuring of behavioral actions on the basis of temporally separate but mutually contingent items of information."

This chapter reviews evidence from single-unit studies that substantial numbers of cells in prefrontal cortex are attuned to two or more events in a task, and that cells with widely different properties may be seen in close proximity to each other. Fuster points out that short-term memory is temporally retrospective while preparatory set is prospective, and that delay tasks involve a need to bridge the time between interdependent events. He concludes that neurons of the prefrontal cortex participate in that supraordinate function.

In experimental studies, one often loses sight of the fact that the data collected are only as interpretable as the parameters of the task administered. In other words, if task parameters are ambiguous, results are at best uninterpretable and at worst misleading. In the present volume, this issue is addressed explicitly by Pribram (Chapter 2) and implicitly by Paul Wang (Chapter 10).

Pribram reviews the experimental literature on the frontal lobes with particular attention to overcoming the lack of uniformity in terminology used to refer to particular lesions, and to an analysis of the tasks used to isolate frontal lobe function. He then goes on to reinterpret research findings in light of his reanalysis of the tasks themselves. He proposes, for example, that one can resolve the apparent inconsistency in the finding that limbic resections impair recognition memory, though it is the parietal convexity that has always been associated with agnosia, if one reinterprets the delay task to test for novelty/familiarity, not object identification.

In Chapter 10, Wang presents a critical review of tests created for the purpose of evaluating concept formation. After analyzing the Halstead Category Test, the Wisconsin Card Sorting Test and the Modified Vygotsky Concept Formation Test, he isolates four factors common to all of these. Each tests (1) the ability to apply varied and pertinent solutions based on confined but implicit information, (2) the ability to create hypotheses in accordance with feedback, (3) the ability to maintain a set and avoid erratic responses, and (4) the ability to recognize changes of condition and flexibility in thinking in order to shift response approach. On the basis of this analysis, Wang proceeds to outline his notion of the optimal test for frontal lobe dysfunction.

The evolutionary school of behavioral neurology is rather well represented in this volume. Pandya and Barnes (Chapter 3) point out that classic cytoarchitectonics does not provide any theoretical framework for understanding the pattern or organization of the frontal lobes, and suggest that a productive theoretical framework is found in the evolutionary model of cerebral morphology proposed by Sanides (1971, 1972).

According to Sanides's theory, the six-layered isocortex ultimately has a dual origin in the hippocampal formation, for the spatial analysis of information, and in the olfactory cortex, concerned with the emotional tone of sensory information. Pandya and Barnes describe the patterns of connections which suggest that a given cortical region within each of these two trends projects both to an architectonically less well-differentiated area and to a region with more developed cortical laminar organization.

Pandya and Barnes speculate that each further differentiation in cytoarchitecture and each new set of connections "might reasonably be expected to subserve a new and more advanced behavior." These authors share with Jason Brown, Gary Goldberg, and Elkhonon Goldberg and Robert Bilder a concept of the process of a behavioral act in which each stage in the generation of the behavior contributes to the definition of that behavior and, in this particular case, that "by virtue of the interconnectivity among these units, each would contribute a part that would ultimately affect the motor cortex and result in the properly planned behavior."

Brown has explored this concept extensively in the domain of language (Brown, 1977, 1982; see also Brown and Perecman, 1986) and visual perception (Brown, 1983). In Chapter 14 of this volume, he applies the concept to action.

Action and the Frontal Lobes

In a chapter on the contribution of the frontal lobes to the microtemporal processing—the microgenesis—of action, Brown proposes that the action system develops out of a rhythmic configuration that is bilaterally represented at early stages and becomes gradually biased to left hemisphere representation. Brown takes as his premise the idea that perception and action systems are interrelated ("exteriorize together"), arguing that just as "early stages in object formation [perception] provide the contextual background out of which objects develop and persist abstractly as levels of conceptual or symbolic content within the object itself . . . early stages in action elaborate the instinctual and affective bases that drive the action forward to its goal." For him, conscious awareness develops with the action (or perception) itself and is not superimposed upon the action development.

He characterizes the motor envelope of an action as an early processing stage that elaborates an archaic stage in speech and motility, centered on the space about the body axis and linked to respiratory, locomotor, and other rhythmic automatisms close to motivational and drive-like states.

Brown develops the argument that in the case of action development the evolutionary progression from limbic to motor cortices retraces the sequence of processing stages in the microtemporal elaboration of an action and that disruption at successive points gives rise to symptoms which reflect this progression.

The notion that pathological symptoms identify different levels of representation within a neurocognitive hierarchy is central to the chapter by E. Goldberg and Bilder on motor perseveration. These authors argue that prefrontal pathology may lead to the disintegration of hierarchic relations among representational levels, and that different types of perseveration mark the different levels of representation. They suggest, however, that focal prefrontal damage is not necessary to produce "executive syndrome" and that this syndrome may be relatively common with global cerebral deterioration, in view of the fact that any diffuse brain dysfunction affecting much of the brain to an equal extent from structural and/or from biochemical points of view will disrupt executive functions before it will disrupt other functions.

They point out that while various focal nonfrontal syndromes may lead to perseverative behavior, perseveration in these cases is usually limited to a specific sensory modality or type of behavior. In cases of massive prefrontal pathology, "perseveration is more ubiquitous, permeating virtually every cognitive domain and manifest at every level of the neurocognitive hierarchy." The levels they isolate are (1) a level of selection of a general cognitive mode, (2) a level of retrieval from semantic store, (3) a level of execution of individual task items, and (4) a level of elementary or motor operations.

The role of frontal lobe systems in the organization of action is treated from yet another perspective in Chapter 15, where Gary Goldberg addresses the issue of the relation between intention and expressed action. Goldberg proposes the "dual premotor systems hypothesis": that there are at least two frontal premotor systems, a lateral and a medial system, and that each corresponds to a distinct evolutionary trend in frontal lobe differentiation over phylogeny. The lateral system controls action which is triggered in direct response to external information, and the medial system is used for the prospective control of behavior.

Goldberg presents data on the "alien hand sign" to illustrate his point that a range of clinical and basic physiological observations may be understood in the context of the dual premotor systems hypothesis. He suggests that, in patients with medial frontal infarcts whose symptoms are in the hand opposite the lesion, purposeful action is occurring independent of conscious volition. Patients report unambiguous identification of one hand as alien and the other as the force used to control the alien hand.

Goldberg believes that volitional control is limited to proximal limb musculature. He interprets these "wayward" behaviors as resulting from unconstrained action of the lateral premotor system of the damaged hemisphere, though limited volitional control occurs through activation of the medial system of an intact ipsilateral hemisphere.

The Frontal Lobes and Memory

Donald Stuss and D. Frank Benson (Chapter 8) point out that one of the earliest theories attempting to explain behavioral deficits in animals with frontal lobe lesions attributed the deficit to loss of recent memory, and that in fact the role of frontal lobes in memory remains a controversial issue. Kesner (1985) suggests that the role of the prefrontal co...

Table of contents

• Cover
• Half Title
• Title
• Copyright
• Dedication
• Contents
• Contributors
• Preface
• 1 Consciousness and the Meta-Functions of the Frontal Lobes: Setting the Stage
• 2 The Subdivisions of the Frontal Cortex Revisited
• 3 Architecture and Connections of the Frontal Lobe
• 4 The Riddle of the Monkey’s Delayed-Response Deficit Has Been Solved
• 5 Conditional Learning and the Primate Frontal Cortex
• 6 Single-Unit Studies of the Prefrontal Cortex
• 7 The Midline Frontolimbic Cortex and the Evolution of Crying and Laughter
• 8 The Frontal Lobes and Control of Cognition and Memory
• 9 The Frontal Lobes and Hierarchical Organization of Cognitive Control
• 10 Concept Formation and Frontal Lobe Function: The Search for a Clinical Frontal Lobe Test
• 11 Frontal Lobe Dysfunction in Obsessive-Compulsive Disorder
• 12 Regulatory Function of the Frontal Lobes: A Neurolinguistic Perspective
• 13 The Supplementary Motor Region and Speech
• 14 The Microstructure of Action
• 15 From Intent to Action: Evolution and Function of the Premotor Systems of the Frontal Lobe
• Index