8/13/2019 K. Pribram T-192

1/25

Social amd IEmotiomal Be CIWegunlantiomaDON M. PH A N LU U ,h A N D K A R L H. PRIBRAMd.'bPsychology Departmenr

Univers ity of O regonand

Electrical G eodesics, lnc .Eugene, Oregon

dRadford UniversityRadford, Virginia

Stanford UniversityStanford, California

The assumption of some form of frontal dysfunction in emotional disorder haslong been im portant in psy chiatry. In the Un ited S tates during the 1940s and 1950s,this assumption led to many thousands of frontal lobotomies, leukotomies, andtracto tom ies for the treatm ent of affective and psychological dysfunctions.'. ' Yetit was clear at the time that the scientific evidence relating these deliberate frontallesions to psychiatric sym ptom s was thin at best. ' T he rationale was that psyc ho-surgery treated the psych otic proce ss by disrupting the fixed pathological idea-t i ~ n . ' . ~n fact. however, although orbital frontal and anterior cingulate lesionsreliably decreased the sym ptom s of anxiety and depressio n, the clinical outcom estudies of this era show ed con sistently that the psychotic disorder of schizophre nicpatients was unchanged by the p r o c e d ~ r e . ~In Sweden, physicians evaluated the effects of lobotomy by talking with thepatients' family members. The damage to personality was clear.The wife of patient 2 say s, Doctor, you have given me a new husband. Heisn't the same man. Th e mother of patient 4 declares, She is my daughterbut yet a different person. She is with me in body but her soul is in someway lost. Those d eep feelings, the tendernesses a re gone. She is hard, some-how. The brother of patient 3, a clergyman , states that her personality isaltered; her interests, her outlook on life, her behavior, are different. I havelost my husband. I'm alone . 1 must take over all responsibilities now , say sthe wife of a schoolteacher. I'm living with another person, say s the friendof patient 7. She is shallow in some way. ' (p. 695)

With naturally occurring frontal lesions, such as from stroke or head injury.the psychosocial deficits are often u napprec iated by clinicians until they hav e ledto major failures in occ up ation al and social adjustmen t. Fo r exa m ple, one patientappeared to ha ve been a m odel citizen prior to sustaining a ventromedial frontalinjury.' After the injury, although this patient scored well abo ve aver age on stan -dard tests of intelligence, he soon lost his job , his mon ey, and his marriage.

This work was supported by NlMH research grants MH42128 and MH42669 to theUniversity of Oregon and small business innovation research grants MH50409 and MH5 1069to Electrical Geodesics, Inc.Address correspondence to Don M. Tucker, Ph.D., Psychology Department, Universityof Oregon, Eugene, OR 97403.

8/13/2019 K. Pribram T-192

2/25

2 4 NN LS NEW YORK C DEMY OF SCIENCES

An effective theory of human frontal lobe function must be able to explain thecomplex psychological and social skills that are impaired in such patients. Thelevel of psychological description must go beyond the familiar concepts of cogni-tive neuroscience, such as spatial attention or working memory, and enter thedomain of personality. On the other hand, the theoretical challenge at the neurallevel is to go beyond labeling the functions of the frontal lobe to formulate thekey neurophysiological mechanisms. These mechanisms link the operations offrontal cortex to the multiple systems of the brain's control hierarchy, rangingfrom the control of arousal by brain-stem projection systems to the control ofmemory by reentrant corticolimbic interactions. When sufficiently understood,lhese mechanisms must be found to regulate not only the physiology of neuraltissue, but the representation and maintenance of the self.

In this paper, we consider the social and emotional functions of the frontallobe in terms of three anatomical dimensions. The first might be described as thevertical dimension because it emphasizes the integration of the lower func-tions-brain stem and limbic-with the highest operations-cognitive and motorplanning-of the frontal neocortex. For this dimension, we provide a brief over-view of theoretical approaches to vertical integration. Frontal lesions may disruptself-regulation at the most elementary level by impairing the capacity to engageand maintain adequate levels of activation and arousal in service of long-rangegoals. At more complex levels, the adaptive control of frontal lobe contributionsto attention and memory may be traced to the limbic networks that form theadaptive base for the operations of frontal neocortex.The second dimension examines the functional differentiation between the dor-sal and ventral anatomical pathways linking frontal cortex to the limbic structures,I-eflecting he dual origins of frontal cortex in the archicortical and paleocorticaldivisions of paralimbic cortex. We consider the differing clinical syndromes result-ing from lesions to these pathways. Dorsomedial lesions may le2d to apathy anda loss of initiative. Orbital (ventral) lesions may be more likely to lead to behavioraldisinhibition. We interpret these syndromes in terms of a theory of.differing moti-vational biases that shape the differential forms of motor control emerging in thedorsal and ventral pathways.The third anatomical dimension is lateral, reflecting hemispheric specializationfor emotion. We review the increasing evidence that the left and right frontal lobescontribute differently to emotional self-regulation. This evidence includes not onlybrain lesion studies, but brain function studies with both normal and psychiatricsubjects using EEG cerebral blood flow, and cerebral metabolism measures. Therecent blood flow studies are particularly important haddressing the key theoreti-cal issue of whether the emotional effect of a hemispheric lesion results from theilisinhibition of the opposite hemisphere, or the disinhibition of the ipsilaterals~lhcortical tructures.Although these three dimensions may seem to divide the frontal lobes alongxparate axes, they are not necessarily independent. The dorsal and ventral path-ways may incarporate different forms of activation and arousal control, leading

8/13/2019 K. Pribram T-192

3/25

TUCKER et al.: SELF REGULATION 215ventral corticolimbic pathways within each hemisphere, leading to different pat-terns of frontolimbic interaction on the two sides of the brain.

CONCEPTS OF VERTICAL INTEGRATION

To frame the problem of self-control in terms of the relevant neurophysiologicalsystems is to face the theoretical problem of vertical integration. This is the prob-lem of functionally coordinating the multiple levels of the vertebrate neural hier-archy, from brain stem through midbrain, striatal, and limbic to the extensiveparalimbic and neocortical network^ ^ The frontal cortex appears able to recruitthe multiple levels of the hierarchy in support of extended, goal-directed behavior.Whereas the perceptual systems of the posterior cortex are dedicated to representational operations, developing the internal model of the environmental contextwithin each sensory modality, the networks of the frontal cortex are uniquelysuited to achieve regulatory operations, linking the multiple levels of the neuralhierarchy in service of effectively motivated action^ ^ In the human brain, theextensive frontal cortex also provides representational capacity-working mem-ory-that is dedicated not just to the representation of the sensory context, butto a complex and flexible organization of the regulatory functions across the neuralhierarchy. In this sense, the working memory of the frontal lobe could be describedas the representation of the regulatory process. The most basic level of the regula-tory process is the control of arousal.I0

Self Regulation through Activation and ArousalObservations of frontal-lesioned patients have suggested that frontal cortex

plays an integral role in the self-regulation of arousal in light of behavioral de-mands. Mechanisms of this control may include both influences on brain-stemneuromodulator projection systems and frontal regulation of nonspecific thalamicprojections.

Psychological concepts of arousal have typically considered autonomic signsas the critical c o m p ~ n e n t . ' ~ . ~ ~he concept of the brain-stem reticular activatingsystem was important in moving beyond the nineteenth century notion of arousalas a visceral mechanism, in order to consider neural mechanisms that regulatealertness as a function of both external and internal events.I5 However, even whenframed within neurophysiological terms, a unidimensional construct of arousalhas proven inadequate to account for the range of specific controls on the activityand attentional capacity of the brain. An important theoretical challenge has beento find concepts that bridge between the control of level of neural activity andthe control of qualitative features of attention and memory.

Pribram and McGuinnes~'~ifferentiated between an arousal system, centeredon the amygdala, that responds in a phasic fashion to changes in stimulus .inputand an activarion system, centered on the basal ganglia, that maintains the motorcircuitry in preparation for action. In addition, an effort system regulated by thehippocampus was proposed to coordinate between arousal and activation.

8/13/2019 K. Pribram T-192

4/25

2 6 NN LS NEW YORK C DEMY OF SCIENCES

Building upon this formulation, Tucker and Williamson theorized how qualita-tive changes in attention could be produced by brain-stem neuromodulator sys-tems regulating activation and arousal. Operating to apply a redundancy bias onworking memory, the dopaminergic activation system routinizes actions and fo-cuses attention. Operating under an opposite control system principle, a habitua-r i o t bias the noradrenergic arousal system allocates attention to a broad arrayof novel events, leading to an expansive, holistic perceptual mode.Although these models remain controversial, they provide ways of understand-ing how elementary neurophysiological mechanisms could have fundamental psy-chological roles for the self-regulation not only of attention and cognition, but ofpersonality. For example, a person who relies strongly on the phasic arousalsystem for self-control would be strongly regulated by external events. A childwith this dominant mode of arousal control may be described as having an attentiondeficit. An adult whose personality was dominated by this mode m y be de-scribed as extraverted.I7The frontal lobe may fine-tune these qualitative controls on attention in accor-dance with ongoing adaptive demands. For example, lesions of the right frontallobe may result in particularly severe cases of the neglect syndrome, in which thepatient ignores objects, and even body parts, in the half of sensory space oppositeto the lesion.I9This syndrome appears to involve dysfunction of brain-stem, thala-m i ~ ,nd cortical alerting system^. Positron emission tomography (PET) studiesof attention have shown increased blood flow in right frontal cortex in a numberof experiments that require orienting to targets.20The noradrenergic (NE) brain-stem projection system courses through the frontal lobe before projecting caudallyto posterior cortex, primarily of the dorsal (archicortical) p a t h ~ a y . ~ 'or humanattention, Tucker and Williamsoni7proposed that the NE phasic arousal systemis particularly important to the holistic attentional mode of the right hemisphere.Although many issues remain to be worked out, theoretical models that link frontalcontrol to arousal regulation provide ways of understanding the deficits of motiva-tion and initiative that may follow frontal lesions.22Further clarification of theo-retical issues may help explain the normal role of frontal cortex in recruiting theappropriate state of arousal and alertness in service of effective behavior.

Corticolimbic Network rchitectureOn the basis of both lesion and stimulation evidence and considering the con-nectivity of frontal cortex, Pribram and his associates have theorized that thefrontal lobe is essential to integrating complex behavior because it representsthe neocortical extension of the limbic s y ~ t e m . ~ ~ - ~ ~ecent research continues toconfirm that areas of frontal cortex are closely connected to autonomic responses,as are areas of paralimbic cortex.26In addition, areas of frontal cortex appear tobe important in integrating kinesthetic information with ongoing behavior, andimpairment in kinesthetic processing may be a factor in the learning deficits ofmonkeys with frontal lesion^.^Any theory of the motivational basis of the function of the frontal lobe must

8/13/2019 K. Pribram T-192

5/25

TUCKER l al : SELF REGULATIONtion considered the limbic structures as providing interoceptive reference pointsto serve as adaptive guides for the frontal lobe's direction of beha~ior.~'n amanner similar to Teuber's corollary discharge to perceptual systems,29an effer-ent copy of a frontal action plan could be evaluated in terms of the limbic refer-ence points for desired outcomes.28

In the cognitive neuroscience model of today's research, the function of thefrontal lobe is often considered in terms of working memory.30Corticolimbic con-nections are essential for memory as well as emotion. In monkeys, disruption ofthe conical pathways linking perceptual systems to the hippocampus, amygdala,and associated paralimbic cortices results in severe memory irnpairment~.~ ' .~~nhumans, the amnesia syndromes can be traced to damage to limbic structures andparalimbic cortex.33Corticolimbic connections are often thought of in terms ofthe perceptual operations of the posterior brain, but they must also be importantin guiding action on the basis of experience as well. The frontal neocortex shows apattern of connectivity that links t to the archicortical and paleocortical paralimbiccortices, just as for the posterior brain.34However, the primary direction of infor-mation flow for the posterior brain appears to be from neocortical (sensory cortex)to limbic, whereas the primary flow for the anterior brain is from limbic to neocorti-cal (primary motor).35An interesting theoretical question is whether the mecha-nisms of memory operate differently when the dominant direction of control re-verses in the corticolimbic pathways.

Recognizing the dual functions of the limbic networks-memory and emo-tion-suggests important possibilities for theoretical insight into the adaptive baseof frontal lobe function. To relate the anatomical and functional evidence to atheory of the cognition of the human frontal lobe, two theoretical questions arise.First, what does it mean that the networks that are most critical for consolidatingmemory (the paralimbic cortices) are also those that represent kinesthetic andvisceral information? Second, how do these primitive regions of cortex shape theorganization and control of actions?

For both these questions, psychological theory has provided an important per-spective. Heinz Werner proposed that in the child's primitive, syncretic percep-tion, motor attitudes, and bodily feelings form the elementary substrate for experi-ence, the postural-affective matrix. From this primitive experiential basis,specific thoughts and actions become articulated through a progressive developmental process.36 Although the articulation becomes more differentiated in theadult's cognition, Werner believed that the adult's cognition still begins at a syn-cretic, primitive level of organization and becomes progressively articulated intoeach discrete act. This developmental process is said to be microgenetic, becauseit occurs within the milliseconds required for the formation of each thought andaction.

Drawing from Werner's model, Brown3' theorized that specific forms of apraxia(motor disorder) result from specific frontal lobe lesions because they representthe disruption of specific stages in the microgenetic process: frontal limbic lesionsimpair the initiation of actions; prefrontal lesions impair the direction and organiza-tion of actions once they are initiated; premotor and precentral lesions impair thefinal articulation of the action sequence. Each level of the reentrantly connected

8/13/2019 K. Pribram T-192

6/25

2 8 NN LS NEW YORK C DEMY OF SCIENCESlimbic-cortical progression thus serves to differentiate the action from the primi-tive motivational impetus.In reviewing the theoretical issues in the research on frontal lobe anatomy andfunction, PribamZ7 roposed that Brown's microgenetic model provides a usefulmodel for the development of motor plans across the linked limbic-neocorticalnetworks of the frontal lobe. A microgenetic account might also explain the inte-gration of visceral and kinesthetic representations within the organization of actionprograms. The frontal cortex may mediate between the interoceptive state repre-sented within limbic networks and the external context as it is interfaced by pri-mary sensory and motor c o r t i c e ~ . ~~ . ' ~Derryberry and Tucker39developed this line of reasoning by considering thecomputational architecture of the mammalian cortex. Within a connectionist orparallel-distributed model of information processing, the representational functionof a network can be inferred in large part from its pattern of connectivity. Theanatomical studies of Pandya and Yeterian40have shown that the interconnectionamong widespread cortical regions is sparse for neocortical networks (which there-fore appear to process in a local fashion) and dense for paralimbic networks (whichtherefore appear to process in a more global fashion). This evidence shows thatthe most essential association cortex may not be that on the lateral convexityof the hemisphere, as traditionally thought. Rather, the greatest integration ofsensory, motor, and evaluative information may occur in the primitive paralimbiccortex. In the cognitive domain, a central integrating role for paralimbic networkswould be consistent with Brown's3' observation that semantic language disordersinvolve damage to limbic cortex.Thus the connectivity to limbic regions may help explain the cognitive as wellas the motivational functions of the frontal lobe. Derryben-y and Tucker pro-posed that the representation of interoceptive information within paralimbic net-works provides a reference for evaluating and motivatingcognitivarepresentationsformed at this holistic level, before they are articulated as realized-actions or fullyconscious ideas. The limbic base for cognition may not be limited to thought andbehavior that is obviously emotional. Tucker and Der r~ben-y~~heorized that themotivational substrate from limbic networks may be essential for guiding thehigher executive functions of the frontal lobe. Thus anxiety, emerging from ventrallimbic structures and becoming elaborated within orbital frontal cortex, may be anintegral component of the focused attention and anticipation required for effectiveplanning. Although pathologically high anxiety may disrupt frontal lobe function,4'inadequate anxiety may contribute to the self-control deficits and personality dis-order in the pseudopsychopathic syndrome that results from orbital frontal le-s i ~ n s . . ~ ~

Although our purpose in this section has been to consider the vertical integra-tion across limbic and neocortical networks in a general sense, the example ofanxiety and the role of anticipation and planning pertains to a specific anatomicalsubdivision, the orbital frontal cortex emanating from the paleocortical limbicnetworks. The evolutionary parcellation of the cortex shown by the anatomicalti it li s of Pandya and associates has given an important new perspective on theI'~inctional natomy of the frontal lobe. In the following section, we review thei~nntomyof the archicortical and paleocortical pathways, the interpretation of

8/13/2019 K. Pribram T-192

7/25

TUCKER l al : SELF REGULATION 2 9

differing forms of motor control in each pathway by G ~ l d b e r g , ~ ~nd we proposethat there are unique motivational biases for each pathway that are consistentwith the different modes of motor control.

DORSAL AhlD VENTRAL CORTICOLIMBIC PATHWAYSIf the executive functions of the frontal lobe involve working memory,27.30~47-s'

these functions must be bound by the motivational constraints of limbic networkson one end of the processing stream and by the requirements of motor articulationon the other. The theoretical challenge is to characterize the progressive organiza-tion of behavior across frontal networks in a way that captures the integration ofdiverse motivational constraints, the recruitment of activation and arousal controlsintegral to the process, the extended working memory made possible by largenetworks, and the fine differentiation of motor programs that are suitably con-strained by the extended representational process. In this section, we considerthis process in reverse microgenetic order, beginning with a model of motor articu-lation, considering the role of working memory in planning action, and then theo-rizing on the emotional and motivational foundations from which the actions areorganized. We argue that the theoretical challenge must be met twice, becausedifferent principles may be required to describe the dorsal and ventral limbic-cortical processing streams.

Clinical observations have long suggested that there may be differing motiva-tional disorders resulting from damage to dorsal and ventral areas. Kleist notedin 93 that patients with damage to the mediodorsal areas of the frontal lobesmay show apathy and indifference, whereas patients with damage to orbital areasmay show poor inhibition of impulses.53A number of recent findings have beenconsistent with Kleist's observations. A lack of initiative is often seen with bilat-eral dorsomedial frontal lesions. This condition may be confused with psychiatricdepression, and has been called the pseudodepression syndrome. An extremeform of apathy may be seen in the syndrome of akinetic mutism, in which thepatient does not initiate action or speech even though capable of doing so. Al-though damage to basal ganglia or rostra1 brain stem may be required for a chronicform of this condition, it is not uncommon to see this syndrome in the period soonafter cingulate and mediodorsal frontal lesions.54 Thus, consistent with Kleist'sformulation, an intact mediodorsal frontal lobe may be required for normal motiva-tional initiative.

In contrast, lesions of the orbital frontal lobe may produce a deficit in control-ling motivational impulses. Although the disinhibition syndrome 'has tradition-ally been related to frontal lesions generally, the classical neurological literatureshows disinhibition of impulses, puerility, and euphoria to be associated withdamage to the orbital surface s~ecifically.~~n the pseudopsychopathic syn-drome, damage to the orbital frontal region leads to the inability to maintainnormal social constraints on behavior.'. These deficits of inhibition form aninteresting counterpoint to the overly restricted behavior of the anxious person,which may be associated with exaggerated activity of the orbital frontal l ~ b e . ~ ' , ~ '

We propose that understanding the role of the frontal lobe in human social

8/13/2019 K. Pribram T-192

8/25

22 ANNALS N W YORK ACADEMY OF SCIENCESand emotional behavior may require an appreciation of the differing modes ofmotivational control applied by the dorsal and ventral pathways that lead fromlimbic networks to the motor cortex. The anatomical differentiation of these path-ways reflects the fact that the neocortex evolved from two points of origin: thedorsal, archicortical limbic cortex connected with the hippocampus and the ven-tral, paleocortical region associated with olfactory cortex. This evolutionaryperspective has provided new insights into the connectional architecture of thefrontal lobe.35

In this section, we briefly outline the anatomical evidence for dual evolutionaryorigins of frontal cortex. We then propose that, just as the dorsal and ventralpathways display unique modes of motor control as they culminate in motor cor-

these pathways may stem from unique modes of motivational control as eachthought and action emerges from the archicortical and paleocortical substrate.Consistent with the principle of vertical integration, the unique motivational biasesof the dorsal and ventral pathways may extend below the limbic networks, engag-ing differential modes of controlling activation and arousal by the brain-stem neu-romodulator projection systems.

Dorsal and Ventral ortical MoietiesThe archicortical trend begins in the medial aspect of each hemisphere and

projects to the mediodorsal surface of the frontal The evolution of thearchicortical moiety from the hippocampus gave rise to proisocortical areas (cingu-late cortex, Brodmann areas 24, 25 and 32 and finally to the isocortical areas9 , 10,46, and 8 on the dorsal surface). Within motor cortex, area 24 differentiatedinto premotor cortex,' which includes the supplementary motor area.(SMA) andprimary motor cortex (area 4). As it differentiated from primitive paralimbic cor-tex, the neocortex for both dorsal and ventral moieties accentuated the supragran-ular layers. Within the dorsal trend the architectonic differentiation emphasizedthe pyramidal cells. Within the ventral, paleocortical trend the differentiation em-phasized the granular cells.

The paleocortical trend differentiated from the paleocortex on the ventral sur-face of the frontal lobe, into the proisocortex of the orbital and rostra1 insularregions, and finally into the isocortex on the ventrolateral surfaces of the prefrontalcortex, including Brodmann areas 10, 12,46, 14,8, and 1 Paralleling the evolu-tion of the dorsal trend, the paleocortical trend gave rise to the motor cortex on theventral surface (area 6), which includes the face, head, and neck representations.Reflecting the shared paleocortical origin, researchers have noted the similaritiesbetween the insula and orbital cortex in terms of both architectonics and projec-t ion~.~ ' . '~

Projectional and Responsive Modes of Motor ontrol

8/13/2019 K. Pribram T-192

9/25

TUCKER t al : SELF REGULATION 221

movements. Similarly, PribramZ7 roposed that the function of the frontal lobemay be discerned by understanding how internal experiences are translated intomotor actions. An instructive theory of how motor control may be effected differ-entially by the archicortical and paleocortical limbic-cortical pathways was pro-posed by G ~ l d b e r g . ~ ~

Goldberg suggested that the mediodorsal frontal pathway, derived from archi-cortex, is concerned with projecting actions based on probabilistic models of thefuture. Within this network, motor behavior is organized according to the organ-ism's internal model of the world that is based on experience in similar context^. ^In this pathway, the control of action is achieved through a projectional or feed-forward mode, in that the motor plan is directed by a preexisting model of theaction rather than ongoing feedback about the course of the action in the environ-mental ~ituation.~ ' he entire action sequence is organized and launched as aholistic unit.

The ventrolateral motor system, in contrast, appears to link motor sequencesto perceptual objects in a responsive manner.46This system must be able to iden-tify objects and their motivational significance, and then a feedback guidanceof motor action causes the motor plan to be articulated with specific reference tothe ongoing perceptual input. The ventral motor plan seems to be more differen-tiated in time than that in the dorsal stream, in that each segment can be linkedto perceptual data about its progress.

Observing the separation of these systems of motor control in the frontal lobesuggests that evolution has encountered the same dilemma faced by artificial intel-ligence researchers in designing intelligent machines (Hendler, this volume). Adeliberate system, one that projects actions in future scenarios, is poorly suitedto reacting to unforeseen events. A reactive system, on the other hand, is gearedfor feedback control, and this architecture may not support control by plans.

Could the dorsal and ventral modes of motor control be dependent on differingmotivational biases? Are these biases unmasked by the personality deficits result-ing from dorsal versus orbital frontal lesions? If the patient with a dorsomediallesion is apathetic and lacks behavioral initiative, this may suggest that the projec-tional mode of action in the dorsal pathway has a characteristic motivational ba-sis-a bias toward initiation of action that results in holistic motor plans beingprojected into the environmental context. If the patient with ventrolateral lesionsis impulsive and inappropriate, this may reflect an unbalanced exaggeration of theimpulsiveness of the dorsal stream. If so, the normal contribution of the ventralpathway would be to restrict and monitor motivational impulses, perhaps in amanner analogous to the feedback guidance of the action plan by perceptual dataon Goldberg's model of the ventral trend.

earning Mechanisms and Work ing MemoryIf there are inherent relations between the motivational biases suggested by

clinical observations and the modes of motor control in Goldberg's analysis, weshould expect to find these biases of motivational control integral to the cognitiveoperations of dorsal and ventral regions of frontal cortex. In a general sense, goal-

8/13/2019 K. Pribram T-192

10/25

NN LS NEW YORK C DEMY OF SCIENCES

directed behavior must be organized over time; and therefore it must be guidedby the working memory capacities of frontal networks. Given the essential roleof corticolimbic interaction in memory consolidati~n,~e can assume that frontalconnections with limbic networks will be necessary to consolidate the cognitiverepresentations that support extended motor planning. Although there is substan-tial evidence that limbic networks are integral to memory and that there are uniquememory capacities for dorsal and ventral pathways in the frontal lobe, i t is anunanswered question how these memory capacities relate specifically to differingmethods of motor control.Several lines of evidence suggest that the archicortical and paleocortical moie-ties support functionally as well as anatomically differentiated memory circuits.The ventral memory system appears to be dependent upon rhinal sulcus, themediodorsal thalamus, and the orbital ~ o r t e x . ~ ~ . ~ 'n contrast, the dorsal circuitappears to e centered on the hippocampus, anterior nucleus of the thalamus, andthe cingulate lobe.6' Lesions to both the orbitoventral and cingulate cortices resulti n memory defi~its,~'nd similar memory impairments are observed after lesionsto the mediodorsal and anterior thalamic nuclei.63Although the functional differentiation of these two memory circuits remainsto be clarified, a strong hypothesis is that they are differentially involved in objectand spatial memory. The dorsal memory circuit centered on the hippocampusmay be involved in spatial memory.64One speculation is that the dorsal pathwayis important to contextual memory, which may be analogous to spatial relation^.^The ventral trend, on the other hand, may be especially involved in object memoryand the fine-tuning of the neocortical representation of objects, whether the ob-jects are conceptual or pe r~ep tua l .~~A similar framework for cognition was suggested by Kleist in 1934 in a remark-able anticipation of today's cognitive neuroscience model of dorsal and ventralmemory systems.65The studies of perceptual memory by Ungerleider and Mis-hkin3' have led to the realization that objects, the what -of perception, arerepresented in the ventral processing stream, whereas spatial relations, the

where of perception, are represented in the dorsal processing stream. Kleistproposed that what is represented in orbital frontal cortex, whereas the howof organizing actions is organized in dorsal regions of frontal cortex.65Although generalizations to complex cognitive processes remain speculative,there is substantial experimental evidence with monkeys to differentiate betweenobject and spatial memory capacities of ventral and dorsal frontal regions. In themonkey, the principal sulcus is the boundary dividing the two cortical trends.56I t has long been known that lesions to the dorsal areas above the principal sulcusresult in poor performance on spatial delay tasks, and that lesions to areas ventralto the principal sulcus result in poor performance on object alternation tasks.27Current work with single-cell recording i n monkeys has provided support for theseobservation^ ^^ ^^Studies by Goldman-Rakic and associates have provided convincing evidencethat the dorsal and ventral pathways of the posterior cortex, with their respectivearchicortical and paleoconical targets, are continuous with the dorsal and ventralpathways ofthe frontal lobe. Neurons below the principal sulcus are responsiveto foveal visual stimulation and to recognition of objects in the perceptual field.

8/13/2019 K. Pribram T-192

11/25

TUCKER et ul : SELF REGULATION 3Both of these functions are linked to the posterior ventral pathway of the visualsystem proceeding from occipital to inferior temporal areas.s1 Neurons above theprincipal sulcus are responsive to peripheral visual stimulation and to spatial as-pects of the perceptual task, consistent with the posterior dorsal visual pathwaythrough parietal lobe to cingulate ~ortex.~'he working memory operations offrontal cortex appear to maintain the functional continuity with the dorsal andventral processing streams of posterior ~o r t ex .~Fustee9sMproposes that the memory capacities of the frontal lobe provide theprimate brain with an extended time frame within which more complex patternsof behavior may be organized. Many human cognitive processes can be said tobe motor plans that are rehearsed, and evaluated for their adaptive significance,covertly. The most complex forms of cognition require the capacity to evaluateevents after they have occurred and to anticipate action before it is required.These are skills that draw explicitly on the temporal span of experience that Fusterdescribes.

If the dorsal and ventral pathways represent integrated networks for highercognitive functions, we might expect there would be general principles that couldrelate the specialized forms of spatial and object working memory to the projec-tional and reactive modes of motor control, respectively. Do peripheral visionand spatial memory provide a holistic context to support the ballistic, projectionalmode of action in the dorsal pathway? Do foveal vision and object identificationprovide a parsing of the sensory stream in a way that supports a differentiatedfeedback-monitoring of sequential actions?If there are coherent systems of working memory that are integral to dorsaland ventral motor control pathways, these may provide clues to the initiativeversus inhibitory motivational biases suggested for the dorsal and ventral path-ways by clinical neurology. Substantial evidence indicates that the memory opera-tions of the limbic circuitry are closely linked with motivational mechanisms.Clues to the unique adaptive controls inherent to the archicortical and paleocorti-cal substrates of the neocortex may be present in this evidence.

Motivational ias o the Ventral PathwayThe ventrolateral motor system, with its limbic cortical base in the orbitalfrontal lobe, may derive its affective influences through extensive connectionswith the amygdala, insular, and temporal pole c o r t i c e ~ . ~ ~ - ~ 'he temporal andinsula regions provide the ventrolateral system with data from the auditory, visual,and somestheiic modalities for evaluation. In addition, the interconnections ofthe ventral trend with the insula may be important for linking visceroautonomicassociations to perceptual events and to the organization of action plans. .39 Basedupon their review of the literature, Buchanan and Powell6' emphasized the impor-tance of sympathetic autonomic responses to ventral limbic cortex. By integratingsensory information with autonomic responses, the ventral limbic complex is wellsuited to evaluate stimuli for their motivational significance in relation to internalstates. Given the evidence linking the ventral trend to the flightlfight response?sympathetic regulation may be particularly important for dealing with threat.

8/13/2019 K. Pribram T-192

12/25

4 ANNALS NEW YORK ACADEMY OF SCIENCES

The aiygdala appears important to integrating the sensory data that lead tofear responses in rats.68 In primates, Pribram and his associates have observedeffects of amygdala lesions that may suggest ways that memory consolidationin the ventral trend is associated with a specific motivational bias. This biasmay be consistent with a role of the ventral limbic networks i n anxiety4' and inthe inhibition of impulses suggested by classical and by more recenP9 clinicalobservations.Pribram70 suggests that the amygdala integrates visceroautonomic informationwith ongoing perception in a process of memory consolidation familiarization-that marks an episode i n time. This parsing of an episode from the flow ofexperience may be relevant for the learning deficits of amygdalectomized mon-keys. In addition, the behavioral abnormalities of these monkeys are consistentwith the classical Kluver-Bucy ~yndrome:~'hey show inappropriate approachbehavior to previously feared objects, and they appear hypersexual and hyperoral.These examples of disinhibited behavior may be consistent with the loss of thenormal inhibition of hedonic impulses that would stem from the anxiety and threat-monitoring operations of the ventral trend. This tight, inhibitory control in theaffective domain may represent the motivational counterpart to the reactive, feed-back mode of control of the ventrolateral system in the motor domain.46

Motivational ias of the orsal Pathwayn considering the control of learning by the hippocampus, Pribram70 has sug-gested that it may support a representation of the context in which behavior oc-curs. The mechanism for doing this is an interesting one. Several findings suggestthe hippocampus may code information about nonreinforced stimuli. This formof discrimination may be important to the extinction of ineffective attention andbehavior, and it may be important in relegaiing nonreinforced stimuli to the back-ground or context of the current behavior.

This framing of the context may be related to the emergence of spatial attentionand memory skills of the archicortical and perhaps to the notionthat the dorsal cortical regions represent contextual information in more generalsemantic cognition in humans.42There is also the suggestion that the learningand memory mechanisms of the hippocampus are associated with a particularmotivational bias. Monkeys with hippocampectomy become more conservativeand take fewer risks in task perf~rmance.~' his appears to be an opposite biasto the fearless impulsivity of the amygdalectomized monkeys.70These differentialeffects of amygdala versus hippocampal lesions may provide clues to the limbicsubstrate of the apathy and loss of initiative with dorsal frontal lesions versus thedisinhibition of impulses observed with ventral frontal lesion^.^^ ^^^^^^Some researchers have argued that the motivational and emotional processesof the limbic circuitry are centered on the amygdala and that the hippocampusand associated dorsal limbic cortex are more relevant to cognition than emotion.However, this view ignores the substantial evidence of the importance of thecingulate coqex to emotion in both animals and humans.76 The cingulate cortexruns along the superior surface of the corpus callosum and is separated from it by

8/13/2019 K. Pribram T-192

13/25

TUCKER et d :SELF REGULATION 225

the callosal sulcus. Recent studies suggest the cingulate is a highly heterogeneousstructure. In addition to being divided in the rostrallcaudal dimension, it is alsodifferentiated in the dorsallventral dimen~ion.~'he anterior cingulate (areas 24,25, and 32 can be differentiated from the posterior cingulate based upon cytoarchi-tecture and patterns of projections, as well as f~nction.~' ost notably, the ante-rior cingulate receives afferents from the amygdala, whereas the posterior cingu-late does not.79 The posterior cingulate does not have direct projections to thepremotor areas of the frontal lobe, whereas the anterior cingulate does.'' Consis-tent with a general rostraVcaudal motorlsensory distinction, the anterior cingulateis characterized as executive in function, whereas the posterior is characterizedas e~alua tive . ~~One way of interpreting the apathy and loss of initiative resulting from dor-somedial frontal lesions would be to attribute these effects to impairment of thedorsal limbic contribution to integrating hedonic value with potential action plans.Patients with cingulate lesions are found to lose interest in formerly importantactivities, such as hobbies. ' This evidence is consistent with the view that thecingulate cortex contributes to attention by monitoring the motivational signifi-cance of ~tirnuli.'~MacLean has emphasized that the dorsal limbic structures have become en-larged in mammalian evolution in parallel with the appearance of complex socialand emotional behavior, including care for the young, emotional vocalization,and Research examining this hypothesis for emotional vocalization hassupported the importance of cingulate cortex. Ploog and a~soc ia t e s '~ .~ave useda combination of lesion and stimulation studies to show the control hierarchy foremotional vocalization in the monkey, with fragmentary motor features repre-sented in brain-stem motor nuclei, patterned species-specific calls represented inthe midbrain, emotional coloration of calls deriving from limbic influences, andvoluntary call initiation being controlled by cingulate ~ o r t e x . ~ ~ . ~n contrast, lat-eral motor Cortex appears to control voluntary call formation through articu-lated actions mediated by direct pyramidal pathways from motor cortex to brain-stem motor nuclei.The motivated initiation of holistic patterns of vocalization by the cingulateregion bears interesting similarities to both the motivational initiative and theprojectional mode of motor ~ontrol ~scribed to dorsomedial frontal cortex. Inhumans, there are suggestions that the cingulate region may be important in attach-ing motivational significance, and self-relevance, to the organization of actions inthe dorsal limbic-frontal pathway. The decrease in agitation following cingulatelesions for chronic anxiety or for intractable pain4 may be interpreted as a lossof caring about the condition. The fact that patients lose interest in formerly valuedactivities8' suggests that the cingulate contribution to motivational significance isnot limited to aversive initiation of action, but that it may involve hedonic value aswell. The incorporation of motivational significance, visceral tone, and kinestheticsensation within the organization of an action may be integral to perceiving theaction as part of the self. G ~ l d b e r g ~ ~escribes the alien hand syndrome result-ing from dorsomedial frontal lesions, in which an action of the hand contralateralto the lesion, apparently arising within the ventrolateral motor system, is perceivedas belonging to someone else.

8/13/2019 K. Pribram T-192

14/25

6 ANNALS NEW YORK ACADEMY OF SCIENCES

Redundancy and Habituation Biases as daptive ttentional Modesn theorizing about the motivational basis of the orbital frontal lobe s contribu-

tion to the executive functions, Tucker and Der~yberry~~roposed that anxietymay be the affective characteristic of.the preparation for fightlflight within theextended amygdala and ventral limbic-frontal pathway. This interpretation wouldbe consistent with the decreases in anxiety with psychosurgery of the orbitalregion4and with the increases in blood flow in ventral frontal cortex seen in clinicalanxiety states.43This view would not be consistent with Jeffrey Gray s view thatanxiety is regulated by the hippocampus. Gray, however, emphasized behavioralinhibition as the key feature of anxiety, whereas Tucker and Derryberry empha-sized vigilance and attentional focusing. Although anxiety is often considered tobe a pathological state, it may have an integral role in optimal brain function,focusing attention on adaptively important objects.

Tucker and D e r r ~ b e r r y ~ ~rgued that the redundancy bias of the dopaminergictonic activation system17 may mediate the attentional focusing associated withanxiety. This elementary mode of controlling working memory may have bothprimitive and sophisticated influences on behavior. In the primitive form, redun-dancy bias would facilitate routinized actions, such as in habit formation or in thestereotyped motor sequences of fightlflight responses. In the more sophisticatedform, the redundancy bias may focus the representation of plans in working mem-ory on motivationally significant issues, allowing an extended representation thatsupports the continuity of goal-directed behavior over time. Tucker and Derry-berry suggest that the focused attention of the dopaminergic redundancy bias maybe especially important to the analytic cognition of the left hemi~phere.~

In both primitive and sophisticated forms, the redundancy bias may be integralto the feedback modulation of discrete motor sequences in the ventrolateral motorsystem. The pathological symptoms of exaggerated redundancg,in working mem-ory, such as the ruminations and compulsions of the chronicalljl anxious person,may represent the distortion of a neurocybernetic mode that is essential to thenormal maintenance of motivated attention.42

We speculate that the dorsal motor system may also be regulated by a qualita-tively-specific activity control system, the habituation bias of the noradrenergicphasic arousal system. The noradrenergic projections from the brain stem denselyinnervate cingulate cortex, ascend to the frontal pole, then proceed caudally toinnervate the dorsal regions of the neocortex preferentially 2 Tucker and William-sonI7 heorized that, by decrementing attention to constant features of the environ-ment, a habituation bias would create the positive control of a selection for nov-elty. They proposed that this novelty selection is integral to the orienting responseand that in humans the resulting expansive allocation of working memory is impor-tant to the holistic spatial cognitive skills of the right hemisphere. Whereas righthemisphere specialization is qn integral aspect of spatial attention in humans, thismust be an elaboration of the more fundamental organization of spatial attentionand memory within the primate dorsal corticolimbic pathway.ss

At the limbic root of the archicortical pathway, the hippocampus may regulatelearning and memory through mechanisms that are consistent with a habituation

8/13/2019 K. Pribram T-192

15/25

8/13/2019 K. Pribram T-192

16/25

128 NN LS NEW YORK C DEMY OF SCIENCESdamage.92Normal subjects show greater expressivity of emotion on the left sideof the face, and they show greater attention to the speaker's emotional tone ofvoice when passages are presented to the left ear.94

This evidence of the importance of the right hemisphere to emotion may beconsistent with certain clinical observations suggesting that right frontal lobe le-sions are particularly likely to produce the personality disinhibition of the frontallobe syndrome.'O However, other evidence has suggested that the left hemispherealso plays an important role in emotional experience and behavior, and a numberof recent findings point to the importance of left-frontal lobe function in particular.For both right and left frontal lobes, a key question is how the frontal cortexrelates to the emotional processes mediated by subcortical circuits.

hferal izat ion of Positive and Negalive motionsAltered emotional and personality processes with right-hemisphere lesions had

been recognized since Babinski's observation that anosognosia, denial of illness,was most common with left hemiplegia. However, the depressive-catastrophicresponse to stroke or other brain damage was recognized by Goldsteing5 o occurmore frequently with left-hemisphere lesions. The obvious interpretation of thisassociation was that the loss of language is more devastating than loss of nonverbalintelligence. However, a number of studies have failed to correlate the degreeof depressive response with the degree of language or cognitive impairment,%suggesting that a more fundamental relation may exist between hemispheric spe-cialization and the balance between positive and negative emotional orientations.

An important milestone in this literature was Gainotti's confirmation that cata-strophic responses are more likely with left-hemisphere lesions, whereas indiffer-ence denial of problems may be more likely with right-hemisphere lesion^.^ As-suming that these findings provide an insight into human emotional balance, theinterpretive question became whether damage to a hemisphere results in a releaseof the contralateral hemisphere's normal emotional orientation?' or a release ofthe damaged hemisphere's subcortical circuits.99

In support of the contralateral release interpretation, Sackeim r reviewedseveral forms of evidence from the neurological literature. A strong associationbetween the laterality of the lesion and emotional valence was found for cases ofpathological laughing (more common with right-hemisphere lesions) and crying(more common with left-hemisphere lesions). The classical interpretation of suchcases of pseudobulbar palsy is a release of brain-stem emotional mecha-nisms.'OO-'O' inn points out that whereas corticobulbar projections to brain-stemmotor nuclei are contralateral, the pathways disrupted in pseudobulbar palsy in-volve the reticular formation and, therefore, are bilateral.

n their review, Sackeim r a/. also observed that outbursts of laughter werefrequently associated with left-hemisphere seizures. Reasoning that seizures rep-resent an exaggeration of hemispheric function, Sackeim r al concluded thatthis evidence implicates a positive emotional bias for the left hemisphere. Thisconclusion would fit with a contralateral release view of the effects of lesions,assuming that the left hemisphere normally tends toward positive emotion and

8/13/2019 K. Pribram T-192

17/25

TUCKER l al : SELF REGULATION 229

the right hemisphere toward negative emotion. Particularly important to this issuewas the evidence on chronic changes in emotional outlook in temporal lobe epi-lepsy.I0' In this research, patients with left-hemisphere pathology showed a nega-tive, critical orientation in self-report measures, whereas those with right-hemi-sphere pathology showed an inappropriately positive approach to self-evaluation.form of ipsilateral release was suggested by the cognitive styles of these patientgroups. The patients with a left focus were highly intellectualized as well as self-critical, suggesting exaggerated if degraded left-hemisphere cognitive function.The patients with a right focus were emotionally expressive as well as inappro-priately positive, suggesting exaggerated right-hemisphere function.

symmetric Frontal Lobe Contributions

Although temporal lobe mechanisms are obviously critical to this controversy,the frontal lobe has been found to have an integral role as well. Some of theinitial evidence came from EEG studies with normal emotion, which have foundasymmetries in frontal lobe alpha activity in a number of paradigms. The initialreporttwobserved greater EEG activation (alpha suppression) over the right fron-tal lobe in response to negative emotional material, in contrast to EEG activationover the left frontal lobe in response to positive emotional material. Independently,Tucker t al. found a consistent pattern of results: normal subjects in an induceddepressed mood showed alpha suppression (EEG activation) over the right frontallobe.'OsAlthough the findings of frontal lobe EEG asymmetry were consistent in theseinitial studies, the functional interpretations were not. In line with Sackeim tal.'s reasoning, Davidson and associates proposed that the left hemisphere con-tributes to positive emotion and to approach behavior generally,Io6whereas theright hemisphere is responsible for negative emotion and behavioral withdrawal.In contrast, Tucker t al.lo5 interpreted their frontal EEG results in line with theipsilateral release interpretation of the neurological evidence, proposing that thefrontal activity may be inhibitory in nature. In their mood induction study, Tuckert al. had observed that the depressed mood was associated not only with rightfrontal EEG activation, but impaired visuospatial performance suggestive of de-creased right-hemisphere cognitive functioning.The evidence of poor visuospatial perception in depression is now quite sub-stantial, and a number of findings implicate impaired right-hemisphere function~pecifically.~'n addition to replicating and extending their findings of frontal-lobe alpha asymmetries in a number of experiments, Davidson and associateshave also observed poor right-hemisphere cognitive function in depression. Theinterpretation that the role of the frontal lobe could be inhibitory is consistent withthe many findings of disinhibition with frontal lesions. Knight and associate^, ^^ forexample, observed increased auditory RP responses over the ipsilateral hemi-

8/13/2019 K. Pribram T-192

18/25

L U NN LS NEW YORK C DEMY OF SCIENCES

sphere in'frontal-lesioned patients, suggesting the normal attentional control offrontal cortex may be inhibitory.An important recent addition to this line of evidence has been the finding that,in normal subjects, left-frontal alpha suppression is related less to the subject'scurrent emotional state than it is to the tendency to deny negative characteris-t i c ~ . ' ~n this research i t was repressors, subjects who present themselves in afavorable light, who showed the greatest left-frontal alpha suppression in the nor-mal sample of university students. This finding, coupled with an inverse relationbetween left-frontal blood flow and bilateral amygdala activity in depressed pa-tients, has led Davidsonl'O to propose that an important role of left-frontal activitymay be the inhibition of negative affect.Frontal lobe function has been found to be critical to the interpretation ofhemispheric contributions to emotion in lesioned patients as well as in normalsubjects. In studies of acute depression in stroke patients, Robinson and associatesconfirmed the previous reports of greater depression with left-hemisphere lesions,and they found a striking trend for greater depression with lesions of more anteriorregions of the left hemisphere.%Tucker and Frederick' interpreted these obser-vations in line with an inhibitory role for the left-frontal region, specifically inhibit-ing the left-hemisphere limbic and subcortical contributions to anxiety and nega-tive affect. However, at least for striatal contributions to emotional responsivity,this reasoning does not seem to hold. Starkstein t al. ' examined emotionalresponses in patients with lesions of the caudate nucleus as well as frontal cortex;depression was common in patients with left-caudate lesions as well as left frontalcortex.If the left frontal lobe is important in inhibiting negative affect, the subcorticalstructures that are inhibited may be the limbic structures of the left hemisphere.Recent P T blood flow findings have suggested that increased functioning of theamygdala of the left hemisphere may accompany negative affect in both normalsubjects and depressed patients. Coupled with previous reports of increased activ-ity of left frontal cortex in negative emotion, these findings raise interesting ques-tions about hemispheric frontal-limbic interactions in emotional self-regulation.number of studies have observed increased blood flow and metabolism ofregions of left frontal cortex in negative affect. With the Xenon surface rCBF(regional cerebral blood flow) method, Johanson and associates examined anxietydisorder patients as they considered the source of their anxiety. Increased bloodflow was observed in inferior regions of the left hemisphere.Il3 Using positronemission tomography (PET) measures of rCBF with normal volunteers, Pardo etal.'14 found increased orbitofrontal.blood flow bilaterally for women in their sam-ple, but only on the left for the men.An important question for mood induction research is the uncontrolled cogni-tion, such as self-verbalization, that may be induced by the instructions in additionto the affect. Extending their study of anxious patients with a high-resolutionrCBF scanner, Johanson et al also included a control condition of a neutral moodinduction that served to equate the possible demands for self-verbali~ation.~)heyagain found high flow over inferior (orbital) left-frontal areas in anxiety. Giventhe chronic high anxiety of most obsessive-compulsivepatients, a consistent find-

8/13/2019 K. Pribram T-192

19/25

TUCKER el al.: SELF REGULATION 3

ing may be that of Baxter t al . who found increased metabolism in both caudatenuclei and the left orbital frontal cortex in a PET study of obsessive-compul-s i v e ~ . ~

The improved anatomical precision of PET rCBF, particularly with registrationwith magnetic resonance anatomical images, has allowed estimates of activity inthe amygdala. Examining unipolar depressed patients, Drevets and associatesfound increased blood flow in the left amygdala and in left frontal ~ o r t e x . ~on-verging findings with normal emotion have come from the PET rCBF study ofSchneider, Gur and associates,''' who used viewing of emotional faces as a moodinduction procedure. In the negative-emotion condition of this experiment, thesubjects showed increased flow of the left amygdala. In the positive-emotion con-dition, they showed increased blood flow in the right amygdala. Interestingly, ina manner similar to that described by David~on, ~everal measures of frontalcortical flow were found to be inversely correlated with amygdala blood flow.

These several findings may be consistent with the unilateral release interpreta-tion of the effect of hemispheric lesions on emotional orientation.* The inherentnegative affect (anxiety and hostility) of the left hemisphere may be seen to bemodulated by cortical control in the normal brain, such that the depressive cata-strophic response to left frontal damage reflects a release of the ipsilateral limbicemotionality. Similarly, the inherently positive emotional tone of right limbic re-gions may be normally modulated by the right frontal lobe, such that right frontaldamage leads to personality disinhibition and denial of problems. Within thisframework, the exaggerated corticolimbic interconnection in temporal lobe epi-lepsyIo3 eflects the inherent relations between a self-critical emotional tone andthe intellectual ideation of the left hemisphere, compared to the optimistic, self-aggrandizing emotional tone and emotional expressivity of the right hemisphere.These inherent relations between hemispheric cognitive styles and hemisphericaffective styles are important clues to the structure of both normal personalityand the personality disorders that include avoidant, schizoid, and anxious person-alities on the one hand, and histrionic, antisocial, and narcissistic personalitieson the other.'Is

The implications of this line of reasoning for frontal lobe function in emotionalself-regulation are interesting and somewhat complex. The frontal lobe has beendescribed as inhibitory for hemispheric emoti~nality;'~~his would be consistentwith a release (disinhibition)of emotional behavior following a frontal lesion. Yet,at least for orbitofrontal regions, the rCBF findings suggest that the emotionalstate is associated with increased frontal activity. The interesting question iswhether that increased activity during the emotional state reflects frontal inhibi-tory modulation of the limbic emotional response, or whether it reflects an elabora-tion of the emotional process itself.

ASYMMETRIES OF CORTICOLIMBIC ARCHITECTUREVery likely, the frontal lobe contribution to emotional experience and behavior

involves both excitatory and inhibitory influences from both left and right frontalregions. As neuroimaging methods provide increasingly detailed views of human

8/13/2019 K. Pribram T-192

20/25

8/13/2019 K. Pribram T-192

21/25

234 ANNALS NEW YORK ACADEMY OF SCIENCESpa thway f rom the amygda la t o o r b it a l fr on ta l co r tex m ay imp lemen t a t ight , re-s t r ic ted mode of m otor c ontro l tha t r e flec ts adapt ive cons t ra in ts o f se l f -preserva-t ion . In th e hum an bra in , hemispher ic spec ia l iza t ion ap pea rs to h a v e l ed to asymmetr ic e labo r a t ions o f the do r sa l and ven t ra l pa thways . Und e r s tand ing th einhe r en t a symm et r ie s o f co rt ico l imb ic a r ch i t ec tu r e may b e im por tan t in in te r p r e t -ing the increas ing ev id ence tha t the lef t and r igh t f ron ta l lobes contr ib u te d i ffer -en t ly t o normal and pa thologica l form s of se l f- regula t ion .

REFERENCESVALENSTEIN,. S. 1992. Therapeutic exuberance: A double-edged sword. I n SoHuman a Brain: Knowledge and V alues in the N eurosciences. A. H ani ngt on , Ed.

Birkhausen. Boston, MA.V A L E N S T E I N ,. S. 1990. The prefrontal area and psychosurgery. Prog. Brain Res.85: 539-554.PRIBRAM, H. 1950. Psychosurgery in midcentury. Surg. Gynecol. Obstet. 91:364-367.F L O R - H E N R Y ,. 1977. Progress and problem s in psychosurgery. I n Current Psychiat-ric Therapies. 1 H. M asserman, Ed.: 283-298. Grune and Stratton. New York.R Y L A N D E R ,. 1948. Personality analysis before and after frontal lobotomy. I n TheFrontal Lobes: Proceedings of the Association for Research in N ervous and MentalDisease, Vol. 27. J . F. Fulton, C. D. Aring S . B. Wortis, Ed . Williams Wilkins.Baltimore, MD.LEZAK, . D. 1976. Neuropsychological Assessment. Oxford University Press. NewYork.DAMASI O,. R., D. TR AN EL H. DAM ASIO.990. Individuals with soc iopa thic behav-ior caused by frontal damage fail to respond autonom ically to social stimuli. Behav.Brain Res. 41: 81-94.T U C K E R , . M. 1993. Em otional experience and the problem of vertical integration.Neuropsychology 7: 500-509.P R I B R A M ,. H. 1981. Emotions. I n Handbook of Clinical ~ e u r ~ s ~ c h o l o ~ ~ .. K .Filskov T. J. Boll, Eds. Wiley-Interscience. New York.L U R IA , . R . 1973. The working brain; an introduction to neuropsychology. BasicBooks. New York.LU RIA, . R. E . D. HOMSKAYA.970. Frontal lobe and the regulation of arousalprocesses. I n Attention: Contemporary Theory and Research. D. Mostofsky, Ed.Appleton-Century-Crofts. New York.Y N G L I N G ,. D. J . E . SK I NN ER .977. Gating of thalamic input to ce rebra l cortex bynucleus reticularis thalami. I n Attention Voluntary Contraction and Event-relatedCerebral Potentials; Progress in Clinical N europhysiology. Vol. 1. J . E. Desmedt,Ed .: 70-96. Karger. Basel.JA M E S , . 1884. What is emotion? Mind 4: 118-204.SCHACHTER,. I . E. SINGER.962. Cognitive, social, and physiological determi-nants of emotional state. Psychol. Rev. 69 5): 379-399.Monuzz~ ,G. H. W. MA GO UN .949. Brain stem reticular formation and activationof the EEG. Electroencephalogr. Clin. Neurophysiol. 1: 455-473.P R I E R A M ,. H . D. MC GUINN ESS.975. Arousal, activa tion, and effort in the controlof attention. Psychol. Rev.. 82: 116-149.TU CK ER , . M. P. A. WILLIAMSO N.984. Asymmetric neural control systems inhuman self-regulation. Psychol. Rev. 91 2): 185-215.M AL ON E, . A., J. R. KERSHNER,. SIEGEL J . SWANSON.emispheric processingand methylphenidate effects in ADHD. J. Child Neurol. In press.H E I L M A N ,. M. 1979. Neglect and related d isord ers. I n Clinical Neuropsychology.

8/13/2019 K. Pribram T-192

22/25

TUCKER n d : SELF REGULATION 23520. PARDO . V . P. J PARDO . W. JA NE R M. E. RAICHLE.990. The anterior cingulatecortex mediates processing selection in the Stroop attentional conflict paradigm.Proc. Natl. Acad. Sci. USA 87: 256-259.21. FOO TE . L. J . H. MORRISON.987. Extrathalamic modulation of cortical function.Annu. Rev. Neurosci. 1 : 67-95.22. HE CA EN . M. L. ALBER T. 978. Human neuropsycho logy. W iley. New York.23. BUC K . C. K. H. PRIBRA M.943. Localized sw eating as part of a Localized convul-sive seizure. Arch. Neurol. Psychiatry 5 : 456-461.24. KAADA . R. K . H. PRIBRAMJ . A. EPSTEIN.949. Respiratory and vascular re-sponses in monkeys from temporal pole insula orbital surface and cingulate gyrus.J . Neurophysiol. 12: 347-356.25. PRIBRAM. H. P. D. MA CLE AN .953. Neuronographic analysis of medial andbasal cerebral cortex. 11. Monkey. J . Neurophysiology 16: 324-340.26. NEAFSEY . J . 1990. Prefrontal cortical control of the autonomic nervous system:Anatomical and physiological observations. I n The P refrontal Cortex: Its S tructureFunction and P athology. H. B. M. Uylings r a l . Eds.: 147-166. Elsevier. NewYork.27. PRIBRAM . H . 1987. The subdivision of the fron tal cortex revisited. I n The F rontalLobes Revisited. E. Perecman Ed.: 1-39. IRBN Press. New York.28. NAUTA . J. H. 1971. The problem of the frontal lobe: A reinterpretation. J Psychi-atr. Res. 8: 167-187.29. TEUBER . L. 1964. The riddle of the frontal lobe function in man. I n The FrontalGranular Cortex and B ehavior. J. M. Warren K. Akert Eds.: 410-444. McGrawHill. New York.30. GOLDMAN-RAKIC. 1995. Ann. N.Y. Acad. Sci. This volume.31. UNCERLEIDER. G. M. MIS HK IN.982. Two cortical v isual system s. I n The analy-sis of visual behavior. D. J . Ingle R. J . W . Mansfield M. A. Goodale Eds.:549-586. MIT Press. Cambridge MA.32. M ISH KI N . 1982. A memory system in the monkey. Philos. Trans. R. Soc. Lond.B 98: 85-95.33. SQUIRE . R. 1986. Mechanisms of memory. Science 232: 1612-1619.34. PAN DY A . N. B. S E L ~ E RH. BARBAS.988. Input-output organization of theprimate cerebral cortex. I n Comparative Primate Biology Vol. 4: Neurosciences.:39-80. Allen Ardlis Inc . New York.35. PA ND YA . N. C. L BA RN ES . 987. Architecture and connections of the frontallobe. I n The Frontal Lobes Revisited. E. Perecm an Ed.: 41-72. IRBN Press. NewYork.36. W ER NE R . 1957. The comparative psychology of mental development. Harper. NewYork.37. BROWN . 1987. The microstructure of action. I n The Frontal Lobes Revisited. E.Perecman Ed. IRBN Press. New York.38. TU C K E R . M. 1992. Developmen t of emotion and cortical networks. I n MinnesotaSymposium on Child Development: Developmental Neuroscience. M. GunnarC. Nelson Eds. Oxford University Press. New York.39. D E R R Y B E R R Y. D. M. T U C K E R 991. The adaptive base of the neural hierarchy:Elementary motivational controls on network function. I n Nebraska Symposiumon Motivation. R. Dienstbier Ed. Un iversity of Nebraska Press. Lincoln NE .i 40. PANDYA . N. E. H. YETERIAN.985. Architecture and connections of corticalassociation area s. I n Cerebral Cortex. Vol. 4. Association and auditory cortices.A. Peters E . G . Jones Eds.: 3-61. Plenum Press. New York.41. DERRYBERRY. D M. TUC KER.991. The adaptive base of the neural hierarchy:Elementary motivational controls of network function. I n Nebraska Sym posium onMotivation. A. Dienstbier Ed .: 289-342. Unive rsity of Nebraska Pres s. LincolnNE.42. TU CK ER . M. D. DERRY BERRY .992. Motivated attention: Anxiety and the frontalexecutive functions. Neuropsychiatry Neuropsychol. Behav. Neurol. 5: 233-252.1

8/13/2019 K. Pribram T-192

23/25

TUCKER t 01 : SELF REGULATION 237

of the frontal cortex in sequential motor and learning tasks. Hum. Neurobiol.4: 143-154.FUSTER,. M. 1985. The prefrontal cortex and tem poral integra tion. I n Cerebral Cor-tex, Vol. 4. Association and Auditory Cortices. A. Peters E. G . Jones , Eds.:151-177. Plenum Press. New York .B U C H A N A N ,. L. D. POW ELL.993. Cingu lothlamic and prefrontal control of auto-nomic function. I n Neurobiology of the Cingulate Cortex and Limbic Thalamus.B. A Vogt M. Gabriel, Eds.: 38 14 14 . Birkhauser. Bos ton, MA.L ~ D o u x ,. E . 1991. Inform ation flow from sensa tion to em otion: Plasticity in neuralcomputation of stimulus value. I n Learning and Computational Neuroscience:Foundations of Adaptive Netw orks. M. Gab riel J. Moore, Eds.: 3-51. MIT Press.Cambridge, MA.LEHRMITTE,., B. PILLON M. SERDARU.986. Human autonomy and the frontallobes. Part I. Imitation and utilization behavior: A neuropsychological study of 75patients. Ann. Neurol. 19: 326-334.PRIBRAM,. H. 1991. Brain and Perception: Holonom y and Structure in Figural Processing. Erlbaum. Hillsdale, NJ.K LU VE R, . P. C. BUC Y. 939. Preliminary analysis of functions of the temporallobes in monkeys. Arch. Neurol. Psychiatry 42: 979-1000.P A N D Y A ,. N. E. H . YETERIAN.984. Proposed neural c ircuitry for spatial memoryin the primate brain. Neuropsychologia 22: 109-122.SPEVACK,. K. H. PRIERAM.973 A decisional analysis of the effects of limbiclesions in monkeys. J. Com p. Physiol. Psychol. 82: 211-226.DAMASIO,. R., G. W. VANHOESEN J. VILENSKY.981. Limbic-motor pathwaysin the primate: A means for emotion lo influence motor behavior. Neurology 31:60-84.L ~ D o u x , . E. 1987. Emotion. I n Handbook of Physiology. Sect. 1: The .NervousSystem. Vol. 5. Higher Functions of the Brain, Part I., F. Plum, Ed.: 419-459.

American Physiological Society. Bethesda, MD.MACLEAN,. D. 1993. Introduction: Perspectives on cingulate cortex in the limbicsystem. I n Neurobiology of the Cingulate Cortex and Limbic Thalamus. B. A . VogtM. Gab riel, Eds.: 1-15. Birkhauser. Boston, MA .VOGT,B. A., D. N. PAN DY A D. L. ROSENE . 987. Cingulate cortex of the rhesusmonkey. I. Cyto architecture and thalamic afferents. J. Comp. Neurol. 262:256270.VOGT,B. A., D. M. FINCH C. R. OLSON.1993. Functional heterogeneity in thecingulate cortex: T he anterior executive and posterior evaluative regions. C ereb.Cortex 2: 435-443.VOGT, B. A. D. N. PA ND YA . 987. Cingulate cortex of the rhesus monkey. 11Cortical afferents. 1.Comp. Neurol. 262: 271-289.PANDYA,. N., G. W. VANHOESEN M.-M. MESULAM.981. Efferent connec tionsof the cingulate gyms in the rhesus monkey. Exp. Brain Res. 42: 319-330.DEV INSK Y, D. LUCIANO.993. The contributions of cingulate cortex to humanbehavior. I n Neurobiology of the Cingulate Cortex and Limbic Thalamus. B. A.Vogt M. Gabriel, Eds.: 427-556. Birkhauser. Boston , MA .M ESU LA M , . 1981. A cortical network for directed attention and un ilateral neglect.Ann. Neurol. IO 4): 309-325.MACLEAN,. D. 1990. The Triune Brain in Evolution: Role in Paleocerebral Func-tions. Plenum Press. New York.PLOOG,D. 1981. Neurobiology of primate audio-vocal behavior. Brain Res. Rev. 3:35-61.BEAR,D. M. 1983. Hemispheric specialization and the neurology of emotion. Arch.Neurol. 40: 195-202.H E I L M A N ,. M. T. VANDENABLE. 1980. Right hem isphere dominance for atten-tion: The mechanism underlying hemisphere asymmetry of inattention neglect).Neurology 30: 327-330.PEARLSON,. D. R. G. ROBINS ON.981. Suction lesions of the frontal cerebral

8/13/2019 K. Pribram T-192

24/25

XX

XY

YO

YY

100

101

ANNALS NEW YORK ACADEMY OF SCIENCES

cortex in the rat induce asymmetrical behavioral and catecholaminergic responses.Brain Res. 218: 233-242.FLOR-HENRY,. 1979. On certain aspec ts of the localization of cerebral systems regu-lating and determining emotion. Biol. Psychiatry 14: 677-698.FOG EL, . S F. R. SPARADEO.985. Focal cogn itive deficits accentuated by depres-sion. J . Nerv. Ment. Dis. 173 1): 120-124.BRU M BA CK ,. A., R. D. STATON H. WILSON . 980. Neuropsychological study ofchildren during and after remission of endogenous depressive episodes. Percept.Mot. Skills 50 0): 1163-1 167.LIOITI,M. D. M. TUCKER.992. Right hem isphere sensitivity to arousa l and depres-sion . Brain Cognition 18: 138-151.BOROD,. C. 1992. Interhemispheric and intrahem ispheric control of emotion: A focuson unilateral brain dam age. 3 Consult. Clin. Psychol. 60: 339-348.S A C K E I M ,. A., R. C. G UR M. C. SA UC Y.978. Emotions are expressed more

intensely on the left side of the face. Science M : 34-436.SA FE R, . A. H. LEVEN THAL.977. Ear differences in evaluating emotional tonesof voice and verbal content. J Exp. Psychol. Hum. Percept. Perform. 3 1): 75-82.GOI.I>STEIN,. 1952. The effect of brain damage on the personality. Psychiatry IS:245-260.ROB~NSON,. G., K. L. Kueos, K. RAO T R. P RIC E. 984. Mood disorders instroke patients: Importance of location of lesion. Brain 107: 81-93.G A I N O I T I ,. 1972. Emotional behavior and hemispheric side of the lesion. Cortex8: 41-55.S A C K E I M ,. A., M. S. GR EE NB ER G,. L WEIMANl al 1982. Hemispheric asymm e-try in the expression of positive and negative emotions: Neurologic evidence. Arch .Neurol. 39: 210-218.T U C K E R ,. M. 1981. Lateral brain function, emotion, and conceptualization. Psychol.Bull. 89: 19-46.BRODAL,. 1969. Neurological Anatomy in Relation to Clinical Medicine. OxfordUniversity Press. New York.R I N N , . E. 1984. The neuropsychology of facial expression: A review of the neuro-logical and psychological mechanisms for producing facial expressions. Psychol.Bull. 95: 52-77. I.M O N RA D K RO H N ,. H . 1924. On the dissociation of voluntary and eniotional innerva-tion in facial paresis of central origin. Brain 47: 22-35.BEAR, . M. P. FED IO. 977. Quan titative analysis of interictal behavior in temporallobe epilepsy. Arch. Neurol. 34: 454-467.DAVIDSON,. J., G. E. SCHWARTZ,. SARONl al 1979. Frontal versus parietal EEGasymmetry during positive and negative affect. Psychophysiology 16: 202-203.T U C K E R ,. M., C. E. STENSLIE,. S. ROTH S SHEARER.981. Right frontal lobeactivation and right hemisphere performance decrement during a depressed mood.Arch. Gen. Psychiatry 38: 169-174.DAVIDSON,. J . 1984. Affect, cognition and hemispheric specialization. n Emotion,Cognition and Behavior. C. E. Izard, J . Kagan R. Zajonc, Eds. Cambridge Uni-versity, Press. New York.HENRIQUES,. 9 . R . J . DAVIDSON.990. Regional brain electrical asymmetriesdiscriminate between previously depressed and healthy control subjects. J . Ab-norm. Psychol. 99: 22-31.K N I G I I T ,. T., S. A. HIL LY AR D,. L. WOODS H. J . NEVILLE.981. Th e effects offrontal cortex lesions on event-related potentials during auditory selective a ttention.Electroencephalogr. Clin. Neurophysiol. 52: 571-582.T O M A RK E N ,. J . R. J . DAVIDSON.rain activation in repre sso rs and non-repressors:Implications for affective regulation. J . Abnorm. Psychol. In press.DAVIDSON,. J . 1994. Role of prefrontal activation in the inhibition of negative affect.

8/13/2019 K. Pribram T-192

25/25

TUCKER et al.: SELF REGULATION 39

book of Psychophysiology: Emotion and Social Behaviour. H . Wagner T .Manstead Eds. John Wiley. New York.112. STARKSTEIN E. R. G. ROBINSON T. R. PRICE. 987. Comparison of corticaland subcortical lesions in the production of poststroke mood disorders. Brain 11 :1045-1059.113. JOHANSON. M. J. RISBERG . SILFVERSKIOLDG. SM ITH . 986. Regional changesof cerebral blood flow during increased anxiety in patients with anxiety neurosis.n The Roots of Perception. U Hentschel G. Smith J. G. Draguns Eds. North-Holland. Amsterdam.114. PA RD O . V. P. J. PAR DO M. E. RAICHLE.993. Neural correlates of self-induceddysphoria. Am. J. Psychiatry 150: 713-719.115. BAXTER.. R. M. E. PHE LPS . C. M AUIOTTA B. H. GA ZE. 987. Local cerebralglucose metabolic rates in obsessive-compulsive disorder. Arch. G en. Psychiatry44: 21 1-218.116. DREVETS . C. T 0 IDEEN . L. PRICE . K. PRESKORNl a/ 1992. A functionalanatomical study of unipolar depression. I . Neurosci. 12: 3628-3641.117. GUR R. C. 1994. Personal comm unication.

18. AMERICANSYCHIATRICSSOCIATION.994. Diagnostic and Statistical Manual of Men-tal Disorde rs 4th edit. Am erican Psychiatric Press. W ashington DC.119. Llo rrl M. D. M. TU C K E R .994. Emotion in asymmetric corticolimbic networks.I n Human Brain Laterality. R. J. Davidson K. Hugdahl Eds. Oxford UniversityPress. New York.120. BROWN . W. 1989. The natu re of voluntary action. Brain Cognition 1 : 105-120.