The

Kenneth

Neurobiology
M. Heilman, M.D.

of

Emotional

Exp enence

The author discusses a neurological model of a modular network that mediates emotional experience. According to this theory, emotional experience has three components: valence (positive and negative), arousal, and motor activation (approach, avoid, neither). In this model, the cortex is critical in regulating activities of the limbic system, basal ganglia, and reticular system. The frontal lobes are important for valence: the left mediates positive emotions, the right negative emotions. The right hemisphere, especially the parietal lobe, is important in activating arousal systems, and the left hemisphere modulates inhibition of these systems. The right hemisphere is also critical in motor activation. The frontal lobes, especially the orbitofrontal portions, mediate avoidance behaviors, and the parietal lobes mediate approach behaviors. The cortical areas discussed have rich interconnections and are also closely connected with the limbic system, basal gang/ia, and reticular systems. Emotional experience may depend on the patterns of neural activation in this modular network.
(The Journal of Neuropsychiatry 1997; 9:439-448) and Clinical Neurosciences

A
but

lthough

almost

everyone

knows

what

emotions

are, the word emotion is a psychological construct that remains difficult to define. Perhaps emotions are difficult to define because they are not objects or things rather are complex, There are at least three there and system. multicomponential major components processes. of emotion.

First, havior ous through including

is emotional behavior, changes in the viscera Second, there tone of voice expressions. of

including overt beand autonomic nervcommunication and gestures, is emotional although motivating

is emotional

word, facial

(prosody), Third, there

feeling or experience. subjective, is one

Emotional the major

experience, factors in

human behavior. It is not only the direct experience of emotion that motivates behavior, but also the knowledge that certain stimuli, situations, and actions could in the future reproduce emotional states. In this review, I explore the neural basis experience. Building models may help Although of the neural tional experience emotional states. us understand studies based of emotional basis of emoabnormal on the ablaI do such

tion paradigm were not discuss here the as panic feedback and depression. and central

used to help form psychiatric affective

this model, disorders

I first briefly review theories and the more and I provide explain the discuss

the classic recent revi-

sions of these theories, theories cannot fully tional experience. I then

evidence that these neural basis of emoa distributed modular

From Medicine, Medical Heilman,

the

Department and Center, Box

of Neurology, Service, Florida.

University Department Address

of Florida of Veterans correspondence

College

of

Neurology Gainesville, 100236, University

Affairs to Dr.

of Florida,

Gainesville,

FL 32610-0236.

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network posed volves activation.

theory

of

emotional

experience.

The

proinmotor

model suggests the components

that emotional experience of valence, arousal, and

non who

argument studied

was not patients

fully with either

supported spinal

cord

by Hohmann,2 injuries and

found that patients with transection did experience Cannon, but that patients stronger Higher efferent nervous

high or low spinal cord emotions as predicted by with lower lesions reported higher likely lesions. to affect

FEEDBACK Facial Feedback

THEORIES Hypothesis that he Darwin who also gives violent believed that gesthe

emotions than those with cervical lesions would be more control of the viscera systems efferent

and injure the autonomic output. Therefore, Hohsupport be noted for that the the and with possibe little

Charles Darwin2 noted ture increases his rage.

manns visceral vagus cervical this from

observations provide partial feedback theory. It should also nerve is the spinal cord ability viscera. the primary transection to provide However, of autonomic that brain the even control viscera

means by which we express and Ekman et al.4 performed facial seven emotional to nine

emotions are cross-cultural

innate. Izard3 studies of that the appeared same to

visceral afferent nerve, would not interfere the brain if feedback there have above, afferent paradigm, might with was

expression and found emotional facial expressions

nerves

feedback

be universal, hypothesis Tomkins56 facial feeling. pressions providing pothesis. There the facial example, valence ones emotion tary facial facial are, emotions

thereby providing support that emotional expression posited to that the it was brain the that

for may

Darwins be innate. of these emotional facial exthereby hywith For the altering one volun-

ble, with a loss to feed back. Cannon afferent emotional the vagus addition, input

feedback induced

thought to the

insufficient in inducing however, nerve. Katkin In

to be important mentioned a visceral detection

Laird7 and

experimentally found that patients support many for

manipulated felt emotions, the facial

experience. As nerve is mainly using a heartbeat

some

feedback problems experience. emotion, by express that emotional can

however, one

unresolved

feedback when of this while

theory of emotional is feeling a strong cannot and another. cannot be a person entirely changed

et al.13 not only found that some normal subjects can accurately detect their heartbeats, but also that the subjects who had the strongest emotional responses to negative slides were the subjects who were able to detect their own heartbeats.14 that because the different emotions, could not account same visceral feedback of for the varibe Ax5 asCannon responses these visceral also thought occur with responses

emotion feeling

expression, emotions

It is possible control

experience because the innervatory patterns of voluntary facial gestures are different from those that occur naturally. Patients with pseudobulbar palsy may express strong facial emotions that they are not feeling,89 but it is possible that these patients brain lesions also interrupt of the facial feedback nerve to the motor brain. unit, a change suggested, feedback Patients even when with the diseases problem

ety of emotions demonstrated sociated Thus, feedback have work. with Cannons theory

that humans that different different arguments of emotional how neocortex

experience. However, bodily reactions can

emotions. fail to refute the visceral experience. However, we this and feedback limbic system cortex may play

not yet discussed In humans, the

is bilateral, do not report it is possible, as Darwin sions this may influence embellish is not from

of emotion. Although that facial expresit remains from the possible facial central that muscles, nervous

emotions,

a critical role in the analysis and interpretation ous stimuli (see Heilman et al.16 for review). viscera respond to complex stimuli (such there enable nomic The the must the be efferent cortex to descending control the neural viscera

of variBecause the as speech), systems via the system. components, The descendfrom the projecincluding that auto-

but rather is mediated system by associative

Visceral Feedback

totally within networks.

Hypothesis

nervous autonomic

system and the endocrine nervous system has two and the parasympathetic. receive hypothalamus and paralimbic neurons and the limbic The vagus. situated

sympathetic

William James#{176} proposed emotion induce changes self-perception of these duces This who brain, not emotional feedback argued eliminate that as occurs experience. theory the with emotional

that in the visceral was

stimuli viscera changes

that provoke and that the is what proby viscera injuries, the Cannon,1 from the does Can-

ing sympathetic hypothalamus, tions from many the amygdala. nerve is the motor nucleus

projections receives areas,

challenged of the spinal cord

most important parasympathetic The vagus originates in the dorsal in the heart. brainstem and projects not direct to only proThe amygdala but also sends

separation cervical experience.

However,

the viscera, including the projects to the hypothalamus,

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jections motor amygdala system. Although part

to the nucleus The

nucleus of

of the solitary tract the vagus. In this influence receives may to

and the manner

dorsal the

may directly amygdala the limbic and insula receive amygdala

the parasympathetic neocortical input. be influence the most the important autonomic

their autonomic response was reduced, they showed no differences in the experience of anticipatory anxiety.21 In addition, the strongest argument against the cognitive-visceral arises strong temporal epileptic first and ence theory from emotions lobe or patients, the feedback observations (such as fear) theory of or attribution patients who with theory have medial

of the

system

associated

nervous including induce structures mentioned,

system the autonomic also

viscera, stimulation and orbitofrontal and visceral input to feedback from the changes, the

of other areas, cortex, can also and neocortex. nerve these As that is in to

amygdala seizures. In many of these the emotional experience is often the in these changes before and the Singer patients come cannot after The account cognitive the for experithese attribution set

symptom. rather than

Therefore,

autonomic/visceral of Schacter

in regard

major

experience.

carries visceral afferent information back to the brain the vagus. These vagal afferents terminate primarily the nucleus of the solitary tract. This nucleus projects the central nucleus of the amygdala, nucleus of the amygdala projects nuclei and the insula. The amygdala project to several neocortical areas, poral, parietal, and frontal lobes. Luria and Simernitskaya7 thought hemisphere might be more important perceiving visceral changes. To test Davidson et al.18 gave mal individuals. They influenced the right by heart hemisphere

observations.

and the central to other amygdala and insula, in turn, including the temthat than this the right the left in postulate,

CENTRAL To account

THEORIES for that emotional stimuli experience, enter which can the activates in turn brain Cannon and are the hypoactivate the

proposed transmitted thalamus.

afferent

to the thalamus, The hypothalamus

a variety of tapping tests to norfound that the left hand was more than may the be right superior hand, at suggesting detecting in by visceral superiority replicated the

endocrine system and and it is these systems changes nomic and aid perience, thalamus LeDoux pothalamic in and

the autonomic that induce

nervous system, the physiological to Cannon, autoprimarily adaptive Emotional exby the hypoMore recently, thalamic-hythe amygdala role in for

rate

the viscera. According visceral activation are survival of the to Cannon, back to the have modified circuit did

in the

organism. is induced cortex. Cannons

heartbeat. Unfortunately, the detection of heartbeat other There investigators. are other observations cannot epinephrine

this left hand has not been for account. into the not which

according feeding et al.22 emotion

to include not propose

feedback theory ra#{241}on19injected quired subjects. barrier, viscera. epinephrine tional Schacter experimental cally induced and as

For subjects

example, Maand then in-

fear conditioning. Cannon and

LeDoux

a critical

to the nature of Epinephrine does

emotion felt by these cross the blood-brain nervous that with as system injections genuine if feelings. into not and of emo-

but it affects However, were experiences,

the autonomic Maranon found not but associated rather with

the cortex in the some conditioned Doux, may induce tion, the many there neocortex stimuli,

interpretation of stimuli. stimuli, similar to those emotion without cortical evidence for interpreting stimuli that are For example, spoken strong emotions. orthographic, lexical, by the the primarily that the

Although used by Leinterpretain humans meaning complex and These and written stimuli semantic of and

is overwhelming is critical especially learning. engender that

Singer2#{176}also injected subjects and reported autonomic and visceral unless this set. Although

epinephrine that pharmacologiactivation did

rely on past stimuli may need processing

phonological,

produce an emotion nied by a cognitive

arousal Schacter

was accompaand Singers

is mediated et

left cerebral

study suggested that visceral feedback combined with centrally mediated cognition is important for emotional experience, observations in our laboratory did not entirely support Recently, these findings. we tested the autonomic-visceral if the right visceral hemisphere changes. feedback

cortex. Recently, Ross sphere is important

al.23 posited that for primary emotions

right hemi(such as anger

or fear) and the left (such as embarrassment). observation hemispheric emotional curred subjects ened, earlier told but when that response some anesthesia

is important for social emotions They based this theory on the patients (the to Wada traumatic undergoing test) events changed that had selective their oc-

theory to learn role in perceiving pation normal lesions paradigm, control had

plays a dominant Using a shock anticiwhen compared with with right hemisphere response. Although

we found that subjects, patients autonomic

in their lives. of an incident his right

For example, where he was was

one of their very frightanesthetized,

a reduced

hemisphere

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he

stated

that did

he

felt not

embarrassed. demonstrate

However, that left social emotions. are alternative observations,

Ross hemisphere

and

co-workers

cating module, network mines that activation

a behavior or the orchestra contains valence controls with three (pleasant approach

experience. is the

If the network.

violinist is the The proposed that deteranother motor

dysfunction led to a loss of absence of such evidence, there tions of Ross and colleagues will be discussed below. Cannons diencephalic-hypothalamic Douxs diencephalic-limbic Ross and colleagues left-right not only fail to account for emotion explain tions. in response how humans to complex can

In the explanaand model, these Le-

major modules, one versus unpleasant), and a third or avoidance that mediates

arousal,

behaviors.

(amygdala) model, and social emotional theories how humans experience stimuli, but a variety also fail of emoto

Valence

Goldstein28 hemisphere and sad. He

reported lesions called

that often this

aphasic appeared

patients anxious, syndrome

with left agitated, the catawith he rehad a normal such that Babinski,3#{176} a

behavioral

experience

strophic reaction. Gainotti2#{176} studied right or left hemisphere strokes. Like ported catastrophic that patients reaction, to serious or and with but cognitive Denny-Brown hemisphere indifferent left he hemisphere thought and In

160 patients Goldstein, lesions this was deficits

MODULAR There variety One

THEORY in which the experiences. is that the brain brain may may contain modulate specialthere one a

response as aphasia

physical contrast, lesions or often even

hemiparesis.

are two ways of emotional possibility

H#{233}cean et al.,31 patients either

et al.32 noticed appeared euphoric.

with right inappropriately confirmed patients unawareness

ized emotional systems (devoted would be a special system for for happiness, emotion was and so forth. This uniquely mediated. is not uniquely that mediates

systems), fear, one

so that for anger,

Gainotti29 that these denial or

these observations indifference might of illness

but suggested be related to the (anosognosia) that

would imply that each A second possibility is one mediated-that emotion may the not

that each emotion neural apparatus only even play a role nonemotional

often is associated with right Although Gainotti proposed logical some patients responses of the with right to their and own emotional

hemisphere lesions. that patients psychoillness hemisphere may observed lesions, account between there for

in other emotions, but may functions (nondevoted

also mediate systems).

asymmetries left

The nondevoted dimensional view

systems view is consistent with the of emotion favored by many cogni-

tive emotional theorists. Wundt24 proposed that emotional experiences vary in three dimensions: quality, activity, and excitement (arousal). Similarly, Osgood et al.25 performed factor analyses on verbal assessments of emotional judgments for by and found that the variance could valence arousal be accounted (positive/negative, (calm/excited), of control). three major dimensions: pleasant/unpleasant),

are additional reports that a psychological reactive theory cannot entirely explain. Terzian33 and Rossi and Rosadini34 studied the emotional reactions of patients recovering from selective hemispheric barbiturate-induced anesthesia (the Wada test). These investigators noted that whereas right carotid injections were often associated with euphoria, barbiturate injections into the left carotid artery strophic reactions. causes only transient fore seems unlikely reactive depression the test. In addition, were often associated The Wada test is a diagnostic hemiparesis that that we and aphasia. would only this procedure occurred during have seen right with test catathat a of

and control or dominance (in control/out Using this type of multidimensional scale, different high emotions. arousal, For example, fear and out of control; arousal. Frijda of emotion and compo-

It therecause a part

one can define the would be unpleasant, sadness could also explored found that

hemisphere-

be unpleasant the cognitive readiness

and low structure was

action

an important

nent. Studies using a variety of techniques with normal subjects27 have supported this dimensional view. The modular theory posits that the conscious experience of emotion is mediated by anatomically modular networks. By modular, we mean works that cannot mean independently. modules are be influenced the sum total However, encapsulated by other of modules this in such systems. that are does a way distributed that a system not that mean they

damaged stroke patients who appear to be emotionally indifferent but do not demonstrate anosognosia or verbally explicit denial of illness. The catastrophic-depressive reaction associated with left hemisphere lesions is seen most commonly in patients who have anterior (frontal) It is possible that the hemispheric tries reported by Gainotti disorder Tucker that ability experience. reported their and a communication emotional sulam jects lost rather perisylvian emotional others may than be Ross lesions.3536 asymmerelated and to in Medifferences

et al.37 and

By network, we critical in predi-

right hemisphere-damaged to express emotional

subprosody.

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Patients and unable

with

left

hemisphere themselves

lesions using

may rely

be

aphasic

is not hemisphere To

clear learn

that primary if there

Ross are

et emotion

al.

fully

explored physiological

this

right

to express

propositional more on right affective commay emotional intone facial

hypothesis. changes of investigastudies of pa-

speech. To express hemisphere-mediated, munication, their speech expressions. patients may emotional tional. sions In may and more

feelings, they may nonpropositional therefore heavily and these use left need more

discrete

patients

associated tors have tients with investigations left frontal However, ity in the and thalamus. Davidson

with depression, several groups conducted functional imaging primary depression. have noted a decrease lobe as well as the left Drevets left prefrontal et al.46 and and Raichle45 cortex, Tucker47

Because these have a greater they may

hemisphere-damaged to use these expressive to be highly emoleleft and

Several of these of activation in the cingulate gyrus.4344 increased basal activganglia, the hemi-

systems,

appear

found amygdala, investigated

contrast, patients with right hemisphere have more difficulty than patients with disease in expressing Therefore, may emotional faces

hemisphere

emotional speech prosody. with left hemisphere-damaged right hemisphere damage Although sion may tions by hemispheric account for Goldstein,28

when compared patients, those with appear to be indifferent. expresobservathey

spheric valence hypothesis with electrophysiological firmed region tions moods, the ablation studies,

by studying techniques. suggesting

normal subjects Their studies conthat the frontal contributhan left negative activaand Fox left and right to labora-

defects of emotional some of the behavioral Babinski,3#{176} and Gainotti,29

of each hemisphere makes to emotional experience: activation and greater left is than

asymmetric greater right with hemisphere the right

hemisphere tion is associated Unfortunately, hemispheres Davidson positive avoidance

associated right moods. how

cannot explain the results of Gasparrini et al.,39 who administered the Minnesota Multiphasic Personality Inventory (MMPI) to a group of left and right hemisphere-damaged assess emotional aged patients left and were right and cognitive quire The spheric patients. experience. not The MMPI is widely used The left hemisphere-damaphasic. were MMPI or facial supported found In addition, balanced does not to the for re-

with positive it is not known may influence that are left related

emotional

valence.

severely

suggest emotions behaviors. the be

hemisphere-mediated to approach and emotions recently are related in our

hemisphere patients motor defects. The speech et al. They

hemisphere-mediated tory we studied proach-avoidance emotions can avoidance

negative However, relationship behavior. We associated with (G.

emotionally intoned findings of Gasparrini valence hypothesis.

expressions. the hemithat patients

of emotions and apfound that negative both approach and et al.: valence annual Dissociation in the meeting Boston, both with exof

with left hemisphere tion of the depression hemisphere disease differences and others disorders deficit.

disease showed a marked elevascale, whereas patients with right did not. Therefore, the right-left by Gainotti expressive or cognitive

behaviors

P. Crucian

of behavioral action and emotional pression of affect. Presented at the the American April, 1997). negative and anger For Academy example, but fear with

in emotional behavior observed cannot be attributed to emotional or to the severity of the motor

of Neurology, fear and anger is associated approach.

MA, have a this the that

valence,

avoidance how such

is associated

In addition, not explain organized

Starkstein et al.4#{176} also sociated with stroke and of stroke that patients the had depression found frontal to the severe

studied emotional changes asalso found that about one-third a depression. was lesions, lesion Many associated but was They with also that located, of the not both the the only left closer more with anxwere

approach-avoidance two hemispheres they make proach-avoidance opposite

model does are differently contributions theory does not

to mood. explain

This aphow other

and left caudate frontal pole the was the depression. lesions patients

emotions are mediated, and it also role of other areas in the brain, such Tucker and Williamson49 think be related cholinergic more lence asymmetries may trol of neuropharmacological hemisphere being more and the right hemisphere that may appear left The et al.5#{176} reported hemispheres imaging, hemisphere it binding, binding. they

does not explain the as the limbic system. that hemispheric vaconleft to asymmetrical systems, the and dopaminergic changes stroke. strokes serotonergic in the Using in the

patients

left hemisphere ious. In contrast,

and depression were also with right frontal lesions

often indifferent or even euphoric. investigators agree that after stroke pression with left Milner42 found than right hemisphere et al.4 and asymmetries cussed sphere hemisphere could in prior et al.23 social

However, not all there is more delesions. House

noradrenergic. after

Mayberg two PET right

not replicate the emotional reports. In addition, as disposited emotions that emotions. the and left the However, hemiright

pharmacologic be different that to increase

reported hemisphere lower the

whereas

above, Ross mediates mediates

receptor

all primary

strokes serotonergic

lower serotonergic binding, the more

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severe clinical

the

depression. that influence may mechanism mood also

Although

it is well

known systems

from may

uli

being

associated stimuli.59

with

higher

firing

rates

than

the relay sen-

psychiatry

neurotransmitter on mood and induce either by which the

unimportant

have a profound in these systems dysphoria, the cal changes induce The frontal lobes liinbic system. The

that changes euphoria or pharmacologito the lobe

Sensory information projects nuclei. From the thalamus, this

to the thalamic modality-specific

remains unknown. have strong projections and medial frontal

sory system projects to the primary sensory cortices. Each of these primary sensory cortices (visual, tactile, auditory) projects only to its association cortex. For example, projects dality-specific areas such and poral gence lobe.6 lus Although the determination of the may be mediated by modality-specific novelty of a stimusensory assoorbitofrontal) sulcus.6#{176}Both areas project Brodmann to Brodmann association as the frontal and both area 17, the primary area 18. Subsequently, areas cortex converge (periarcuate, banks of the polymodal inferior visual these cortex, mo-

dorsolateral

project primarily to the cingulate gyrus; the orbitofrontal cortex, via the uncinate fasciculus and anterior temporal Although important means tively known. lobe, has strong connections such emotions and limbic left to as the such frontal structures the amygdala. are the selecunlimbic structures in negative by which influence the these right amygdala as fear, lobes remain

on polymodal prearcuate, superior temconverparietal

of these sensory to the supramodal

Arousal The term difficult

arousal, to define.

like

the

terms and

attention whereas

and an

emotion, aroused stimand several

is

Behaviorally, alert, organism process

organism is awake, uli, an unaroused not prepared to

prepared is lethargic

to process to comatose has

ciation cortex, determination of the significance of a stimulus requires knowledge as to both the meaning of the stimulus and the motivational state of the organism. The motivational state is dependent on at least two factors: goals. limbic immediate It has system, been together biological demonstrated with the needs that and portions long-term of the moni-

stimuli.

Arousal

physiologic definitions. arousal usually refers or the priately ally propensity activated. measured

In the central to the excitatory to discharge imaging, of

nervous system, state of neurons when arousal flow, approis usuand

hypothalamus,

of neurons In functional by increases

tor the internal milieu fore, limbic input into stimulus immediate significance biological

and develop drive states. Thereregions important in determining may needs. provide Regarding information long-term about goals,

blood

electrophysiologically it lion of the EEG or by evoked potentials. Outside arousal usually refers to nervous system and the Arousal pear modular original anatomy lar network.51 network, articles. of this and attention This but Much network human more of this inferior article to be mediated

is measured by desynchronizathe amplitude and latency of the central nervous system, activation of the sympathetic viscera, including the heart. are intimately limbic one provides of what initially linked reticular should refer about studies an overview we know came from and apmoduof this to the the of lehas asso-

the frontal lobe has role in goal-oriented

been demonstrated to play a major behavior and set development,6263

and frontal input into the attentional-arousal systems may provide information about goals that are not motivated by immediate biological needs. Studies of cortical connectivity temporoparietal with also portions with the in monkeys region not have only system demonstrated has strong (cingulate that connections gyrus) the but

by a cortical for details

of the frontal

limbic cortex.

Stimulation of the mesencephalic (MRF) in animals induces behavioral arousal.M In contrast, coma, and unilateral sphere aroused.65 discussed cance, MRFP influence remain possible cortical ascending but The to be The above bilateral lesions

reticular formation and physiological induce hemihypocortex signifithe areas cortex three an

monkeys and sions. However, confirmed lesions ciated with in monkeys ated cordings appear important with much of the

patients recently ablation parietal

with discrete brain functional imaging research. lobe are most In humans, often

lesions of the MRF cause the ipsilateral and physiologically and supramodal determine stimulus

behaviorally polymodal not only by the

disorders of attention and temporoparietal ablations attentional disorders.57 in the postulate Unlike parietal that neurons

arousal,5556 and are also associPhysiological reis

also modulate exact means the MRF and However,

arousal which MRF there the and

by influencing these cortical influences are MRF Lewis67 at may The the least describe

from neurons to support the in attention.

lobes of monkeys the parietal lobe in the primary neurons cortex, and

unknown. mechanisms processing. cholinergic

by which First, Shute reticular

influence nucleus input projec-

sensory cortex, these etal lobe, a supramodal association between cance of the stimulus

attentional association

in the panshow an signifistim-

formation.

the rate of firing to the monkey-the

the relevant

basalis, which is in the basal forebrain, receives from the reticular formation and has cholinergic

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tions appear sivity.68 activity

to the

entire the

cortex. MRF thalamic that lateralis regions by

These may

cholinergic neuronal influence also

projections responthe Steriade cortical and

to be important Second, through

for increasing projections.

trol of arousal tion that the activating hemisphere stimulus with left Perhaps inhibitory ticular Motor Some ness surprise). or this action

may right

be related hemisphere

to privileged has with portions role in

communicathe reticular of the right computing

system. may significance. hemisphere the left control activating

Alternatively, play a dominant

Glenn69 demonstrated such as centralis widespread can be reticular account cleus thalamus nuclei. sensory networks cortical activated formation. for cortical reticularis

nonspecific thalamic nuclei and paracentralis project to and these of the mechanism involves thin nucleus the thalamic mesencephalic that may thalamic envelops thalamic thalamic cortical is significant inhibinuclei nervin the perisweating if there and left subjects. with noof sweating, help nuthe relay relay of limbic nuclei

The increased arousal associated lesions also remains unexplained. hemisphere over the system. and Approach-Avoidance (for example, (anger, fear, with (approach) sadjoy, action, or right maintains some type hemisphere or the of re-

stimulation The third arousal

(NR).

This

Activation

and projects Physiologically, information.70 determine

to all the sensory NR inhibits the However, that a stimulus when

emotions do not call for action or satisfaction), but others do When may emotions be toward are the stimulus

associated

novel, corticofugal tory NR, thereby

projections allowing the

may inhibit the thalamic sensory cortex. autonomic

away from the stimulus emotion. Although one that are unpleasant pleasant emotions, avoidance with the we emotion are

(avoidance) would like

that induces the to avoid emotions induce and

to relay sensory information The level of activity of the

to the peripheral

and approach when we discussing and not relation to one would when one ones

situations that discuss approach the ones like does behavior plans to for

ous system usually mirrors the level of arousal central nervous system. One means of measuring pheral by were using autonomic the et differences arousal galvanic in the skin is to measure response. To control hemispheric hand learn

associated structuring

ones behavior in example, whereas that has ing induce anger, a propensity this emotion.

environment. For avoid situations angry, one that is inducis also associactivation to

become

Heilman hemisphere These ciceptive patients

al.71 studied patients with right damage as well as normal control presented these subjects

to approach the stimulus Joy, a positive emotion, use the term

investigators

stimuli (electric shock) with right hemisphere

and demonstrated that lesions had a reduced normal subjects subjects. Subsimilar findings. et al.73 also patients had a

ated with Pribram denote uli. We

approach behaviors. and McGuiness76 the physiological have posited that

arousal response when compared with and left hemisphere-damaged control sequently, other investigators reported For example, found that reduced Heilman esting patients greater Morrow et al.72 and right hemisphere-damaged

readiness motor

to respond to stimactivation or intention porlimbic The

Schrandt

is mediated by a modular network that includes tions of the cerebral cortex, basal ganglia, and system (see Heilman et al.54 for a detailed review). dorsolateral frontal motor preparatory from rons presented cells that in the have with lobe appears network.52 dorsolateral enhanced a stimulus that activity to be the Physiological frontal lobe when is meaningful and frontal from the

skin and finding.

response to emotional stimuli. However, his co-workers71 reported another interWhen compared with normal subjects, hemisphere response. lesions appear to have a Using changes in heart rate

hub of this recording reveals animal and preneuis

with left autonomic

as a peripheral obtained results Using physiological that in cases

measure of arousal, Yokoyama et al.74 similar to those using skin response. imaging, Perani et al.75 also found hemisphere left stroke there was also hemisphere. Unfortucontrol patients were the remains right left asymmetrical unknown. hemisphere hemispheres could corticofugal sysone conhemiBecause not

dicts movement.78 inputs from the

The dorsolateral cingulate gyrus that

lobes receive the posterior

of right

cortical association areas polymodal, and supramodal. rior neocortical areas may information about the and its spatial location. the cingulate but circuit) nonreciprocal also may

are modality-specific, Inputs from these posteprovide the frontal lobes with ncluding system only part Yakolovs its meaning (for example, of the Papez latlobe ganglia organbasal frontal the basal

metabolic depression of the nately, left hemisphere-damaged not reported. The mechanism control restricted interfere underlying of arousal to with the the

stimulus, The limbic is not input The caudate), which frontal information from

gyrus,
receives

which

circuit eral isms has

spheric lesions directly

provide state. connections

as to the

motivational

dorsolateral with which projects cortex.79

projections to the reticular tems corticipetal influence would have to propose that

systems of the the right

or the reticular left hemisphere, hemispheres

(for example, to the globus which projects

with the pallidus, back

in turn projects to the thalamus, The dorsolat-

to the

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EXPERIENCE

eral

frontal

lobes

also

have

extensive

connections of the These by their

with thalamus intralamiinfluence or by (yenfrontal The obthe nu-

iors

has

not

been

entirely

elucidated. of

Animals

with

fron-

the nonspecific (centromedian nar nuclei may

intralaminar nuclei and parafascicularis). gate motor activation especially portion

tal lesions show an increase Patients with left dorsolateral should induce creased arousal, to hostility and

aggressive behavior. frontal lesions (which

on the basal ganglia, influencing the thalamic tralis lobe

the putamen, of motor circuits

an emotion of negative valence, inand approach behaviors) are also prone anger.84 Patients with orbitofrontal leinappropriate and studies also limbic to be demonstrate cortex system important that, with demlesuch in in orbitofrontal sexof

lateralis pars oralis). Lastly, the dorsolateral has strong input into the premotor areas. that lesions gyrus, the of the dorsolateral basal ganglia, the thalamus that

sions are prone to irritability, anger, ual advances, and euphoria-jocularity,85 animals abnormal is closely as the emotional with ventral frontal behaviors. with that and manual patients areas are lesions The of the known approach connected amygdala experience. Chambers83 grasp with

servation cingulate clei, nesia motor The

frontal lobe, intralaminar

and the supports

ventrolateral the postulate

may all cause aidthis system mediates to play a special and lesions role in

activation. right hemisphere or that

appears

Denny-Brown contrast frontal onstrate sions, move eyes parietal eyes, addition, not withhold to the lesions, avoiding especially or show toward lesion, head, and unlike

demonstrated response panetal Patients associated lesions may with

motor activation demonstrated likely those sured initiate spheric

intention. Coslett right hemisphere with contralateral

Heilman54 are more than

to be associated

akinesia

responses.

parietal

of the left hemisphere. Howes reaction times (a measure of a response) lesion and of the demonstrated with slower However, be related in mediating hand that

and Boller8 meathe time taken to to a hemithan disrole Heilman right hemisphere

of the right side, may not a delay in moving their arms, a part but arms patients their response of these the toward with space that may ipsilateral frontal to stimuli, patients even lesions

only fail to heads, and the their In canwith stimuli severe deviate

ipsilateral

is opposite hemispace. who to more patients

lesions were left hemisphere cussed, of the this right

associated lesions. finding hemisphere may

reaction times as previously to the important arousal.

and Van Den Abe1182 measured times of normal subjects who directed found to either their that, independent right of

the reduction of reaction received warning stimuli or left hemisphere. the hand used, They warning

parietal lesions (neglect). These with right than

may be unable to respond avoidance responses are left hemisphere lesions.

stimuli delivered to the right hemisphere tion time to midline stimuli more than stimuli delivered to the left hemisphere. Some emotions iors, others with the portions of avoidance Denny-Brown behaviors and are associated with avoidance behaviors. the brain that mediate been entirely suggested have not Chambers83

reduced reacdid warning

SUMMARY In addition and central discussed against experience influence may use Doux. ences thalamus humans stimuli, We have the to reviewing theories of a central postulate some of the former emotional experience, theory. feedback Although is critical that feedback be conditioned as proposed feedback I have I argue to the may and by Le-

approach behavUnfortunately, approach and elucidated. that the fron-

modular that

tal lobes mediate avoidance behaviors lobes mediate approach behaviors. suggested be reciprocal, that approach so that a loss and avoidance of one

and the parietal These authors also behaviors may the lobe behaviors, behaviors, In support frontal lesions may release frontal lesions and of

of emotions, I do suspect emotions. Emotions may thalamic limbic circuits, most by emotional complex interpret. modular and the that

However, are induced

behaviors stimuli that

and experian isolated

behavior because frontal

the other behavior.83 lobes mediate avoidance would because parietal this cause inappropriate

Therefore, behavior, approach

could not has complex develop proposed Almost two or

The cerebral cortex of systems that analyze interpret experience meaning. of emotions can is be devalence, of

percepts,

the parietal lobes mediate approach lesions would induce avoidance. one can see patients with a variety of approach grasp reflexes, visual magnetic response area or cause

dimensional. scribed with arousal, valence

all primary three factors, activation. whether the

emotions including

postulate,

who demonstrate cluding manual rooting zation

behaviors, ingrasp reflexes, apraxia, inhibition. utiliUn-

and motor is based on

The determination stimulus is beneficial

and sucking responses, behaviors, and defective which when specific damaged,

(positive) or detrimental being. Whereas the right connections emotions its with

(negative) to a persons wellfrontal lobe and its subcortical in the mediation left frontal lobe important in of and the

fortunately, frontal lobes,

areas within the approach behav-

appear to be important negative valence, the connections may be

subcortical

446

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mediation ing on

the

of emotions with positive nature of the stimulus,

valence. Dependsome positive and

some negative emotions (such as joy and fear) are associated with high arousal, and others (such as satisfaction and sadness) are associated with low arousal. Whereas the right parietal lobe appears to be important in mediappears to and negaare associating arousal response, the left hemisphere inhibit the arousal response. Some positive tive emotions (such as anger, fear, and joy) ated with motor activation, are not. The right frontal in motor activation. The with emotions may Approach be behaviors.
References 1.Heilman mediating Zeidel 2. Darwin KM: Emotion emotional and the experience, brain: in a distributed modular Neuropsychology, Press, 1994, pp 139-158 in Man and Animals. York, WV: 1969; Plenum, 1977 elements vol vol effects 1: The 2: The in facial Positive Negative behav1974; with network edited by London,

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have discussed have these neocortical the limbic system, Therefore, system. the

basal

ganglia, anatomic

that mediate valence, are richly interconnected Emotional experience of neural activation of this

arousal, and activation and form a modular depends on the patmodular network.

and others (such as sadness) lobe appears to be important motor activation associated either approach may or avoidance by the be mediated

behaviors

This work Department

was supported of Veterans

by the Medical Affairs.

Research

Service

of the

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