Proc. Nadl. Acad. Sci. USAVol. 91, pp. 11771-11776, December 1994

Review

The amygdala complex: Multiple roles in associative learningand attentionMichela Gallagher* and Peter C. HollandtDepartnent of Psychology, University of North Carolina, Chapel Hill, NC 27599; and tDepartment of Psychology, Duke University, Durham, NC 27706

ABSTRACT Although certain neuro-physiological functions of the amygdalacomplex in learning seem well established,the purpose of this review is to proposethat an additional conceptualization ofamygdala function is now needed. Theresearch we review provides evidence thata subsystem within the amygdala providesa coordinated regulation of attentionalprocesses. An important aspect of thisadditional neuropsychology of the amyg-dala is that it may aid in understanding theimportance of connections between theamygdala and other neural systems ininformation processing.

Kluver and Bucy (1) observed that mon-keys became remarkably tame after sur-gical removal of the temporal lobes, aphenomenon noted as early as 1888 byBrown and Schaefer (2). Subsequent re-search extended these observations toindicate that the amygdala complex playsan important role in emotional behavior.This conceptualization ofamygdala func-tion led to subsequent research on therole of the amygdala in emotional learn-ing (3).

The Role of the Amygdala CentralNucleus (CN) in Associative Laing

Dating from Kluver and Bucy's (1) clas-sic studies, many lines of research havecome to support the tenet that neuralprocessing within the amygdala complexis important for assigning emotional sig-nificance or value to events through as-sociative learning. For example, in ani-mals with amygdala damage, a cue thatsignals an impending aversive event(such as footshock) fails to elicit fearfulbehavior (4, 5). Learned associations be-tween cues and positive experiences arealso deficient in animals with amygdaladamage. In one commonly employedtask, rats normally learn to seek, or re-main in, an environment associated withreward, a phenomenon referred to asconditioned place preference. Rats withamygdala damage fail to show this formof associative learning (6). In the pastdecade, the study of acquired emotionalresponses has yielded much informationabout the neural circuits in the amygdalathat are involved in associative learning.

In addition to a well-established role inemotional learning, specific circuitrywithin the amygdala complex contributesto the regulation of attention. The re-search that led to this view of amygdalafunction began with an exploration of therole of the central nucleus (CN) of theamygdala in Pavlovian appetitive condi-tioning (7). Removal of CN neurons wasproduced by microinjection of the neu-rotoxin ibotenic acid, which spared fibersof passage and neurons in adjacentamygdala nuclei. In our behavioral stud-ies, rats received training in which pre-sentations of an originally neutral cue,such as a tone or light, were followed bydelivery offood at a recessed cup locatedin a standard animal test chamber. Ratswith CN lesions learned as readily asintact rats; in the presence ofthe cue, ratsapproached the recessed cup in anticipa-tion offood delivery. Our result suggeststhat this nucleus of the amygdala is notnecessary for learning the motivationalsignificance of a cue signaling food re-ward. If this is the case, then an impor-tant functional distinction between sub-systems within the amygdala complexmight be possible. In contrast to ourresults, McDonald and White (6) foundthat damage to the lateral nucleus of theamygdala abolished the acquisition oflearned cue preferences in rats. Thebasolateral nucleus of the amygdala hasalso been implicated in the acquisition ofcue value (8). To establish whether thisaspect of associative learning is trulyspared in our animals, we conducted fur-ther experiments to examine the natureof the learning acquired by cues duringappetitive Pavlovian conditioning in ratswith selective CN damage.

Perhaps the most frequently cited mea-sure of a cue's changed motivationalvalue, as a consequence of its pairingwith a biologically meaningful stimulus,such as food, is its ability to reinforcesubsequent learning-for example, thephenomenon known as second-orderconditioning. We tested a cue's ability tosupport Pavlovian second-order condi-tioning in rats with CN damage. Asshown in Fig. 1, second-order condition-ing was as robust in rats with CN lesionsas it was in normal control rats (seelegend to Fig. 1 for description of task).

Thus, CN damage did not interfere witha cue's ability to acquire reinforcingpower when paired with food.We also tested whether a cue's acqui-

sition of motivational properties remainsintact in rats with CN damage by using aprocedure called "conditioned potentia-tion of feeding." In this procedure, satedrats are induced to eat by presenting apreviously trained cue for food (9). Totest for this effect, rats were placed backon ad libitum feeding after standard ap-petitive training and exposed repeatedlyto the test chamber with food available toeliminate all tendency to consume food inthat environment. Two test sessionswere then conducted, during which 20food pellets were made available. In onesession the formerly trained cue was pre-sented; in the other no cue presentationsoccurred during the test. Our experimentshowed that feeding was potentiated sub-stantially by the cue in normal rats;whereas an average of 0.2 pellet wasconsumed in the unsignaled test, on av-erage, 15.2 pellets were consumed in thecue-signaled condition. The rats with CNdamage showed a comparable effect ofcue presentations; lesioned rats ate 3.8pellets in the unsignaled condition and16.9 pellets in the signaled condition (10).These results provide strong support

for the conclusion that the motivationalvalue associated with cues during appet-itive learning is acquired normally by ratswith amygdala CN damage. Taken to-gether with research conducted in otherlaboratories (e.g., refs. 6 and 8), it ap-pears that a separate subsystem withinthe amygdala is necessary for this func-tion. Despite the normal appearance ofrats with CN damage on the tests de-scribed above, the lesions were highlyeffective in producing other behavioralimpairments. One that can be observedduring simple appetitive conditioning willbe described here; others will be intro-duced in a later section of the paper.We observed that neurotoxic damage

to the amygdalaCN produces a profounddeficit in the acquisition of learned ori-enting behavior to either visual or audi-tory cues (7). Fig. 2 illustrates food-

Abbreviations: CN, central nucleus of theamygdala; US, unconditioned stimulus; CS,conditioned stimulus.

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FIG. 1. Second-order Pavlovian condition-ing. Rats were initially trained to approach afood cup in response to a light paired with food(first-order conditioning, data not shown).Then rats received training sessions in whicha tone was either paired with the light (pairedgroups) or presented alone (control groups).The results for the second-order conditioningsessions in the graph show learning to the tonewhen it was paired with light but not when itwas presented alone. This learning was equiv-alent in CN-lesioned rats (CN-paired) andcontrol rats (CTL-paired).

reinforced orienting to visual cues, whichconsists of rearing on the hind legs andorientation toward the light source. Al-though the topography of learned orient-ing resembles the spontaneous orientingof rats to novel stimuli, CN damage didnot alter spontaneous orienting. Habitu-ation of spontaneous orienting to re-peated nonreinforced presentations ofthose stimuli, either within single ses-sions or across sessions over days, wasalso entirely normal (7). These findingsresemble those from earlier studies ex-amining an autonomic component of theorienting response and conditioning ofthat response in rabbits. Damage to the

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CN or neuropharmacological treatmentswithin the CN were found to prevent theacquisition of conditioned heart-rate re-sponses while entirely sparing the occur-rence of heart-rate orienting responses tonovel stimuli (11-13). Thus, it appearsthat CN is critically involved only in thedevelopment of learned orienting re-sponses. Because the Pavlovian task weuse to study rats permits this learning tobe monitored in the same experiment inwhich learning to approach the food-cupalso occurs, we confirmed that deficits inthe acquisition of orienting were evidentin the previously summarized studies inwhich CN damage did not affect learningthe motivational/reinforcing value ofcues (see Fig. 2). This impairment oforienting during learning, without anychange in the cue's ability to acquirereinforcing properties, led us to considerother contributions of the CN to associa-tive processes. A description of the sub-sequent behavioral research we con-ducted will follow a section in which weconsider the anatomical connectivity ofthe CN as a framework for understandingthe function of this subsystem of theamygdala.

A Neuroanatomical Frameworkfor CN Function

Among the nuclei of the amygdala com-plex, the CN is distinguished by its pro-jections to the lower brainstem (14-16).Much research has shown that manybrainstem targets of CN exert controlover autonomic and behavioral re-sponses used in the expression of asso-ciative learning. Conditioned-freezing,heart-rate, potentiation of startle and

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FIG. 2. (Lower) The cartoon illustrates the occurrence of orienting behavior (ConditionedOR) early in the CS interval and the occurrence of the learned food cup response (Food CupCR) toward the end of the CS presentation. (Upper) Graphs show the performance of intact rats(o) and rats with CN lesions (e) on the learned orienting response (Left) and food cup response(Right) when a visual CS was paired with food (eight trials per session). Damage to CN onlyimpaired learning of orienting to the CS.

eyeblink reflexes all appear to depend onoutput from brainstem systems that areinnervated by CN (17-20). For example,the acoustic startle-reflex circuit is orga-nized at the level of the brainstem andincludes the nucleus pontis caudalis,which receives a substantial projectionfrom CN that is critical for potentiation ofthe reflex based on learning (21).

In addition to the somatomotor andautonomic effector targets of CN in thebrainstem, a collection of ascending sys-tems receive input from the CN, includ-ing monoamine systems (norepinephrine,serotonin, and dopamine), the pontomes-encephalo-tegmental areas where brain-stem cholinergic neurons are located,and the basal forebrain system that in-nervates the cortex (15, 21-25). Collec-tively, these ascending systems havebeen assigned roles in arousal, vigilance,and attentional functions. A subset ofthese projections, which will be dis-cussed further, is shown in Fig. 3. Wethink that the CN uses these pathways toexert control over forebrain processingduring learning. For example, severalpathways provide potential routes for thecontrol of learned orienting. The CN hasan indirect influence on the striatumthrough its input to midbrain dopamineneurons in the substantia nigra (shown inFig. 3). Considerable research indicatesthat dorsolateral striatum plays an impor-tant role in the initiation of responsesguided by sensory events, including theregulation of orienting behavior to cues inmany different modalities (e.g., refs. 26-29). It is notable that a prominent com-ponent of the projection from CN inner-vates a dorsal tier ofdopamine neurons inthe lateral substantia nigra pars compacta(30), neurons that project primarily todorsolateral striatum (31). In addition tothis circuitry, input from CN to pon-tomesencephalo-tegmental regions in thebrainstem (LDT/PPT shown in Fig. 3)may also be involved in orienting behav-ior. The cholinergic neurons in these re-gions innervate subcortical structuresthat influence cortical processing (via an-terior, reticular, mediodorsal, centralmedial, and posterior nuclear regions ofthalamus) and other areas that controlsensorimotor function (e.g., superior col-liculus, extrapyramidal structures, etc.)(32, 33). The superior colliculus, in par-ticular, plays an important role in visualorienting (e.g., ref. 34).Recent neuroanatomical studies have

shown that CN output also targets sys-tems located in the basal forebrain, whichin turn regulate cortical processing. Thisanatomy is interesting in light of recentstudies indicating that the basal forebrainis involved in the allocation of attentionalresources, even when overt orienting be-havior is absent (35-37). A component ofthis basal forebrain system uses acetyl-choline as a neurotransmitter. In the

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FIG. 3. Schematic of the rat brain in a parasaggital view. The CN is in the temporal lobe andprojects to several systems that innervate the forebrain. The projection to the substantia nigra(SN) provides access to dopamine neurons that innervate the dorsolateral striatum (ST).Projections from CN to the lateral dorsal tegmental nucleus (LDT) and pedunculopontinenucleus (PPT) provide a route for regulating pathways to midline thalamic nuclei (TH) andsuperior colliculus (SC), as well as other extrapyramidal structures (data not shown). A systemofmagnocellular neurons in the basal forebrain (BE), which projects to the cortex (CTX), is alsounder the influence of CN efferents.

monkey these cholinergic neurons areconcentrated in the nucleus basalis ofMeynert, and efferents from CN ontocholinergic neurons in the nucleus basalisof Meynert have been identified in theprimate brain (38). A homologous systemof cholinergic neurons-scatteredthroughout the sublenticular substantiainnominata and ventral globus pallidus,as well as the nucleus basalis of Mey-nert-also receive input from the CN inthe rat (ref. 23 and illustrated in Fig. 3).

The Regulation of Attention by the CN

Progress in research on the neurobiologyof attention in the past decade has pro-vided a number of key insights. (i) At-tention is mediated not by a single systembut by a set of systems, each of whichspecializes in components of attentionthat can be specified in cognitive terms.For example, Posner and colleagues (39,40) have defined a number of specializedfunctions, such as maintaining vigilanceor an alert state, orienting to sensoryevents, and detecting signals for focalprocessing, which rely on distinct neuralcircuitry. In addition, different opera-tions within these networks are respon-sible for the dynamic control of atten-tion-i.e., disengaging attention, shiftingattention, and engaging a selective focusof attention. (ii) Considerable evidencenow indicates that these attention sys-tems are anatomically separate from in-formation-processing systems that dealwith specific inputs from the externalenvironment.The neuroanatomical connectivity be-

tween the amygdala CN and other brainsystems noted in the preceding sectionprovides potential routes for regulatingcomponent processes of attention, in-

cluding alerting/vigilance (through thelateral dorsal tegmental nucleus/tha-lamic/cortical system and ascending nor-adrenergic pathway), the selection of ori-enting responses to cues (via pedunculo-pontine nucleus/superior colliculus anddopamine/dorsostriatal systems), andshifts in the focus of attention (throughthe basal forebrain projection to cortex).The following section will deal with stud-ies of CN function in attention. The re-sults of these studies suggest that CNoutput may be particularly critical forengaging or incrementing attention tocues when expectations established byassociative learning are modified.The original impetus for our studies on

the role of the CN in attention duringassociative learning stemmed from theobservation that CN-lesioned rats failedto acquire orienting responses. Researchbased on modern theories of learning hasindicated that conditioning episodes pro-duce important changes in the processingof cues, as well as in the formation ofassociations between the conditionedstimulus (CS) and unconditioned stimu-lus (US) (e.g., refs. 41-44). Such changesin attention may be characterized as ei-ther incremental or decremental. For ex-ample, Pearce and Hall (42) suggestedthat losses of attentional processing canoccur when a cue provides no new infor-

mation about subsequent events, but in-creases in attention occur when impor-tant events happen unpredictably orwhen expectations about the occurrenceof events are violated. By this view, thefailure to learn orienting behavior mightreflect a failure to increase attention to acue when its relation to another signifi-cant event (the US) is initially detected.In subsequent studies of rats with CNdamage, we found a general absence ofthe tendency to increase attention-forexample, when contingencies between acue and other events were altered. At thesame time, no effect of CN damage wasfound in a variety of situations in whichdecremental changes in attention to cuesare observed-for example, when a cueconsistently signals the absence of food.An associative learning task initially

developed by Wilson et al. (45) was usedto investigate the role of the CN in mod-ifying attention to a cue (46). As shown inTable 1, two training conditions are used.In one condition, a "consistent" predic-tive relationship between a light followedby a tone occurs throughout phases 1 and2 of training, and these trials are them-selves reinforced with the food US onhalf the trials. In the "inconsistent"training condition, trials identical tothose in the consistent procedure occurin phase 1, so that rats come to expectthat the light is invariably followed by thetone, but a manipulation of the reliablerelationship between these cues occurs inphase 2; the tone is unexpectedly omittedon nonreinforced trials. In phase 3 allo-cation of attention to the light is assessedby monitoring how readily rats learn toapproach the food cup during the lightwhen it is paired directly with food.Wilson et al. (45) originally showed

that the inconsistent training procedureincreases attention to the light in phase 2,as evidenced by facilitated acquisition oflearning in the final test phase. Fig. 4 Leftshows this result for groups of intact ratsin our study (46). Fig. 4 Right shows theeffect of neurotoxic CN lesions. A com-parison ofperformance across Fig. 4 Leftand Right indicates comparable learningfor CN-lesioned and control rats when aconsistent relationship between the cuesis maintained. However, instead of im-proved learning, the inconsistent trainingcondition makes learning worse in ratswith CN damage. It is clear that an un-expected shift in the light's predictive

Table 1. Procedures used to increment attention by altering the predictable relationbetween two cues

Phase 1 Phase 2 (experimental Phase 3 (testTraining (consistent light-tone change in light-tone of learning tocondition relationship) relationship) light)

Consistent L - T- food; L -+T L - T- food; L-- T L-foodInconsistent L - T- food; L - T L - T-- food; L L - food

Half of the trials in phases 1 and 2 are reinforced with food; the other half are nonreinforcedtrials. In phase 3 the trials are always reinforced with food. L, light; T, tone.

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FIG. 4. Augmentation of attention by manipulating the predictive relation between twocues. Training procedures are described in Table 1. The graphs show the results from the finalphase in which simple appetitive learning to the light was assessed. (Left) Data for intact groups(Control). (Right) Data for groups with CN lesions. o, Consistent prior experience; *, priorexperience in which the relation between cues was shifted to an unpredictable condition in phase2 (inconsistent prior experience). Note that rats normally learn better when they haveexperienced a change in what they expected (inconsistent vs. consistent groups). This is not thecase for rats with CN damage. [Reproduced with permission from ref. 46 (copyright AmericanPsychological Association).]

validity in phase 2 did not increase atten-tion to the light in rats with CN damage.In the absence of increased attention tothis cue, there are several reasons whyrats in the inconsistent procedure wouldshow less conditioning-e.g., less pro-tection from extinction, habituation, orlatent inhibition, all of which remain un-affected by CN lesions (refs. 7, 46, and47; see ref. 47 for a full discussion).Another task designed to demonstrate

that altering the predictive relationshipbetween cues can increase attentionalprocessing yielded additional evidencethat rats with CN damage are impaired inthis aspect of attention. The "blocking"paradigm has been commonly used forthe examination of attention in associa-tive learning. Here, learning to a cue,such as a tone, that is presented at thesame time as another cue, such as a light,is prevented or greatly diminished byprior conditioning to the light alone. At-tention-based theories account for thisblocking of learning in terms ofhow priorlearning to one cue may change attentionallocated to a cue that is added later intraining. For example, because the sig-nificant event (the food US) is alreadywell predicted when the compound light/tone is introduced, any attention paid tothe added cue will rapidly diminish; itprovides no new information. Learningthe relationship between the added cueand the occurrence of the food US isblocked, therefore, by decrements in at-tention. Support for this account hascome from the effects on learning pro-duced by variations in the usual blockingprocedure. One such variant is to changethe predicted relationship between theoriginal cue and the food US when com-pound conditioning is introduced. Thischange can be made by either increasingor decreasing the magnitude or value ofthe US. Both procedures augment con-

ditioning to the newly introduced cue, a

phenomenon referred to as "unblock-ing." In particular, the observation thatgreater learning occurs when the value ofthe US is decreased in an unblockingexperiment has provided evidence thatincreased attention to a cue occurs whena previously established relationship be-tween events is altered.

Unlike normal rats, we observed thatrats with CN damage fail to show greaterlearning to a cue when unblocking isproduced by decreasing the value of theUS (47). Two sets of rats (one with CNlesions and a control group) were trainedin each of the conditions shown in Table2. When no training occurred beforetraining with the compound in phase 2(control condition), robust learning oc-curred to the target cue; =60% responseswere observed in both the lesioned andcontrol rats during the final test. By com-parison, learning was blocked when thesame US (either high or low value) wasused throughout training in phase 1 and 2(blocking conditions); the test for condi-tioning to the target cue revealed <25%responses, irrespective of lesion condi-tion (shown in Fig. 5). Relative to thesmall amount of learning for thesegroups, a decrease in US value intro-duced in the phase 2 unblocking proce-dure improved learning to the added cue,but only in the control rats (also shown inFig. 5). Thus, the increase in attentionusually produced by changing the pre-

dicted relationship between events wasabsent in rats with CN damage.The absence of unblocking after CN

damage is significant because other re-sults obtained in the experiment showedthat the shift in value of the US wasdetected by CN-lesioned rats. This resultwas observed in the occurrence of learn-ing to the original cue (the light) acrossthe first two training phases. In the un-blocking procedure, both control andCN-lesioned groups exhibited compara-ble learning to that cue in phase 1 when ahigh-value US was used (79.2% and83.3% responses for control and CN-lesioned groups, respectively), andlearned responding decreased compara-bly in phase 2 when the US was de-creased (68.8% and 65.3% responses forcontrol and CN-lesioned rats, respective-ly). Thus both lesioned and control ratswere equally sensitive to changes in theUS across training, but only the controlrats showed unblocking. These resultshave been replicated in two separate ex-periments (47), indicating that alteringthe cue-reinforcement relation, while de-tected by rats with CN damage, does notproduce an increase in attentional pro-cessing.

In contrast to the effects of CN lesionsin situations where normal animals in-crease attentional processing of cues,such damage does not affect decrementalattentional processes. This result is evi-dent in habituation of spontaneous ori-enting to neutral cues, in blocking itself,and in the effects ofrepeated exposure tocues on subsequent conditioning (e.g.,latent inhibition), all of whjch proceednormally in rats with neurotoxic lesionsofthe CN (7, 44). Interestingly, effects onthose functions spared byCN damage areoften impaired by lesions ofanother brainsystem studied in associative learning,the hippocampal formation including theseptohippocampal pathway (48-52). Thisresult raises the possibility that incre-mental and decremental regulation of at-tention is served by separate neural sys-tems. We turn now to a preliminary ex-ploration of how the regulation ofattention by CN may be mediatedthrough its connectivity with systemsidentified in the previous section of thisreview.The concept that the pathway from CN

to the basal forebrain (shown in Fig. 3)provides a substrate for the regulation ofattention is consistent with other evi-dence for a role of the basal forebrain inattentional processes cited earlier (35-

Table 2. Unblocking experimentGroup Training procedure Phase 1 Phase 2 Test

Control High US, phase 2 only Light/tone -. USH ToneBlocking High US, phases 1 and 2 Light -* USH Light/tone -- USH ToneBlocking Low US, phases 1 and 2 Light -) USL Light/tone -) USL ToneUnblocking High US shifted to low US Light -s USH Light/tone -+ USL Tone

USH, high-value US; USL, low-value US; -*, cued paired with US.

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Hgh to Low US

UNBLOCKING

FIG. 5. Unblocking produced by decreasing the value of the US when training with the

compound cue was introduced. Training conditions conform to the procedures shown in Table

2. The intact rats (CTL group) in the unblocking condition exhibit more learning than rats in

the blocking conditions. This effect is not seen in rats with CN lesions. [Reproduced with

permission from ref. 47 (copyright American Psychological Association)].

37). In addition, amygdala CN regulation to the dorsolateral striatum or its dopa-of the projection from basal forebrain to mine innervation fail to orient spontane-cortex has been recently studied. Whalen ously to cues (27-29). Although CN dam-et al. (53) found that classically condi- age, unlike striatal damage, does not af-tioned neocortical activation of the elec- fect spontaneous orienting to novel cues,troencephalogram (which is sensitive to CN output might engage this system for

drugs that block cholinergic function) is learned orienting behavior.

tightly coupled to conditioned neural ac-

tivity in the basal forebrain. The possi- Conclusionbility that this associative regulation of

basal forebrain activity is controlled by The suggestion that the amygdala com-

the CN is supported by evidence that CN plex is involved in the regulation of at-

stimulation elicits the cortical activation tention is not entirely novel (see ref. 58).mediated by cholinergic input, and neu- Until recently this concept has rested on

rotoxic CN lesions abolish learned acti- only a few fragmentary observations.

vation of the cortical electroencephalo- Earlier research described aimless visual

gram (54, 55). tracking in monkeys with amygdala dam-In a recent experiment, we examined age (59), and an alerting/orienting reac-

the effect of basal forebrain lesions, in- tion evoked by electrical stimulation atduced by microinfusion of the neurotoxin sites in the vicinity of amygdala CN was

a-amino-3-hydroxy-5-methylisoxalzole- originally described in cats (60). More4-propionic acid (AMPA) into this region recently, the notion that amygdala CN(56). These rats along with appropriate regulates arousal during learning hascontrol groups were tested in the task been proposed (61). The neuropsycho-devised by Wilson et al. (45). We found logical perspective of CN offered herethat this damage reproduced the effect of may help to broaden our view ofCN lesions; rats with basal forebrain amygdala function, within a more clearly

damage failed to increase attention when defined neuroanatomical and behavioral

the relationship between events was un- framework for the study of attention. Inexpectedly modified. More recently we additiontotheamygdala'slong-acknowl-

have removed only the neuronsin the edged role in associative learning of emo-

basal forebrain that provide cholinergic tional responses, it is suggested that theinnervation of the cortex using a newly CN regulates the processing of cuesdeveloped immunotoxin, 192 IgG-sa- when predictive relationships betweenporin (57). These selective lesions also events are first noticed or altered. Inreproduced the deficit in attentional reg- particular, the allocation of attention nor-ulation seen after CN damage (A. Chiba, mally engaged when an expectationM.G., and P.C.H., unpublished work). about the occurrence of events is violatedOne result found with CN damage, how- does not happen after damage to this

ever, was not evident in rats with basal system. This role of the CN has potentialforebrain lesions-namely, there was no implications for a number of clinical sit-significant effect of this damage on the uations involving attentional disordersoccurrence oflearned orienting behavior, where the biological basis is poorly de-Thus, increased attentional processing of fined, as well as for the neuropsycholog-target cues may involve a CN-basal fore- ical study of patients with knownbrain pathway, but mediation of learned amygdala damage.orienting must use different circuitry. Assuggested earlier, that orienting behavior 1. Kluver, H. & Bucy, P. C. (1939) Arch.might depend on the CN/nigral/dorso- Neurol. Psychiatry 42, 979-1000.lateral striatal system. Rats with damage 2. Brown, S. & Schaefer, E. A. (1888) Phi-

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