contingent versus incidental context processing during ...tai/readings/unsupervised... · dentate...

Contingent Versus Incidental Context ProcessingDuring Conditioning: Dissociation After ExcitotoxicHippocampal Plus Dentate Gyrus Lesions

M. Good,* L. de Hoz, and R.G.M. Morris

Centre for Neuroscience, University of EdinburghMedical School, Edinburgh, Scotland

ABSTRACT: This experiment explored whether excitotoxic hippocam-pus plus dentate gyrus (HPC/DG) lesions in rats would dissociate thedifferential processing of contextual cues during the performance oflearned associations when (1) their processing during training is incidentalto successful learning or (2) the solution of a discrimination problem iscontingent on their processing. A series of training stages were conducted,beginning with appetitive conditioning to two stimuli (X and Y), each ofwhich was trained in one of two different contexts (operant chambers Aand B) (i.e., AX1, BY1). Conditioning was indexed as appetitive respond-ing. The animals were then trained on a biconditional contextual discrimi-nation with these same stimuli (AX1, AY2; BY1, BX2). The next stageinvolved conditioning trials to two new stimuli (W and Z), one in eachcontext, while the animals were actively discriminating contexts A and Bby continuing to perform the original biconditional discrimination (AX1,AY2, AW1; BY1, BX2, BZ1). Finally, they were trained on a secondbiconditional discrimination involving these new stimuli (AX1, AY2,AW1, AZ2; BY1, BX2, BZ1, BW2). The incidental use of context cueswas examined by looking at the rate of conditioned responding to cues X,Y, W, and Z in their original training contexts or a different context;HPC/DG lesioned rats differed from controls in being unaffected by achange of context. The contingent use of context cues was examined bylooking at performance of each of the two biconditional tasks; HPC/DGlesioned rats reached levels of conditional performance indistinguishablefrom those of controls. These findings point to two distinct ways in whichcontextual information is processed in the brain, revealing a dissociationbetween incidental and contingent processing of contextual cues afterHPC/DG lesions. Hippocampus 1998;8:147–159. r 1998 Wiley-Liss, Inc.

KEY WORDS: hippocampus; context; conditional discrimination; ibo-tenic acid; incidental and contingent processing

INTRODUCTION

All learning occurs in a spatiotemporal context. For some learning tasks,when and where learning takes place is incidental to what is being learned.In such tasks, a failure to process context cues effectively may not bereflected in any immediate behavioural change, but incidental processing ofcontext could nonetheless affect the way knowledge is encoded or retrievedand thus how it is expressed in a place different from that of the originaltraining (Spear, 1971, 1973; Spear et al., 1980). In other tasks, the solutionis contingent upon the processing of contextual cues. In certain types of

conditional discrimination task, for example, a stimulusmay be arranged to signal reward in one context andnonreward in another (e.g., Preston et al., 1986).Similarly, in spatial learning, effective navigation iscontingent upon the processing of at least some contextcues. In both cases, the failure to process context cueseffectively would result in a failure of learning or at leastits retardation. This distinction between incidental andcontingent processing of context cues may reflect a morefundamental distinction between a role for context cuesin declarative or higher-order memory processes, such asthe retrieval of information about events that hasoccurred within the context (possible after incidentalprocessing of context), and a role in associative learningitself (reflecting contingent processing).

Traditional learning theory accounts of the role ofcontext in learning can be divided into associativeaccounts and higher-order function accounts. Associa-tive accounts (Wagner, 1976, 1978, 1981) emphasizethe role of direct associations between contextual cuesand events that occur in their presence. Higher-orderfunction accounts generally acknowledge the associativeproperties of context cues and propose that context cuesparticipate in the retrieval of information about therelationships between cues that have occurred in theirpresence (e.g., Spear, 1973; Swartzentruber and Bouton,1986; Hall and Honey, 1989). The aim of the experi-ments described in the present study was to explorewhether a dissociation between these different ways inwhich context cues may be processed could be realizedusing excitotoxic hippocampal plus dentate gyrus (HPC/DG) lesions. Several studies have implicated the hippo-campus in forming a representation of the context (e.g.,Sutherland and Rudy, 1989; Kim and Fanselow, 1992).If the integrity of HPC/DG is essential, at least tempo-rarily, for forming a context representation, there is noreason to expect a dissociation. Conversely, if some typesof context processing can occur when HPC/DG isdamaged and other types depend on hippocampalfunction (Honey and Good, 1993; Phillips and LeDoux,1994), dissociations between qualitatively distinct typesof context processing might be identified.

Grant sponsor: United Kingdom Medical Research Council.*Correspondence to: M. Good, School of Psychology, Cardiff University ofWales, P.O. Box 901, Cardiff, CF1 3YG, UK.Accepted for publication 28 January 1998

HIPPOCAMPUS 8:147–159 (1998)

r 1998 WILEY-LISS, INC.

The different outcome of two closely related experiments led usto think about this distinction. Good and Honey (1991) foundthat electrolytic lesions of the dorsal HPC/DG impaired theacquisition of a complex biconditional discrimination in which, asin Preston et al. (1986), the reward significance of each of twostimuli was switched between the two contexts in which trainingtook place. Whishaw and Tomie (1991), in contrast, found thatrats with excitotoxic lesions of HPC/DG were unimpaired in theacquisition of a logically similar biconditional discrimination. Inseeking to reconcile the different outcomes of these two studies,the type of the lesion made (electrolytic vs. excitotoxic) may becritical. The electrolytic lesion procedure disrupts fibres ofpassage, vasculature, and cell bodies, and thus the impairment ofconditional learning reported by Good and Honey (1991) mayreflect extrahippocampal damage. In a pilot experiment, weexamined the effects of ibotenic acid lesions of HPC/DG on theacquisition of this same type of biconditional contextual discrimi-nation. The results indicated that neurotoxic HPC/DG lesionedanimals acquired the biconditional contextual discriminationnormally. A similar observation was also made independently byMcDonald et al. (1997). This finding suggests that certain types ofcontext processing are unaffected by HPC/DG lesions. However,we also found that, after the initial training of each of two stimulipresented in their rewarded context only, conditioned respondingto these stimuli upon their first presentation in the other contextwas unchanged in HPC/DG lesioned animals, whereas controlsshowed a much reduced rate of responding. This indication of thecontext specificity of responding in control animals may reflectincidental learning about context that occurs automatically (i.e.,without regard to schedule) but requires the integrity of hippocam-pus. To explore this more formally, various issues needed to beaddressed including the critical one of whether, at the time theyfail to display context specificity of conditioned responding,HPC/DG lesioned rats are actually discriminating one contextfrom the other.

The experimental design was based on the study by Preston etal. (1986). As shown in Table 1, the experiment consisted of sixstages. In the first stage, the rats received conditioning trials withtwo stimuli (X and Y) in two different contexts (A and B) suchthat X was always presented in A and Y was always presented in B(i.e., AX1, BY1). Responding took the form of approachestowards a place in the box where food was occasionally madeavailable. In the second and overlapping third stages, they weretrained for several days on a so-called biconditional contextualdiscrimination task in which the significance of X and of Ydepended on the context in which they were presented (AX1,AY2; BY1, BX2). The first day of training (stage 2) is formallyidentical to a test for context specificity used by Honey and Good(1993). Stage 4 involved continued training on the first bicondi-tional discrimination task but also rewarded presentations of twonew stimuli (W and Z), one in each context (i.e., AX1, AY2,AW1; BY1, BX2, BZ1). After these training sessions, stages 5and 6 were conducted. These consisted of training on a secondbiconditional contextual discrimination with all of the stimuli(AX1, AY2, AW1, AZ2; BY1, BX2, BZ1, BW2). Onceagain, the first day of training on the second biconditional

discrimination (stage 5) served as a context specificity test forconditioned responding to stimuli W and Z. However, in contrastto stage 2, this context specificity test was conducted underconditions in which the animals could be shown to be activelydiscriminating between the two contexts during the same session(as indexed by appropriate responding to stimuli X and Y). At theend of the experiment and prior to death and histology, all ratswere trained in a watermaze to find a hidden escape platformlocated at a single fixed location (reference memory). This simplespatial learning task also makes use of contextual cues in both anincidental and a contingent way, but their processing is for thepurposes of navigation. It also served as a simple behavioural assayof the effectiveness of the neurotoxic lesions.

TABLE 1. _____________________________________________Summary of the Six Stages of the Main Experimentand the Two Subsidiary Experiments*

Main experiment Subsidiary experiments

SurgeryStage 1: Simple conditioning of

S1AX1, BY1 (S1)

Stages 2 and 3: Context speci-ficity test and bicondi-tional acquisition of S1

AX1 (S11), AY2 (S12)BY1 (S11), BX2 (S12)

Odour test: Switching of odorsbetween contexts A and B.

Stage 4: Simple conditioning ofS2 and continued perfor-mance of S1 biconditionaldiscrimination

AW1, BZ1 (s2)AX1 (S11), AY2 (S12)BY1 (S11), BX2 (S12)

Stages 5 and 6: Context speci-ficity test of S2, acquisitionof S2 biconditional dis-crimination, and con-tinued performance of S1biconditional task

AW1 (S21), AZ2 (S22)BZ1 (S21), BW2 (S22)AX1 (S11, AY2 (S12)BY1 (S11), BX2 (S12)

Watermaze aquisition: Placenavigation to a single loca-tion.

*The symbols within each stage refer to contexts (A, B), explicit stimuli(X, Y, W, Z), and reward significance (1, 2). S1 and S2 refer to first andsecond biconditional discriminations, respectively, averaged across therelevant stimuli.

148 GOOD ET AL.

GENERAL METHODS

Subjects

The subjects were 20 adult male hooded Lister rats (bred in theDepartment of Pharmacology, University of Edinburgh) with amean ad libitum weight of 375 g at the start of training. Onegroup of rats (n 5 10) received bilateral ibotenic acid lesions ofthe hippocampus. The second group (n 5 5) served as theunoperated control group. A third group of rats received shamoperations (n 5 5). The rats were housed individually withcontinuous access to water and were maintained at 80% of theirfree-feeding body weights throughout the experiment.

Surgery and Histology

The procedure used to remove cells in the hippocampus anddentate gyrus was similar to that described by Jarrard (1989). Theanimals were first anaesthetised with Avertin (tribromoethanol; 10ml/kg, i.p.) and placed in a Kopf stereotaxic frame. An incisionwas made in the scalp, and the bone overlying the neocortexsituated directly above the hippocampus was removed. Injectionsof ibotenic acid (concentration, 10 mg/ml; pH 7.4; TocrisNeuramin, Ltd., United Kingdom) were made with a 1-mlHamilton syringe mounted on the stereotaxic frame. Injections of0.05–1.0 ml were made over approximately 1 min at each of 26sites. Sham-operated animals received a treatment similar to thatof HPC/DG operated subjects except that passage of the needlewas limited to the cortex and no drug was infused.

At the end of behavioural testing, the HPC/DG rats were giveninjections of Euthatal (200 mg/kg sodium pentobarbital) andperfused with physiological saline and 10% formol saline. Thebrains were removed from the skull and placed in formol–salinesolution. The brains were then frozen and sectioned in thehorizontal plane (30-mm sections). A thionin stain was used todetermine cell loss. Reconstruction of the lesions were then madeon drawings derived from the stereotaxic atlas by Paxinos andWatson (1986).

Apparatus

Two pairs of identical operant chambers (Campden Instru-ments, Ltd.) were used. The chambers were constructed fromthree sheet-aluminium walls, a transparent plastic door as thefourth wall, with grid floors and aluminium ceilings. One of thewalls adjacent to the door contained a recessed food tray. Access tothis tray was guarded by a transparent hinged plastic flap. Inwardmovements of the flap actuated a microswitch, and each closing ofthis switch was recorded as a single response. The primary datameasure in this study was the rate of flap responding. The ceilingof each chamber contained a light and a loudspeaker. The offset ofthe light for 30 sec served as one conditioned stimulus (CS). A20-Hz train of clicks at an intensity of 82 dB(A) for 30 sec servedas a second CS. These stimuli were used in stages 1–3 of training(referred to as stimuli X and Y). Two speakers placed on the wallopposite the food tray were used to present a third CS, a 30-sec

white noise of identical intensity. The ceiling-mounted speakerwas used to present the fourth CS, a 30-sec 200-Hz tone. Stimuli3 and 4 (referred to as W and Z) were introduced at stage 4 oftraining. The boxes were housed in sound- and light-attenuatingshells.

The two pairs of boxes differed in the following respects. Theboxes were in rooms on different floors of the laboratory; one pairhad an odor produced by adding a small amount of eucalyptusoil to the saw-dust tray located below the grid floor, and the otherpair had an odour produced by isoamyl acetate. The pair withisoamyl acetate was also made visually distinctive by addingblack-and-white chequered wallpaper to the door and to the wallopposite this door.

The watermaze in which the animals were trained at the end ofthe main experiment was 2 m in diameter, had a hidden escapeplatform 11 cm in diameter, and was otherwise as described byDavis et al. (1992).

Procedure

The subjects received one session of training in each context oneach day. The stimuli that served as the conditioned stimulus andthe operant chambers (contexts) were counterbalanced. Trainingproceeded in a series of stages.

Stage 1: Pretraining and simple conditioning of S1

On the 2 days of pretraining (days 22 and 21), the rats weretrained to collect food pellets from the food tray. On day 22, theflap in front of the food tray was fixed in the raised position; onday 21, the flap was lowered to its normal resting position. Foodpellets were delivered on a variable time (VT) 60-sec schedule. Ondays 1–8 of conditioning, there were three presentations ofstimulus X that signalled the delivery of a single food pellet incontext A and three presentations of stimulus Y that preceded thedelivery of a food pellet in context B (see Table 1). The onset ofthe first stimulus presentation (trial) was 10 min after thebeginning of the session and the intertrial interval (ITI) was 10min.

Conditioning to stimuli X and Y was assessed by recording therate of flap responding during their presentation. To reduceindividual variability, conditioning was assessed with respect tothe rate during the ITI to yield a measure of ‘‘net’’ rate of response(rate during CS minus rate during ITI). The net rate of response isexpressed in units of responses per minute averaged across eachday or pair of days (blocks).

Stages 2 and 3: Context specificity testand biconditional acquisition of S1

On days 9–20, there were three reinforced presentations of X incontext A and of Y in context B; these are referred to as S11 trialsin Table 1 (where 1 refers to biconditional discrimination task 1).In addition, there were three nonreinforced presentations ofstimulus Y in context A and of stimulus X in context B (S12trials). The order in which trials were presented was random, with

___________________________________________________ CONTINGENT AND INCIDENTAL CONTEXT 149

the constraint that no more than two trials of the same type (S11or S12) were presented in succession. The ITI was 5 min.

Although procedurally identical to succeeding days, the firstday of this procedure (stage 2) was the first occasion that stimuli Xand Y were presented in a context different from that of stage 1training. Each stimulus was presented half the time in the originalcontext and half the time in the other context. The comparison ofthese two is the context specificity test that constitutes the firstopportunity to examine incidental use of context cues. Thesucceeding days (stage 3) provided a test of whether control andlesioned animals could learn to use context cues in a contingentway. Performance in stage 3 was averaged over 2-day blocks.

Odor test

On day 21, a transfer test was conducted to determine whataspects of the contextual cues were being used by the control andlesioned animals. The visual cues and the time of testing remainedthe same, whereas odor cues that comprised the two contexts Aand B were switched. If the discrimination was being solved onthe basis of the odor cues alone, we would expect a reversal of thediscrimination. Conversely, if the discrimination was being solvedby using some combination of exteroceptive cues (but notinteroceptive cues such as time of day), discrimination perfor-mance should merely deteriorate. For this test, odor trays wereremoved on the day before testing, recharged with either isoamylacetate or eucalyptus oil, and then left in the alternative contextovernight before testing the following day. The procedure wasotherwise identical to that used in stages 2 and 3.

Stage 4: Simple conditioning of S2 and continuedperformance of S1 biconditional discrimination

On days 22–29, the odor cues were returned to their originaltraining boxes. Two additional stimuli, W and Z, were nowintroduced, W signalling reward in context A and Z in context B.There were three trials of each stimulus in their respectivecontexts; the procedure is therefore analogous to that of stage 1with the original stimuli X and Y. However, although the animalswere trained on these new stimuli, they were also given another 8days of training on the S11, S12 biconditional discrimination(see Table 1). The CSs that served as either W or Z werecounterbalanced. The animals received exposure to the newstimulus and to X and Y, within the same session using acounterbalanced sequence, subject to the constraint that no morethan two trials of the same type were presented in succession. TheITI was 10 min.

Stages 5 and 6: Context specificity test of S2,acquisition of S2 biconditional discrimination,and continued performance of S1 biconditional task

On day 30, the first day of testing with W and Z, andcontinuing for 12 days (i.e., until day 41), the animals receivedreinforced trials of stimulus W in context A and of stimulus Z incontext B (referred to as S21 trials, where 2 refers to the secondbiconditional discrimination; Table 1) and nonreinforced trials of

Z in A and W in B (S22 trials). By analogy with stages 2 and 3,stage 5 (day 30) was the context specificity test for stimuli W andZ, and days 30–41 (stage 6) examined acquisition of thediscrimination.

It is important to appreciate that performance of the firstbiconditional discrimination (of stimuli X and Y) continuedthroughout stages 5 and 6. That is, testing and training of the S2discrimination (W and Z) were begun alongside the continueddaily presentations of the S1 discrimination (X and Y). There wasa total of 12 trials/day, three trials of each type (S11, S12, S21,and S22). The order in which trials were presented was random,subject to the constraint that no more than two trials of the sametype were presented in succession.

Watermaze training

Upon completion of training in the operant chambers, allsubjects received training in an open-field watermaze. On each of4 days (days 38–41), the animals received four training trials. Atthe start of each trial, the rat was placed into the pool at a randomposition around the perimeter and allowed to search for thesubmerged platform for a maximum of 120 sec. The position ofthe platform (northeast or southwest) was counterbalanced. If ananimal failed to locate the platform within 120 sec, it was guidedto it by the experimenter (this occurred rarely). The animals wereleft on the platform for 30 sec before the start of the next trial. Onday 45, after a total of only 16 training trials, a transfer test wasconducted in which the platform was removed from the pool andthe animals permitted to swim freely for 60 sec. Paths swimmingaround the pool were monitored by an automated videotrackingsystem, and the proportion of time spent swimming in the formertraining quadrant was measured.

RESULTS

Histology

For a subject to be included in the HPC/DG group, it had tofulfill specific criteria. First, it was necessary for at least 90% of theCA1–CA4 pyramidal cells and granule cells in the dentate gyrusto be removed. An animal was excluded if there was incompletecell loss in hippocampus or dentate gyrus. Second, it was essentialthat there was minimal damage to extrahippocampal structures,especially to cells in the subiculum and entorhinal cortex. Ananimal was excluded if it sustained combined damage to eitherstructure at any septotemporal level. Judgments regarding whethera given subject fulfilled these criteria were made without specificknowledge of the behavioural observations.

One HPC/DG lesioned animal failed to fulfill these criteria.The lesion was limited to the dorsal CA3 region of HPC/DG,with very little damage to any other region of the hippocampus atany other level. The remaining animals in the lesion group met thefirst criterion in showing near complete cell loss in the CA1–CA3regions. Four animals showed a small amount of sparing in

150 GOOD ET AL.

dentate gyrus but very few cells remained. With respect to thesecond criterion, no animals were excluded. The subiculumshowed some cell loss, either unilaterally or bilaterally, in nearly allcases. In four cases, damage to the subiculum was minor in theseptal and mid septotemporal aspects of the hippocampus, but thedamage extended as far as the presubiculum. Cell loss in theventral subiculum was variable; most lesioned animals showedsome cell loss in this region also but not enough to warrantexclusion.

A photomicrograph showing a representative hippocampallesion at a mid dorsal-ventral level is shown in Figure 1A. Figure1B shows the maximum and minimum extent of the lesions in theHPC/DG group on horizontal sections taken throughout thedorsoventral extent of the hippocampus.

Behavior

One unoperated control animal persistently failed to consumethe food reinforcement during the first stages of conditioning andwas subsequently dropped from the experiment. All other animalslearned to operate the magazine flap and responded appropriatelyto the scheduled stimuli. There were no systematic differences inthe performance of the sham-operated and unoperated controlanimals at any stage of the experiment and, therefore, to simplifystatistical analyses, the data from these two conditions werecollapsed to form a single control group. The final number ofsubjects in the control and HPC/DG lesioned groups was 9 pergroup.

At the end of the main experiment, the rats were trained in awatermaze for 16 trials. The results of the transfer test conductedafter the final day of training showed that control subjects haddeveloped a clear bias in the proportion of time spent in thetraining quadrant (36.8%, chance 5 25%), whereas HPC/DGlesioned animals showed substantially less bias (19.4%). Thisdifference was highly significant [t(16)5 4.47, P , 0.001]. Theslightly below-chance level of performance by the HPC/DGlesioned animals on the probe trial was caused by one animal whodisplayed a significant bias away from the training quadrant thatappeared to be related to a prominant extramaze cue in this area(door to the laboratory). Because the behavioral protocol used forthe watermaze is one that is exquisitely sensitive to HPC/DGlesions, these findings complement the histology in establishingthe adequacy of the lesions made.

In the data analysis of the main experiment that follows, datafrom successive stages are considered together with respect toperformance during acquisition of conditioned responding (stages1 and 4), to incidental processing of context cues (context test:stages 2 and 5), and to the contingent use of context cues(biconditional discriminations: stages 3 and 6). Although thisorganization is not chronological, it is the simplest way to presenta complex set of data in a manner that is conceptually straightfor-ward.

Conditioning of S11 and S21 cues (stages 1 and 4)

Acquisition of conditioned responding to X and Y. Inspectionof the scores revealed no systematic differences based on the

particular stimuli that were assigned as X and Y and no differencesdependent on the contexts that were designated as A and B.Accordingly, the data were pooled across stimulus type andcontext type for statistical analysis. Figure 2A shows the acquisi-tion rates for the HPC/DG and control subjects, in 2-day blocks,over the course of conditioning to S11 (the average of respondingto X and Y). It is clear that both the lesioned and control groupsacquired conditioned responding, but at no point was there anysizeable difference in the level of responding shown by the twogroups. An analysis of variance (ANOVA), with groups and blockas factors, confirmed these impressions. There was a significantmain effect of block [F(3,48) 5 35.90, P , 0.001], no significantmain effect of group [F(1,16) 5 1.91, P . 0.18], and nosignificant interaction between these factors [F(3,48) 5 2.15, P .0.10]. An analysis of the baseline rates of responding during theITI, with a mean of 2.94 responses per minute (rpm) for theHPC/DG group and 2.45 rpm for the control subjects, revealedno difference between groups [t(16) 5 1.43, P . 0.20].

Acquisition of conditioned responding to W and Z. Inspec-tion of Figure 2B shows that both the control and HPC/DGlesioned animals maintained discriminative responding betweenthe S11 and S1- of the first biconditional discrimination andacquired conditioned responding to the new stimuli (S21 trials).An ANOVA confirmed these observations and revealed a signifi-cant main effect of stimulus significance (S11, S12, S21).Pairwise comparisons (Newman-Keuls) revealed significant differ-ences between S11 and S12 response rates (P , 0.01) andbetween S21 and S12 response rates (P , 0.01) and nosignificant difference between S21 and S11 response rates (P .0.05). This pattern of performance did not differ between thelesioned and control groups [F(2,32) 5 1.51, P . 0.23]. There was asignificant interaction of block with stimulus type [F(6,96) 514.57, P , 0.001] that reflected a steady increase in responding toS21 over the four blocks of training (simple effect, P , 0.001).Although the rate of responding is numerically higher to S21 inthe control than in the lesioned group, this tendency was notsignificant [F(6,96) 5 1.30, P . 0.26]. The mean rates ofresponding during the ITI for HPC/DG and control animals were0.80 rpm and 0.85 rpm, respectively. These did not differ (t , 1).

Incidental processing of context cues(stages 2 and 5)

Figure 3 shows the results of the context specificity tests forconditioned responding to X and Y in each of the two contexts onday 9 (stage 2), to W and Z (stage 5, day 30), and to the S1 stimuliduring stage 5. For clarity, the data are subdivided into theHPC/DG (Fig. 3, left) and control (Fig. 3, right) groups.

Control animals displayed contextual specificity of conditionedresponding in both stages. That is, the level of responding washigher to a stimulus presented in its training (same) context thanwhen presented in a context different from that of originaltraining. HPC/DG lesioned animals did not show this effect ateither stage of training. These impressions were confirmed byANOVA with group, training, and context as factors. There was a


FIGURE 1. Lesion assessment. A: Photomicrograph of a randomly selected HPC/DG animaltaken at a mid dorsal/ventral level. B: Schematic representation of the maximum (stippled) andminimum (solid areas) extent of the lesions in the HPC/DG group throughout the dorsal-ventralextent of the hippocampus.

152 GOOD ET AL.

FIGURE 1. (Continued.)


significant main effect of context change [F(1,16) 5 12.53, P ,0.01] and a significant interaction of lesion group with contextchange [F(1,16) 5 6.01, P , 0.05]. Simple main effectsconfirmed a significant effect of context change in control animals[F(1,16) 5 17.95, P , 0.01], but no significant effect of contextchange in HPC/DG lesioned rats [F(1,16) , 1]. No significantmain effect of stage of training was found [i.e., context specificityafter simple conditioning (stage 1) vs. that after biconditionaltraining (stage 4): F , 1], and no significant interaction of groupwith stage of training (F , 1).

Figure 3 also shows the mean S11 and S12 rates of respondingon the first biconditional discrimination measured during thesecond context specificity test of stage 5. It is clear that bothHPC/DG lesioned and control animals are discriminating be-

tween the contexts equally effectively. This impression wasconfirmed by ANOVA that revealed no significant main effect ofgroup [F(1,16) 5 1.26], but a highly significant main effect ofstimulus significance with respect to context [i.e., S11 vs. S12:F(1,16) 5 28.06, P , 0.0005]. There was no interaction betweenlesion group and contextual significance (F , 1). Thus, theHPC/DG lesion rats are discriminating between the two contextsduring stage 5, but they are unable to use this information tomodulate their responding to stimuli W and Z.

Contingent use of contextual cues (stages 3 and 6)

Biconditional contextual discrimination 1 (stage 3). Figure4A shows the mean net rates of responding during S11 and S12trials for control and HPC/DG lesioned rats during acquisition ofthe conditional contextual discrimination. The S11 data repre-sent responding during X and Y trials when they were reinforced,and the S12 data represent the rates of responding during X andY when they were not reinforced. The lesioned and controlanimals acquired the conditional contextual discrimination rap-idly, reached the same asymptote of performance, and, other thanthe difference on the first day of training (reflecting incidentalcontext processing during stage 2), they learned at essentially thesame rate. An ANOVA revealed a significant effect of stimulussignificance [S11 vs. S12: F(1,16) 5 61.03, P , 0.0001] and asignificant interaction of block and trial type [F(5,80) 5 9.23,P , 0.001] that reflects the course of learning. There was nosignificant difference between groups (F , 1), although asignificant interaction of group with blocks did emerge [F(5,80) 52.74, P , 0.05]. This interaction reflected the overall higher levelof responding on the first block of training in the control animalsversus the lesioned subjects (simple main effects analysis, P ,0.05).

Intertrial interval responding. The mean rates of respondingduring the ITI for HPC/DG lesioned and control animals were2.51 rpm and 2.77 rpm, respectively. They did not differ (t , 1).

Odor test. The effects of changing the odor cues between boxeswas evaluated by comparing discriminative performance on thefinal day of conditional discrimination training (day 20) withperformance on the day of the odor test (day 21). The mean netrates of responding for HPC/DG and control subjects, respec-tively, were: 12.21 rpm (S11) versus 1.03 rpm (S12) and 9.73rpm (S11) versus 0.69 rpm (S12). On the day of switching theodor, discriminative performance deteriorated in both lesionedand control subjects. The rates of responding on the S11 andS12 trials for HPC/DG and control subjects was 6.54 versus 1.13rpm and 5.11 versus 1.03 rpm, respectively. An ANOVA con-firmed these impressions and showed a significant main effect ofday [normal vs. odor switch; F(1,16) 5 12.02, P , 0.01] but nosignificant main effect of group (F , 1) or interaction betweengroup and day (F , 1). There was a significant main effect ofstimulus significance [F(1,16) 5 30.80, P , 0.001]. There wasalso a significant interaction of day with stimulus significance[F(1,16) 5 19.95, P , 0.001] that reflected a main effect of

FIGURE 2. Conditioning of S11 and S21 cues (stages 1 and 4).A: Mean net rates (responses/minute) during S1 presentations forHPC/DG and control animals, presented in 2-day blocks, in stage 1.B: Mean net rates of responding in HPC/DG and control animalsduring the S11 and S12 trials of the first biconditional contextualdiscrimination and during presentations of the S21 trials in stage 4.

154 GOOD ET AL.

odor change for S11 (P , 0.001) but not for S12 (P . 0.50).The rates of responding during the ITI for the HPC/DG andcontrol animals were 0.67 rpm and 0.70 rpm, respectively, whichdid not differ (t , 1).

Acquisition of biconditional contextual discrimination 2 (stage6). Figure 4B–C shows the mean rates of responding, in 2-dayblocks, during acquisition of the second biconditional discrimina-tion (S21 and S22) and performance of the first biconditionaldiscrimination (S11 and S12) for the HPC/DG and controlgroups, respectively. The new discrimination was learned whileperformance was maintained on the first discrimination by bothgroups. An ANOVA, with group, block, discriminations 1 and 2,and stimulus significance (S1 vs. S2) as factors, showed no maineffect of group [F(1,16) 5 2.89, P . 0.10] or block [F(5,80) 51.51, P . 0.19]. There was a main effect of discrimination[F(1,16) 5 9.04, P , 0.01] that reflected the slightly higher rateof responding in the S21 and S22 discrimination (mean rate forstimuli X and Y 5 9.37 rpm, mean rate for W and Z 5 12.90rpm). There were no significant interactions of group with any ofthe factors (maximum F value 5 2.57, P . 0.12). The mean ratesof responding during the ITI for HPC/DG and control animals

were 0.74 rpm and 0.67 rpm, respectively, and these did not differ(t , 1).

GENERAL DISCUSSION

The main finding of the present study is a dissociation betweenthe incidental and contingent processing of context cues inducedby HPC/DG lesions. Rats given ibotenate HPC/DG lesions (1)displayed impaired ‘‘contextual specificity’’ of conditioned respond-ing when stimuli trained in one context were tested for the firsttime in a second context but (2) acquired a biconditionalcontextual discrimination, as did control subjects. This dissocia-tion was not secondary to a failure to discriminate contextsbecause it was apparent with newly conditioned stimuli in animalsdisplaying a contextual discrimination using previously trained stimuli.The lesion extended to approximately 90% of all hippocampal anddentate cell fields and was sufficient to impair spatial learning in awatermaze, and thus the dissociation is unlikely to be due to sparing ofhippocampal tissue. In discussing these findings, we shall consider their

FIGURE 3. Contextual specificity test (stages 2 and 5). Mean netrates of responding to the CS when presented in the same (S1) ordifferent (S2) context on day 1 of the first (S1; stage 2) and second(S2; stage 5) biconditional discriminations for HPC/DG (left) and

control (right) animals. The right histograms within each panelrepresent the mean rates of responding during the S11 and S12biconditional contextual discrimination during the second contextspecificity test (stage 5).


implications with respect to the contribution of the lesion techniqueand theories of hippocampal function.

Lesion Technique

One aim of the present study was to examine the effects ofselective HPC/DG lesions on acquisition of complex bicondi-tional contextual discriminations and the contextual control ofappetitive conditioned responding. The results clearly demon-strate that animals with HPC/DG damage can acquire andperform up to two biconditional contextual discriminationssimultaneously. The lesions damaged approximately 90% of cellfields in the hippocampus and dentate gyrus and were sufficient toimpair acquisition of spatial knowledge in the watermaze test.This pattern of results is consistent with the observations ofWhishaw and Tomie (1991) and McDonald et al. (1997) using aneurotoxic lesion technique but conflict with the findings ofGood and Honey (1991) using electrolytic lesions. The implica-tions are straightforward. First, the learning of biconditional tasks

must involve extrahippocampal connections that are damaged bythe older lesion technique but are unaffected by neurotoxiclesions. Second, some aspects of contextual processing survivehippocampal cell damage.

Theoretical Implications

There are several different theoretical ideas about hippocampalfunction to which the present results are relevant. A prominentview of the role of context cues has been to consider theirprocessing as an aspect of spatial learning, of scene memory, or ofconfigural learning using the ‘‘multimodal’’ cues that make upcontexts. These ideas do not seem capable of adequately capturingthe dissociation we found. For example, the spatial mappingtheory of hippocampal function (O’Keefe and Nadel, 1978)predicts either a deficit in biconditional discrimination learning (iflocale processing is used to discriminate the two contexts) or thelack of a deficit (if a taxon strategy is used). It is not clear, however,that the theory can predict the dissociation between impaired

FIGURE 4. Contingent use of context cues (stages 3 and 6). A:Mean net rates of responding during S1 and S2 trials of the first (X,Y) biconditional contextual discrimination for HPC/DG and controlanimals (stage 3). B–C: Mean net rates of responding for control and

HPC/DG animals, respectively, averaged over 2-day blocks, duringperformance of S11 and S12 trials of the first (X, Y) biconditionaldiscrimination and acquisition of the second S21, S2g2 (W, Z)biconditional discrimination (stage 6).

156 GOOD ET AL.

contextual specificity and unimpaired biconditional learningbecause the difference between these does not map in any obviousway onto the difference between the locale and taxon hypotheses.

Gaffan (1991) proposed that the hippocampus participates inlearning about the spatial arrangements of scenes and that thisinformation can then be used to retrieve personally experiencedinformation from memory. The process of learning about thespatial arrangement of a scene is distinguished from mere placelearning or the creation a cognitive map. Evidence in support ofthe latter distinction was provided by Gaffan and Harrison (1989)who found that monkeys with fornix transection could learn aplace discrimination task in which the reward value of particularobjects was conditional upon their location in the room. Thecontextual cues that constituted each place were different in eachdiscrimination problem. According to Gaffan (1991), the task didnot require the animal to discriminate between different spatialarrangements of these foreground and background cues and was,therefore, insensitive to hippocampal damage. The biconditionaldiscrimination task used in the present study has similarities to thetask developed by Gaffan and Harrison (1989). Different contextsacted as the conditional cues in the discriminations, but theanimals did not need to distinguish them on the basis of thespatial arrangement of the elements. Hippocampal lesionedanimals were also as sensitive as controls to the mispairing of theexteroceptive elements of the contexts, a mispairing that did notrequire a judgment of spatial location. Gaffan’s (1991) accountcannot, however, explain the differential outcome of the contex-tual specificity and biconditional parts of the experiment.

Other theories also suggest that acquiring a memory representa-tion of a context depends on the integrity of hippocampalfunction (e.g., Sutherland and Rudy, 1989; Kim and Fanselow,1992). However, if hippocampal damage impairs the formation ofa contextual representation, the learning of biconditional contex-tual discrimination should be impaired. This was not observed.Moreover, the results from the odor test indicate that hippocam-pal lesioned animals were as disrupted as controls by changing theconfiguration of the exteroceptive stimulus elements. The mostparsimonious explanation for this pattern of results is thathippocampal lesioned animals were able to form a representationof the context (see Maren et al., 1997), did so using the samecombination of stimulus elements as controls, and were somehowable to use this information to solve a biconditional discrimina-tion problem. A possibility is that the lesioned (and control)animals used a configural representation to solve the biconditionaltask. If so, the 1989 version of Sutherland and Rudy’s configuralassociation theory cannot explain this finding.

Rudy and Sutherland’s (1995) revision of the configuralassociation theory may also be relevant. In their original formula-tion of the theory, Sutherland and Rudy (1989) proposed adistinction between a configural association system and a simpleassociation system. Normal hippocampal function was thought tobe necessary for the formation of configural representations.Although able to accommodate a body of data, this theory cannotexplain the lack of hippocampal lesion deficits on certain types ofnonlinear configural tasks such as feature-neutral (Gallagher andHolland, 1992) biconditional discriminations (Whishaw and

Tomie, 1991; present study) and some cases of negative patterning(Davidson et al., 1993). Alvarado and Rudy (1995) suggestedthat, despite the logical similarity between negative patterning andfeature-neutral discriminations, these tasks may be solved differ-ently by control animals. Rudy and Sutherland’s (1995) revisionproposed that the hippocampus plays a more important role inconfigural learning when there is a conflict between the reinforce-ment contingencies associated with the compound stimulus andthe individual elements of the compound. Under these condi-tions, the hippocampal formation enhances the activation orsalience of configural representations, but these are encoded inother areas of the cortex. They predict that, because a bicondi-tional problem does not encourage competition between theelements, this task would not be sensitive to hippocampal damage.This aspect of the revised configural association theory wouldappear to be supported by the results of the present experiment.However, one implication of the theory by Rudy and Sutherland(1995) is that a biconditional problem may become sensitive tohippocampal damage if the elements undergo differential reinforce-ment outside the compounds (e.g., AX1, A2, AY2; BX2, B2,BY1). In the present biconditional discrimination, the elementsof the compound were subject to different reinforcement contin-gencies outside the compound. Stimulus X is reinforced in contextA (X1) and not reinforced in context B (X2), and context A isreinforced during the compound (AX1) but is not reinforcedoutside this compound on all other occasions (A2, AY2).However, the present study may not represent a definitive test ofthe predictions of the hypothesis by Rudy and Sutherland (1995)regarding competition between elemental cues and their config-ural representations.

A different type of context hypothesis to which these resultsmay be relevant is the notion that hippocampal function underliesthe effective contextual retrieval of associative information (e.g.,Hirsh, 1974, 1980). Hirsh’s original account predicts a hippocam-pal deficit in all forms of conditional learning. To the extent thatthe biconditional task used in the present study requires a conditionalsolution, the results do not support Hirsh’s (1974, 1980) account ofhippocampal function. His account, however, may be rescued if it isassumed that the role of the context in helping to retrieve associativeinformation is something that can be supported by automatic,incidental processing in the hippocampus, with traditional conditionaltasks being considered ambiguous because they can be acquired inother ways. We pursue this possibility below.

A different explanation for why hippocampal lesioned animalscan acquire a complex biconditional discrimination but showimpaired context specificity of conditioned responding on the firstday of training may that they are slow to inhibit conditionedresponding. There are also several reasons to doubt this explana-tion. First, the absolute level of responding on trials on which X,Y, W, and Z were presented for the first time in the ‘‘wrong’’context was the same in HPC/DG and control animals. Thedifference between groups arose because of the higher level ofresponding on ‘‘training context’’ trials in control animals (see Fig.3). This finding suggests that control animals are benefitting fromsome process, such as context retrieval, that operates primarily ontrials in the original training context. Second, if there was


impaired inhibition, acquisition of the biconditional discrimina-tions should be more severely disrupted. Not only did we fail toobserve this, but excitotoxic hippocampal damage does not impairacquisition of discriminative responding in other conditional andconfigural learning tasks (cf. Gallagher and Holland, 1992) andmay even yield superior performance in reversal of simplediscriminations (see Whishaw and Tomie, 1991). Impaired re-sponse inhibition seems an unlikely account of the pattern ofresults (for further discussion, see Good and Bannerman, 1997).

Incidental and Contingent Processingof Context Cues

One way of characterizing the difference between the bicondi-tional contextual discrimination and the test for contextualspecificity is that only in the former case do the reinforcementcontingencies explicitly require the animal to process contextualcues; the solution of the task can be said to be ‘‘contingent’’ ontheir processing. However, in the training that precedes the test ofcontext specificity, the context does not have to be processed; itconsists of cues that are merely ‘‘incidental’’ to the task demandsimposed on the animal. A somewhat similar characterisation,derived from work on contextual fear conditioning, was intro-duced by Phillips and LeDoux (1994). They found that lesions ofthe dorsal hippocampus resulted in a deficit in fear conditioningto contextual cues only under conditions where the uncondi-tioned stimulus (US) was signaled by an explicit CS. Condition-ing to the context itself using presentations of the US in theabsence of an explicit CS was unimpaired by hippocampaldamage. Phillips and LeDoux interpreted these results as reflectinga role for the hippocampus in ‘‘background’’ contextual condition-ing, where the primary or ‘‘foreground’’ association involved anexplicit CS paired with a US. This situation was distinguishedfrom ‘‘foreground’’ contextual fear conditioning, where the US isdelivered in the absence of a CS. There is an intriguing parallelbetween the results of Phillips and LeDoux (1994) and those ofthe present study. Hippocampal lesioned animals displayed im-paired contextual processing under conditions in which context cueswere merely a ‘‘background’’ in which a CS–US conditioning task tookplace. However, when the solution to the biconditional discriminationproblem was contingent upon context processing, hippocampal le-sioned animals were able to learn as efficiently as controls.

The question remains of how best to characterise the psychologi-cal processes that can accommodate a distinction between contin-gent and incidental use of contextual information or betweenforeground and background processing.

The key observation is that hippocampal lesioned animals areimpaired in processing contextual information only under certainconditions. Lesioned animals are able to learn about and usecontextual information when the solution of a problem iscontingent on their use or when the context is in the foregroundof a conditioning experience. In contrast, hippocampal lesionsimpair context processing when their processing is incidental orwhen context is in the background of a conditioning episode. Thisdissociation does not appear to be amenable to explanation by themajority of current theories of hippocampal function, includingspatial learning, configural learning, and contextual processing. In

attempting to develop a hypothesis that captures this dissociation,it is necessary to consider the context specificity test in moredetail. Animals clearly need to have acquired a representation ofthe conditioning episodes that include details of the context inwhich learning occurs. One possible way in which this informa-tion could be represented is in the form of a configural representa-tion (for discussion, see Lovibond et al., 1984). The initialconditioned response may be governed by a CS that is a configuralrepresentation of the target CS and the context. Hippocampaldamage may disrupt the formation of such a configural representa-tion and thus impair the decrement in conditioned respondingwhen the elements of configural stimuli are changed. However,the failure to find evidence for context specificity of habituationhas been used as an argument against a configural account of thecontext specificity of conditioning in control animals (Hall andHoney, 1989). In addition, this is not an adequate account of theeffects of hippocampal damage in the present experiment becausethe same lesioned animals were able to acquire a biconditionaldiscrimination that may also be solved effectively by the use ofconfigural cues. For an animal to display contextual specificity, atleast one component of the processing engaged by the test mustinvolve identifying a mismatch between the memory of theconditioning events previously presented in that environment andthe current pattern of stimulation. The detection of a mismatchwould require the retrieval of information about past relationshipsbetween cues that have occurred in a context and comparison ofthis information with current sensory input. Within this scheme,hippocampal damage might be impairing (a) the encoding ofcontext information (i.e., the formation of a context representa-tion), (b) the retrieval of information about cue relationships,and/or (c) the detection of a mismatch between previous andcurrent sensory experience. With respect to (a), there is a growingbody of evidence to suggest that the formation of a contextrepresentation per se is not impaired following hippocampaldamage (Good and Honey 1997; Maren et al., 1997; McNish etal., 1997). Furthermore, the comparable disruption in theperformance of control and HPC/DG lesioned animals when theexteroceptive elements of the context were switched in the presentstudy (the odor test) suggests that the lesion did not disrupt theformation of a context representation. With respect to (b) and (c),the present pattern of results do not, unfortunately, allow us todistinguish between the retrieval and mismatch detection hypoth-eses. Honey et al. (1998) showed that hippocampal damageimpairs the detection of a mismatch between serial presentationsof auditory and visual punctate cues in a simple habituationprocedure. It is worth noting that retrieval and mismatchfunctions have been described for different subfields of thehippocampus, and both functions may contribute overall to hippocam-pal memory processing (cf. Granger et al., 1996; Rolls, 1996).

CONCLUSION

The pattern of spared and impaired context processing follow-ing hippocampal lesions in the present study suggests that

158 GOOD ET AL.

hippocampal damage impairs the incidental processing of contex-tual cues. The results are consistent with the view that context cuesmay have at least two different roles in cognition, one supportinghigher-order processes, such as retrieval and/or mismatch detec-tion, that are engaged during incidental processing of context anda second process supporting associative learning involving thecontingent use of context information.

Acknowledgments

This research was funded by a Programme Grant to ProfessorR.G.M. Morris from the United Kingdom Medical Research Council.We thank Elma Forrest for conducting the histology and RobertHoney for commenting on an earlier version of this manuscript.

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