A limited role for the hippocampus in the modulation of novel-object preference by contextual cues

Recent evidence suggests that rats require an intact hippocampus in order to recognize familiar objects when they encounter them again in a different context. The two experiments reported here further examined how changes in context affect rats' performance on the novel-object preference (NOP) test of object-recognition memory, and how those effects interact with the effects of HPC damage. Rats with HPC lesions and control rats received NOP testing in either the same context in which they had previously encountered sample objects, or in a different but equally familiar context. In Experiment 1, the two contexts had very few overlapping cues within or outside the apparatus; thus, the differences between them were global. Consistent with previous results, control rats showed a novel-object preference in both the unchanged and (globally) changed contexts, whereas rats with HPC lesions displayed a preference only in the unchanged context. In Experiment 2, the context shift included only local features proximal to the test objects. The main results were the reverse of Experiment 1--rats with HPC lesions displayed a novel-object preference in both the unchanged and (locally) changed contexts, whereas control rats displayed a preference only in the unchanged context. The findings are consistent with the view that HPC damage does not cause a general inability to recognize objects, nor an inability to encode or store a representation of the context in which the objects are encountered. They suggest instead that HPC damage impairs the ability to remember specific locations of familiar objects within a particular context.     

Olfactory stimuli as context cues in human memory

Olfactory stimuli were used as context cues in a recognition memory paradigm. Male college students were exposed to 50 slides of the faces of college females while in the presence of a pleasant or an unpleasant odor. During the acquisition phase, ratings of physical attractiveness of the slides were collected. After a 48-hr delay, a recognition test was given using the original 50 slides and 50 new slides. The recognition test was conducted with either the original odor or the alternative odor present. A no-odor control group did not receive olfactory cues. The attractiveness ratings indicated that the odor variations had no effect on these social judgments. Analyses of d' scores, hits, and false alarms for the recognition performance indicated support for the predicted interaction in which presence of the same odor at both sessions led to better overall performance.     

Acetylcholine release in the hippocampus and prelimbic cortex during acquisition of a socially transmitted food preference

Interference with cholinergic functions in hippocampus and prefrontal cortex impairs learning and memory for social transmission of food preference, suggesting that acetylcholine (ACh) release in the two brain regions may be important for acquiring the food preference. This experiment examined release of ACh in the hippocampus and prefrontal cortex of rats during training for social transmission of food preference. After demonstrator rats ate a food with novel flavor and odor, a social transmission of food preference group of rats was allowed to interact with the demonstrators for 30 min, while in vivo microdialysis collected samples for later measurement of ACh release with HPLC methods. A social control group observed a demonstrator that had eaten food without novel flavor and odor. An odor control group was allowed to smell but not ingest food with novel odor. Rats in the social transmission but not control groups preferred the novel food on a trial 48 h later. ACh release in prefrontal cortex, with probes that primarily sampled prelimbic cortex, did not increase during acquisition of the social transmission of food preference, suggesting that training-initiated release of ACh in prelimbic cortex is not necessary for acquisition of the food preference. In contrast, ACh release in the hippocampus increased substantially (200%) upon exposure to a rat that had eaten the novel food. Release in the hippocampus increased significantly less (25%) upon exposure to a rat that had eaten normal food and did not increase significantly in the rats exposed to the novel odor; ACh release in the social transmission group was significantly greater than that of the either of the control groups. Thus, ACh release in the hippocampus but not prelimbic cortex distinguished well the social transmission vs. control conditions, suggesting that cholinergic mechanisms in the hippocampus but not prelimbic cortex are important for acquiring a socially transmitted food preference.     

Short- and long-term decrements in toxicosis-induced odor-aversion learning: the role of duration of exposure to an odor

Six experiments employed an odor-aversion paradigm to investigate the role of the duration of exposure to an odor in determining that odor's subsequent associability with illness. Rats were exposed to an odor at times T1 and T2, and the second of these exposures was followed by toxicosis. When the initial odor exposure was brief, the odor aversion was attenuated with a moderate T1-T2 interval of 3 hr (Experiment 1) but not with long intervals of 28 hr and 76 hr (Experiment 2). In contrast, when the initial odor exposure was long, the odor aversion was attenuated at a long T1-T2 interval (Experiment 3). With a T1-T2 interval of 24 hr, a brief initial exposure did not attenuate odor aversions when the context either remained the same or was changed from T1 to T2, whereas a long initial exposure attenuated such aversions when the context remained the same but not when the context was changed (Experiment 4). With a T1-T2 interval of 3 hr, a brief initial exposure attenuated odor aversions when the context remained the same or was changed from T1 to T2, whereas a long initial exposure attenuated such aversions when the context remained the same but not when the context was changed (Experiment 5). A brief exposure at T1, either with or without a subsequent context "extinction," attenuated odor aversions when the T1-T2 interval was 3 hr but not when this interval was 24 hr; a long initial exposure at T1, without a subsequent context "extinction," attenuated odor aversions when the T1-T2 interval was 4 hr and 24 hr but with a subsequent context "extinction" did not attenuate such aversions at either 4-hr or 24-hr T1-T2 intervals (Experiment 6). The results demonstrate that the duration of exposure to an odor determined whether that odor presentation caused short- or long-term decrements in odor conditionability and are discussed in terms of the relation between self- and retrieval-generated processes.     

Ultrasonic vocalizations by male house mice (Mus musculus) to novel odors: roles of infant and adult experience

Two experiments were conducted to examine 70-kHz ultrasonic courtship vocalizations by adult male mice (Mus musculus) to novel odors following exposure to these odors in infancy and/or adulthood. The research was performed in hopes of better understanding the experiences giving rise to vocalizations to naturally occurring chemosignals. Experiment 1 demonstrated that adult males normally do not vocalize to the urine of female rats but would come to do so if adult female mice odorized with female rat urine were repeatedly encountered postpubertally. On the other hand, encountering their own mother odorized with female rat urine from birth until weaning did not promote vocalizations to the urine of female rats. Experiment 2 was designed to examine vocalizations to the urine of female mice whose urinary odor was altered by the ingestion of fenugreek, a spice. Although the magnitude of the effect was smaller in this experiment, greater amounts of vocalization again were seen by males that as adults encountered females that had ingested fenugreek. Males with such experience also showed a small but significant elevation in vocalizations to the fenugreek odor itself. Again, experience with the novel odor during infancy was not associated with elevated vocalizations during adulthood either to fenugreek-altered urine or to the fenugreek odor itself. Thus vocalizations to two different novel odors occurred only after an adult male had encountered an adult female odorized with the novel odor. On the other hand, none of the novel odor experiences eliminated vocalizations to the naturally occurring chemosignal in female mouse urine.(ABSTRACT TRUNCATED AT 250 WORDS)     

Extinction and latent inhibition of within-event learning are context specific

Exposure to a solution composed of an odor (almond) and a taste (salt) produced a context-independent preference when rats were subsequently tested with almond under a salt appetite. Postcompound exposure to either the almond or the salt alone reduced almond preferences but only when rats were tested in the extinction context. Exposure to either the almond or the salt in 1 context in advance of exposure to the compound in a different context also reduced preferences but only when the rats were tested in the context in which the element had been pre-exposed. These results show that extinction and latent inhibition of within-event learning are context specific.     

Olfactory context and memory retrieval in 3-month-old infants

Three experiments examineed whether olfactory stimuli can produce context-dependent effects in infant memory. In eash, 3-month-old infants learned to kick to control the movement of an overhead modile in the presence of an ambient odor. Retention was assessed 1, 3, or 5 days later. During the retention test, the olfactory context was either the same odor, a different odor, or “no odor.” At 1 day, infants exhibited retention when tested in the presence of the same odor. Infants in the no odor condition exhibited partial retention, whereas memory retrieval was completely disrupted for infants tested in the presence of the different odor. After the 3- and 5-day intervals, all groups showed forgetting. These results were not consistent with recent studies of 3-month-old infants trained and tested in the presence of a distinctive visual and auditory context. The findings suggest that olfactory stimuli are a silent feature of the environment for 3-month-old infants, but that they function as context cues in a way that differs from other sensory modalities.     

The role of the dorsal and ventral hippocampus in olfactory working memory

Olfactory working memory and pattern separation for odor information was assessed in male rats using a matching-to-sample for odors paradigm. The odor set consisted of a five aliphatic acids with unbranched carbon chains that varied from two- to six-carbons in length. Each trial consisted of a sample phase followed by a choice phase. During the sample phase, rats would receive one of five different odors. Fifteen seconds later during the choice phase one of the previous odors was presented simultaneously side by side with a different odor that was based on the number of aliphatic acids that varied in the carbon chains from two- to six-carbons in length and rats were allowed to choose between the two odors. The rule to be learned in order to receive a food reward was to always choose the odor that occurred during the study phase. Odor separations of 1, 2, 3 or 4 were selected for each choice phase and represented the carbon chain difference between the study phase odor and the test phase odor. Once an animal reached a criterion of 80–90% correct across all temporal separations based on 40 trials, rats received a control, dorsal hippocampal, or ventral hippocampal lesion and were retested on the task. On postoperative trials, only the ventral hippocampal lesion group was impaired relative to both control and dorsal hippocampal groups groups. There were no effects on odor pattern separation. All groups of rats could discriminate between the odors. The data suggest that the ventral hippocampus, but not dorsal hippocampus, supports working memory for odor information.     

Odor-context effects in free recall after a short retention interval: A new methodology for controlling adaptation

The present study investigated context effects of incidental odors in free recall after a short retention interval (5 min). With a short retention interval, the results are not confounded by extraneous odors or encounters with the experimental odor and possible rehearsal during a long retention interval. A short study time condition (4 s per item), predicted not to be affected by adaptation to the odor, and a long study time condition (8 s per item) were used. Additionally, we introduced a new method for recovery from adaptation, where a dissimilar odor was briefly presented at the beginning of the retention interval, and we demonstrated the effectiveness of this technique. An incidental learning paradigm was used to prevent overshadowing from confounding the results. In three experiments, undergraduates (N = 200) incidentally studied words presented one-by-one and received a free recall test. Two pairs of odors and a third odor having different semantic-differential characteristics were selected from 14 familiar odors. One of the odors was presented during encoding, and during the test, the same odor (same-context condition) or the other odor within the pair (different-context condition) was presented. Without using a recovery-from-adaptation method, a significant odor-context effect appeared in the 4-s/item condition, but not in the 8-s/item condition. Using the recovery-from-adaptation method, context effects were found for both the 8- and the 4-s/item conditions. The size of the recovered odor-context effect did not change with study time. There were no serial position effects. Implications of the present findings are discussed.     

Context extinction following conditioning with delayed reward enhances subsequent instrumental responding

In Experiment 1, delayed reward generated low response rates relative to immediate reward delivered with the same frequency. Lister rats exposed to delayed reward subsequently responded at a higher rate in extinction if they received nonreinforced exposure to the conditioning context after instrumental training and prior to test, compared with animals that received home cage exposure. In Experiment 2, a signaled delay of reinforcement resulted in higher rates than an unsignaled delay. Nonreinforced exposure to the conditioning context elevated response rate for subjects in the unsignaled condition relative to a home cage group, but had no effect on response rates for subjects that had received the signaled delay. In Experiment 3, following an unsignaled reinforcement delay, groups receiving either no event or signaled food in the context responded faster in extinction than groups receiving no context exposure or unsignaled food.     

Contextual factors in neophobia and its habituation: The role of absolute and relative novelty

In four experiments we investigated the role of contextual cues in the habituation of neophobia in rats. Experiment 1 showed that the consumption of a novel flavour increased across a series of presentations in one context (A) but fell when the flavour was subsequently presented in a second, novel, context (B). In Experiments 2 and 3, subjects again received exposure to a flavour in context A, but also were familiarized with the test context, B. These subjects consumed the flavour with equal readiness, whether it was presented in Context A or in Context B at test. Experiment 4 replicated the results of Experiment 1 and also showed that the consumption of a novel flavour was not influenced by whether it was presented in a novel or a familiar context. Several mechanisms by which the novelty or familiarity of the context might interact with the novelty or familiarity of the flavour were discussed.     

Memory for lateral orientation of slides in picture stories

Three picture stories were constructed by taking slides of people involved in three different activities. Two sequences of these slides were presented. Subjects were asked whether or not each slide in the second sequence was in the same lateral orientation as in the first sequence. Experiment 1 presented the slides in correct or random sequence and in correct or random lateral orientation (2 by 2 design). The two groups who received correct orientation excelled in recognition of orientation in the test series. Experiment 2 replicated the random orientation condition, found that pre-warning of the recognition task had no effect on performance, and suggested that these subjects did not make use of the events in determining laterality. Experiment 3 replicated the correct order and orientation condition and further revealed that new but appropriate slides in the test series were accurately judged as to lateral orientation which fit the context of the original stories.     

Context specificity of operant discriminative performance in pigeons: II. Necessary and sufficient conditions

Six experiments were performed to explore the necessary and sufficient conditions for producing context specificity of discriminative operant performance in pigeons. In Experiment 1, pigeons learned a successive discrimination (red S+/blue S−) in two chambers that had a particular odor present and between which they were frequently switched. The birds subsequently learned the reversal (blue S+/ red S−) in one of these chambers with a different odor present. When switched to the alternative chamber, although the odor and the reinforcement contingency were still appropriate to the reversal, performance appropriate to the original discrimination recurred in subjects for which the houselights were on during training and testing but not for those for which the houselights were off. This indicated the importance of visual contextual cues in producing context specificity. Experiment 2 showed that the frequent switching between boxes in initial training was of no consequence, presumably because the apparatus cues were highly salient to the subjects. Experiment 3 showed significantly less context specificity when odor cues were omitted. Experiment 4 showed that simply using a different reinforced stimulus in each phase of training was ineffective in producing context specificity. Experiment 5 showed that the generalization test procedure used in Experiment 4 was sensitive to context specificity when discrimination-reversal training was used with different odors in the two training phases. Experiment 6 replicated the results of Experiment 4, but then showed that when different odors accompanied the two training phases, context specificity was obtained with the single-stimulus paradigm. Thus in both single-stimulus and discrimination-reversal paradigms, redundant odor cues potentiated learning about apparatus cues.     

Context-dependent olfactory learning in an insect

We studied the capability of the cricket Gryllus bimaculatus to select one of a pair of odors and to avoid the other in one context and to do the opposite in another context. One group of crickets was trained to associate one of a pair of odors (conditioned stimulus, CS1) with water reward (appetitive unconditioned stimulus, US+) and another odor (CS2) with saline solution (aversive US, US-) under illumination and to associate CS1 with US- and CS2 with US+ in the dark. Another group of crickets received training of the opposite stimulus arrangement. At 1 d after the training for 3 d, the former group significantly preferred CS1 over CS2 under illumination but preferred CS2 over CS1 in the dark, and the latter group exhibited the opposite odor preference. The results of control experiments showed that the background light condition had no significant effects on memory formation or retrieval unless it was explicitly associated with US during training. Thus, the visual context affected learning performance only when crickets were requested to use it to disambiguate the meaning of CSs and to predict USs.     

Effects of neonatal handling on play behavior and fear towards a predator odor in juvenile rats (Rattus norvegicus)

The effects of brief daily separation, also known as "handling," during the first 2 weeks of life on play behavior and fearfulness toward a predatory odor were assessed in juvenile rats. Handled rats were more playful than nonhandled control rats, and while handling had no effect on the direct response of these rats toward a predatory odor, handled rats did not exhibit a conditioned suppression of play when tested later in the same context where they had been exposed to the predatory odor. Handled rats were still wary of the environment in that they continued to show a heightened level of risk assessment behavior. These data suggest that early postnatal experiences may play a significant role in determining how an animal deals with predatory threats later in life.     

Recognition memory for social and non-social odors: differential effects of neurotoxic lesions to the hippocampus and perirhinal cortex

The contributions of the hippocampus (HC) and perirhinal cortex (PER) to recognition memory are currently topics of debate in neuroscience. Here we used a rapidly-learned (seconds) spontaneous novel odor recognition paradigm to assess the effects of pre-training N-methyl-D-aspartate lesions to the HC or PER on odor recognition memory. We tested memory for both social and non-social odor stimuli. Social odors were acquired from conspecifics, while non-social odors were household spices. Conspecific odor stimuli are ethologically-relevant and have a high degree of overlapping features compared to non-social household spices. Various retention intervals (5 min, 20 min, 1h, 24h, or 48 h) were used between study and test phases, each with a unique odor pair, to assess changes in novelty preference over time. Consistent with findings in other paradigms, modalities, and species, we found that HC lesions yielded no significant recognition memory deficits. In contrast, PER lesions caused significant deficits for social odor recognition memory at long retention intervals, demonstrating a critical role for PER in long-term memory for social odors. PER lesions had no effect on memory for non-social odors. The results are consistent with a general role for PER in long-term recognition memory for stimuli that have a high degree of overlapping features, which must be distinguished by conjunctive representations.     

Mechanisms of blocking by contextual stimuli

The influence of contextual stimuli on the conditioning and performance of responding to a discrete stimulus was examined in the US preexposure paradigm using both context shift manipulations and a measure of context conditioning. Four groups of rats received both repeated exposure to an electric shock US in one context (Context 1), and repeated nonshocked exposure to a second context (Context 2). Two additional groups of rats received exposure to these contexts, but never received shock presentations. Rats exposed to shock learned to escape from the stimuli of Context 1, but did not escape from the stimuli provided by Context 2. Rats not exposed to shock failed to escape from either context. All rats then received a single CER conditioning session in which four pairings of a 3-min noise CS and shock US were presented. Half the rats received those CS-US pairings in the excitatory Context 1, while the remaining rats received those pairings in the neutral Context 2. Finally, half the rats in each of the CER conditioning treatments received extinction test trials of the noise CS in Context 1, while the remaining rats received those test trials in Context 2. Thus, this design factorially manipulated the presence of excitatory or neutral contextual stimuli during both conditioning and testing of a discrete CS. In comparison with the two groups of rats never preexposed to shock alone, attenuation in acquisition of conditioned suppression observed during test trials occurred only when CER conditioning had been administered in the excitatory Context 1, and this effect was manifested when testing occurred in either the excitatory Context 1 or the neutral Context 2. These results support the model of R. A. Rescorla and A. R. Wagner (1972) (in A. H. Black & W. F. Prokasy (Eds.) Classical Conditioning II, pp. 64–99, New York: Appleton-Century-Crofts) which asserts that contextual stimuli and sicrete CSs compete for limited associative strength supportable by a given US.     

Superlatent inhibition and spontaneous recovery: differential effects of pre- and postconditioning CS-alone presentations after long delays in different contexts

In two pairs of three-stage conditioned taste aversion experiments, we examined the effects of delay interval (1 or 21 days) between the second and third stages, and of context in which the animals spent the delay (same as or different from the context of the other stages) on latent inhibition (LI) and spontaneous recovery following extinction. In the LI experiments (Experiments 1A and 1B), the first stage comprised nonreinforced presentations to saccharin or to water. In the second stage, rats were conditioned by saccharin paired with LiCl. In the extinction experiments (Experiments 2A and 2B), the order of the stages was reversed. For all experiments, Stage 3, the test stage, consisted of three presentations of saccharin alone. There was a super-LI effect in the saccharin-preexposed group that spent the 21-day delay in the different context (Experiment 1A). When the delay was spent in the same context, there was no difference in the amount of LI between the short- and long-delay groups (Experiment 1B). Conversely, there was a spontaneous recovery effect in the long-delay/same-context group (Experiment 2B), but not in the long-delay/different-context group (Experiment 2A). The pattern of results, incompatible with current explanations of delay-induced changes in memory performance, was interpreted in terms of an interaction between the delay conditions (same or different delay context), which modulate the extinction of previously acquired context-CS-nothing associations (during CS-alone presentations), and primacy effects.     

The mind's nose: Effects of odor and visual imagery on odor detection

Abstract— We examined odor imagery by looking for its effects on detection of weak odors. Seventy-two healthy subjects performed a forced-choice odor detection task in one of three conditions: after being told to imagine an odor (odor imagery), after being told to imagine an object (visual imagery), or without having received imagery instructions (no-imagery control). For the two imagery conditions, the presented and imagined stimuli were either the same (matched) or different (mismatched). There was a significant difference between detection in the matched and mismatched conditions for odor imagery, but not for visual imagery. We conclude that our paradigm does measure odor imagery and that the effect of imagery on detection is both content- and modality-specific. Further, the difference between conditions was due to lower detection with mismatched odor imagery than without imagery, indicating that interference underlies the effect.     

Augmentation, not blocking, in an A+/AX+ flavor-conditioning procedure

An A+/AX+ Pavlovian conditioning design typically produces weakened or blocked conditioning to stimulus X. Two experiments were conducted in which rats first received an odor (A+) paired with an emetic US, and then received odor and taste (AX+) paired with the US. In both experiments, the preconditioned odorfacilitated conditioning to the taste. In Experiment 1, a group that received two odor-illness pairings in A+ conditioning had a stronger taste aversion than a group that only had a single odor-illness pairing. Experiment 2 demonstrated that the strengthened taste aversion in the A+/AX+ condition was not due to stimulus generalization. The results represent a unique outcome in the flavor-aversion literature that is similar to potentiation. We propose that this facilitated conditioning to X in the A+/AX+ design be termedaugmentation.