Hippocampal substrate of sensory associations

doi:10.1016/0031-9384(87)90167-3

Physiology & Behavior

Volume 39, Issue 5, 1987, Pages 643-647

https://doi.org/10.1016/0031-9384(87)90167-3 Get rights and content

Abstract

The role of the hippocampus in the association of two conditional stimuli was evaluated using the conditioned rabbit NM preparation and a sensory preconditioning paradigm. Multiple-unit activity was recorded from field CA1 during preconditioning. Paired presentations of CS1 and CS2 resulted in increased excitability which was highly correlated with later preformance during CS2 test sessions. Unpaired presentations evoked a response to stimulus onset often followed by an inhibitory period. Bilateral kainic acid lesions of CA1 had no deleterious effect on traditional CS-US conditioning but abolished the association of CS1 and CS2. These data suggest that the hippocampus may be vital to the association of sensory events. Further, the SPC paradigm could provide an excellent model for evaluating simple cognitive deficits.

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Cited by (47)

Anterior cingulate neurons signal neutral cue pairings during sensory preconditioning
2022, Current Biology
Citation Excerpt :
We showed that ACC neurons not only responded to reward-based information and inference, but they also formed associative correlates of the simple form of latent learning that occurs during the first phase of sensory preconditioning. Our findings add to a small but growing body of literature demonstrating correlates20,33 and necessity of hippocampal and cortical17,34–37 areas for latent learning as assessed by sensory preconditioning. While these findings are not necessarily at odds with theories of ACC function that emphasize value, they would require these theories be expanded to include the observation that ACC neurons form associative correlates in the absence of explicitly rewarding or punishing outcomes.
Of all frontocortical subregions, the anterior cingulate cortex (ACC) has perhaps the most overlapping theories of function.1, 2, 3 Recording studies in rats, humans, and other primates have reported diverse neural responses that support many theories,4, 5, 6, 7, 8, 9, 10, 11, 12 yet nearly all these studies have in common tasks in which one event reliably predicts another. This leaves open the possibility that ACC represents associative pairing of events, independent of their overt biological significance. Sensory preconditioning¹³ provides an opportunity to test this. In the first phase, preconditioning, value-neutral sensory stimuli are paired (A→B). To test whether this was learned, subjects are given standard conditioning during which one of the previously neutral sensory cues is paired with a biologically meaningful outcome (B→outcome). During the final probe test, the neutral cue which was never paired with a biologically meaningful outcome is presented alone (A→) and will elicit a conditional response, suggesting that subjects had learned the associative structure during preconditioning and use that knowledge to infer presentation of the biologically relevant outcome (A→B→outcome). Inference-based responding demonstrates a fundamental property of model-based reasoning¹⁴^,¹⁵ and requires learning of the associations between neutral stimuli before rewards are introduced.16, 17, 18, 19 ACC neurons developed firing patterns that reflected the learning of sensory associations during preconditioning, even though no rewards were present. The strength of these correlates predicted rats’ ability to later mobilize and use that associative information during the probe test. These results demonstrate that clear biological significance is not necessary to produce correlates of learning in ACC.
Retrosplenial cortex and its role in cue-specific learning and memory
2019, Neuroscience and Biobehavioral Reviews
Citation Excerpt :
The role of the hippocampus in sensory preconditioning, however, is not clear. For example, pre-training lesions of the hippocampus have been shown to impair sensory preconditioning of the rabbit’s nictitating membrane response (Port et al., 1987) and conditioned suppression in rats (Talk et al., 2002). In both of these studies, the sensory stimuli were either visual or auditory cues.
The retrosplenial cortex (RSC) contributes to spatial navigation, as well as contextual learning and memory. However, a growing body of research suggests that the RSC also contributes to learning and memory for discrete cues, such as auditory or visual stimuli. In this review, we summarize and assess the Pavlovian and instrumental conditioning experiments that have examined the role of the RSC in cue-specific learning and memory. We use the term cue-specific to refer to these putatively non-spatial conditioning paradigms that involve discrete cues. Although these paradigms emphasize behavior related to cue presentations, we note that cue-specific learning and memory always takes place against a background of contextual stimuli. We review multiple ways by which contexts can influence responding to discrete cues and suggest that RSC contributions to cue-specific learning and memory are intimately tied to contextual learning and memory. Indeed, although the RSC is involved in several forms of cue-specific learning and memory, we suggest that many of these can be linked to processing of contextual stimuli.
Hippocampal subfield volume changes in subtypes of attention deficit hyperactivity disorder
2018, Brain Research
Citation Excerpt :
The fimbria/fornix fiber pathway is connecting the hippocampus to subcortical structures. Lesions to fimbria (i.e., cut of fiber pathways) disrupt subcortical inputs to the hippocampus and may abolish sensory preconditioning in animals (Port et al., 1987). Therefore, reduced fimbria region in combined ADHD may cause an altered information flow throughout the hippocampus and subcortical regions.
Attention-deficit hyperactivity disorder (ADHD) is accompanied by reduction of total hippocampal volume. However, disorder-related fine-grained structural alterations of hippocampal subfields remain unclear.
Here we compared hippocampal subfield volumes in a large sample of patients with ADHD and healthy controls. We used T1-weighted structural 3-Tesla MRI images of 880 individuals (7–21 years old) from the ADHD-200 database. The images were acquired from 553 healthy individuals and 327 children and adolescents with combined (N = 196) and inattentive (N = 131) ADHD subtypes. Hippocampal subfields were segmented into the cornu amonis regions (CA1, CA2/3, CA4), fimbria, hippocampal fissure, presubiculum, subiculum, hippocampal tail, parasubiculum, granule cell layers of the dentate gyrus, molecular layer within the subiculum and the CA fields, and the hippocampal-amygdala transition area using an automatic algorithm available in Freesurfer 6.0.
We found a significant reduction of total hippocampal volume in the combined ADHD group compared to healthy controls. This reduction was due to the atrophy of CA1, CA4, molecular layer, granule cell layers of the dentate gyrus, presubiculum, subiculum, and hippocampal tail. These differences were exclusively driven by the corresponding brain volume reduction in the combined ADHD-subtype, while hippocampal volumes in inattentive ADHD showed no reliable differences relative to controls. Finally, there were negative correlations between the reduced hippocampal subfields and behavioral ADHD indices.
The present results point to a clear dissociation between inattentive and combined subtypes of ADHD. Therefore, hippocampal subfields may contribute towards understanding the pathophysiology of ADHD.
Novel sensory preconditioning procedures identify a specific role for the hippocampus in pattern completion
2016, Neurobiology of Learning and Memory
Citation Excerpt :
The nature of this process can be investigated using sensory preconditioning (SPC): where exposure to a pattern (AX; e.g., an audio-visual compound) can allow fear conditioned to X to be evident during A (e.g., Brogden, 1939; Rescorla, 1980). SPC is disrupted by lesions of hippocampus made prior to behavioral testing in both rabbits (Port, Beggs, & Patterson, 1987) and rats (Talk, Gandhi, & Matzel, 2002; see also, Eichenbaum, Mathews, & Cohen, 1989; but see, Honey & Good, 2000). However, the pattern completion processes that underpin SPC is often characterized in two ways: A could elicit fear at test through the operation of an (elemental) A-X-footshock associative chain (e.g., Hebb, 1943), the component links being forged during exposure to A with X (A-X) and conditioning with X (X-footshock).
Successful retrieval of a memory for an entire pattern of stimulation by the presentation of a fragment of that pattern is a critical facet of memory function. We examined processes of pattern completion using novel sensory preconditioning procedures in rats that had either received sham lesions (group Sham) or lesions of the hippocampus (group HPC). After exposure to two audio-visual patterns (AX and BY) rats received fear conditioning with X (but not Y). Subsequent tests assessed fear to stimulus compounds (e.g., AX versus BX; Experiment 1) or elements (A versus B; Experiment 2). There was more fear to AX than BX in group Sham but not group HPC, while there was more fear to A than B in group HPC, but not in group Sham. This double dissociation suggests that pattern completion can be based upon separable processes that differ in their reliance on the hippocampus.
Reinstatement of conditioned fear and the hippocampus: An attentional-associative model
2007, Behavioural Brain Research
An existing attentional-associative model of classical conditioning [Schmajuk N, Lam Y, Gray JA. Latent inhibition: a neural network approach. J Exp Psychol: Anim Behav Process 1996;22:321–49] is applied to the description of reinstatement in animals and humans. According to the model, inhibitory associations between the context (CX) and unconditioned stimulus (US) are formed during extinction, which help preserve the association between the conditioned stimulus (CS) and the US. However, summation and retardation tests fail to reveal these associations because (a) the CX is not attended or (b) a CX–CS configural stimulus formed during extinction is both poorly attended and weakly active during testing. When US presentations and testing occur in the same context, reinstatement is the consequence of a decreased CX inhibition and the increased attention to the CS, which activates the remaining CS–US association. When US presentations occur in the context of extinction but the CS is tested in a different context, reinstatement results from an increased attention to the CS and the combination of CS–CX and CX–US excitatory associations. The assumption that associations between CSs are impaired following neurotoxic hippocampal lesions or in amnesia, is sufficient to describe absence of reinstatement in those cases. However, additional assumptions might be needed to describe the effect of hippocampal lesions on other postextinction manipulations.
Cholinergic modulation of trace conditioning trained in serial compound: A developmental analysis
2006, Neurobiology of Learning and Memory
In four experiments the effects of serial compound conditioning on responding to a trace-conditioned CS were evaluated using a fear conditioning paradigm. The subjects were 18- and 25-day-old Sprague–Dawley rats, previously shown to exhibit little or no trace fear conditioning. Here, animals as young as 18 days of age were shown to be capable of trace conditioning between a visual CS1 and a shock US, provided the trace interval was filled with a non-target CS2 during serial conditioning trials (CS1 → CS2 → US). To explore cholinergic mechanisms involved in trace and serial conditioning, additional experiments assessed conditioned responding following pre-training administration of the muscarinic receptor antagonist scopolamine. Scopolamine produced a dose-dependent reduction in responding to the trace CS1, regardless of whether subjects were trained with standard trace (CS1 → trace interval → US) or serial (CS1 → CS2 → US) trials. Responding to CS2 was unaffected by scopolamine. These data suggest that central cholinergic systems are functional in the young animals, but are not normally sufficiently activated by standard trace conditioning procedures. The results suggest that serial compound conditioning can promote trace conditioning in young rats, as it does in adults, perhaps by enhancing cholinergic activity during training. Implications for the late ontogenetic emergence of trace conditioning as it relates to maturation of neural pathways and their role in the potentiating effects of a gap filler are discussed.

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^☆: The research presented here was supported by the National Institute of Neurological and Communicative Disorders and Stroke Grants NS10647 and NS14545, the American Osteopathic Association Bureau of Research Grant 81-80-023, and the Ohio University College of Osteopathic Medicine. A. L. Beggs is currently at the Psychology Department, University of Southwestern Louisiana.

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Brief communicationHippocampal substrate of sensory associations☆

Abstract

Behav Brain Res

Brain Res

Physiol Behav

Neuropsychologia

Behav Brain Res

Effect of ablating the frontal lobes, hippocampi and occipito-parieto-temporal (excepting pyriform areas) lobes on positive and negative olfactory conditioned reflexes

Am J Physiol

Long-term potentiation of hippocampal synaptic transmission affects rate of behavioral learning

Science

Role of the hippocampus in classical conditioning of appetitive and aversive behaviors

Single unit analysis of different hippocampal cell types during classical conditioning of rabbit nictitating membrane

J Neurophysiol

Prediction of learning rate from the hippocampal electroencephalogram

Science

Acquisition of motor skill after bilateral medial lobe excision

Neuropsychologica

Classical conditioning

Nictitating membrane: Classical conditioning and extinction

Science

Effect of amount of preconditioning training upon the magnitude of sensory preconditioning

J Exp Psychol

Alzheimer's disease: cell specific pathology isolates the hippo campal formation

Science

The effect of radical hippocampal ablation on acquisition of avoidance response

J Comp Physiol Psychol

Effects of hippocampal ablation and intertrial interval on runway acquisition and extinction

J Comp Physiol Psychol

The effects of bilateral hippocampal lesions in rats

J Comp Physiol Psychol

Brief communication
Hippocampal substrate of sensory associations☆