Novel sensory preconditioning procedures identify a specific role for the hippocampus in pattern completion

Abstract

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.

Conditioning with spatio-temporal patterns: Constraining the contribution of the hippocampus to configural learning

“…According to this analysis, the presentation of the tone during aversive conditioning trials evoked the stored configurations involving the tone (i.e., spotted+morning+tone and checked+afternoon+tone) and these evoked memories become linked to the memory of shock. This analysis is consistent with recent investigations of the conditions under which the hippocampus is involved in sensory preconditioning effects involving audio-visual stimuli (Lin, Dumigan, Good, & Honey, 2016; for a review, see ; see also Wimmer & Shohamy, 2012).…”

“…This behavioral effect that is clearly dependent on the hippocampus (e.g., Iordanova et al, 2009. The involvement of the hippocampus in this behavioral effect could reflect its role in a number of mnemonic processes: configural learning in general (e.g., O'Reilly & Rudy, , co figural learning involving spatio-temporal information (see Aggleton & Pearce, 2001), or mediated learning (or updating) involving evoked configural memories Lin, Dumigan, Good, & Honey, 2016;see also, Lin, Dumigan, Recio, & Honey, 2016). The result of the experiments presented here are inconsistent with accounts which suppose that the hippocampus plays (i) a general role in configural learning, or (ii) a more constrained role in configural learning about spatiotemporal information.…”

“…If the hippocampus is involved in configural learning or specifically configural learning with spatio-temporal stimuli, then lesions to this structure should result in the same pattern of dissociations that was observed by Iordanova et al (2009. However, if the hippocampus is involved in retrieval-mediated learning involving configural memories Lin, Dumigan, Good, & Honey, 2016;see also, Lin, Dumigan, Recio, & Honey, 2016;Schlichting & Preston, 2016;Wimmer & Shohamy, 2012) then direct learning involving the same configurations might not be disrupted by hippocampal lesions. The experimental designs employed to assess these predictions are presented in Figure 1.…”

Mediated configural learning in rats

“…Eight male naive Lister hooded rats (Rattus norvegicus; supplied by Harlan Olac Ltd, UK), with a mean ad libitum weight of 443 g (range: 415-492 g), were used. These rats had received sham surgeries as part of a larger scale study (Experiment 1; Lin et al, 2016). The rats were ≈4 months old at the start of the experiment and were housed in pairs in a colony room that was illuminated between the hours of 8 a.m. and 8 p.m., with food and water available ad libitum throughout the experiment.…”

“…It also included a statistical analysis that allowed the effects of compound familiarity/novelty to be distinguished from those predicted on the basis of a process of mediated learning. The raw results from Experiment 1 are a subset of those reported in a larger scale study that examined the role of the hippocampus in sensory preconditioning effects (Lin, Dumigan, Good, & Honey, 2016). Critically, Experiment 1 involves a secondary analysis that provides critical information about the role of compound novelty.…”