Abstract
During extinction learning (EL), an individual learns that a previously learned behavior no longer fulfills its original purpose, or is no longer relevant. Recent studies have contradicted earlier theories that EL comprises forgetting, or the inhibition of the previously learned behavior, and indicate that EL comprises new associative learning. This suggests that the hippocampus is involved in this process. Empirical evidence is lacking however. Here, we used fluorescence in situ hybridization of somatic immediate early gene (IEG) expression to scrutinize if the hippocampus processes EL. Rodents engaged in context-dependent EL and were also tested for renewal of (the original behavioral response to) a spatial appetitive task in a T-maze. Whereas distal and proximal CA1 subfields processed both EL and renewal, effects in the proximal CA1 were more robust consistent with a role of this subfield in processing context. The lower blade of the dentate gyrus (DG) and the proximal CA3 subfields were particularly involved in renewal. Responses in the distal and proximal CA3 subfields suggest that this hippocampal subregion may also contribute to the evaluation of the reward outcome. Taken together, our findings provide novel and direct evidence for the involvement of distinct hippocampal subfields in context-dependent EL and renewal.
Highlights
A fundamental and indispensable ability of the brain comprises learning of new information and the creation of responses to it, through which stimulus-response associations are formed
Acquisition Successfully Occurs in Animals That Participate in the Appetitive Learning Task, but Control Animals Fail to Learn
When we scrutinized immediate early gene (IEG) expression in the soma of the proximal CA3 region we found that extinction learning triggered a significant elevation of Homer1a expression in the EXP group (n = 7) compared to naïve (N) controls (n = 7; F(2,17) = 8.31, p ≤ 0.01; Figure 4), but effects were not significant when the expression of Homer1a was compared in the EXP and control aleatory reward’’ (CAR) (n = 7) groups (Holm–Sidak, p = 0.057; Figure 4)
Summary
A fundamental and indispensable ability of the brain comprises learning of new information and the creation of responses to it, through which stimulus-response associations are formed. Extinction may be understood as new learning involving new memory formation, in conjunction with the conservation of the original memory trace that is associated with decreased responding in memory tasks (Bouton et al, 2006; Archbold et al, 2010) These two core concepts are not mutually exclusive: part of the original trace might be erased within brain regions, whereas other areas retain and update this information. In line with this possibility, and despite the successful occurrence of extinction learning, spontaneous recovery can occur if the individual is re-exposed, after a delay in time, to the context in which the original experience was learned (André and Manahan-Vaughan, 2015; André et al, 2015a; Packheiser et al, 2019). This renewal of the original learned behavior suggests that the original memory trace is at the very least, partly conserved during extinction: an interpretation that is supported by brain imaging studies in human subjects (Lissek et al, 2013)
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