Why trace and delay conditioning are sometimes (but not always) hippocampal dependent: A computational model

Abstract

A recurrent-network model provides a unified account of the hippocampal region in mediating the representation of temporal information in classical eyeblink conditioning. Much empirical research is consistent with a general conclusion that delay conditioning (in which the conditioned stimulus CS and unconditioned stimulus US overlap and co-terminate) is independent of the hippocampal system, while trace conditioning (in which the CS terminates before US onset) depends on the hippocampus. However, recent studies show that, under some circumstances, delay conditioning can be hippocampal-dependent and trace conditioning can be spared following hippocampal lesion. Here, we present an extension of our prior trial-level models of hippocampal function and stimulus representation that can explain these findings within a unified framework. Specifically, the current model includes adaptive recurrent collateral connections that aid in the representation of intra-trial temporal information. With this model, as in our prior models, we argue that the hippocampus is not specialized for conditioned response timing, but rather is a general-purpose system that learns to predict the next state of all stimuli given the current state of variables encoded by activity in recurrent collaterals. As such, the model correctly predicts that hippocampal involvement in classical conditioning should be critical not only when there is an intervening trace interval, but also when there is a long delay between CS onset and US onset. Our model simulates empirical data from many variants of classical conditioning, including delay and trace paradigms in which the length of the CS, the inter-stimulus interval, or the trace interval is varied. Finally, we discuss model limitations, future directions, and several novel empirical predictions of this temporal processing model of hippocampal function and learning.

The role of working memory and declarative memory in trace conditioning

“…That is to say, by maintaining sustained activation during the trace interval, the PFC may support trace conditioning via working memory-like processes across the trace interval. These findings contrast with some theoretical accounts that suggest the hippocampus maintains a representation of the CS via recurrent loops during trace conditioning (Moustafa et al, 2013; Rodriguez & Levy, 2001). Interestingly, the mPFC, (PL and IL) is directly innervated by neurons originating in the VH (Hoover & Vertes, 2007) and these projections appear to be involved in modulating hippocampal-PFC theta coupling during working memory (O’Neill, Gordon, & Sigurdsson, 2013).…”

Bridging the interval: Theory and neurobiology of trace conditioning

“…Studies have shown that lesions to the hippocampus disrupt trace fear learning (Bangasser et al, 2006; Burman et al , 2006; McEchron et al , 1998). Of note is a computational model accounting for hippocampal involvement in some forms of conditioning (Moustafa et al , 2013), although this model primarily accounts for the emergence of trace-cued responses over many more trials than those used in fear conditioning. The roles of different hippocampal subregions in this task are less clear with reports of conflicting roles for dorsal and ventral poles of the hippocampus (Cox et al, 2013; Czerniawski et al , 2009; Czerniawski et al , 2012; Esclassan et al , 2009b; Trivedi & Coover, 2006; Yoon & Otto, 2007).…”

Training on an Appetitive Trace-Conditioning Task Increases Adult Hippocampal Neurogenesis and the Expression of Arc, Erk and CREB Proteins in the Dorsal Hippocampus

“…Various reports have demonstrated the role of the hippocampus in the formation of the temporal association between the CS and US in trace memory (Christian and Thompson, 2003). On the other hand, the CS-US association forms outside the hippocampus in delayappetitive-conditioning (Wallenstein et al, 1998;Rodriguez and Levy, 2001;Bangasser et al, 2006;Woodruff-Pak and Disterhoft, 2008;Moustafa et al, 2013). It has also been reported that only hippocampus-dependent tasks potentiate the neuronal proliferation and/or survival in the DG (Döbrössy et al, 2003;Deng et al, 2009Deng et al, , 2010.…”