A Behavioral Assessment of Hippocampal Function Based on a Subregional Analysis

Abstract

The purpose of this review is to determine whether specific subregions (dentate gyrus [DG], CA3, and CA1) of the hippocampus provide unique contributions to specific processes associated with intrinsic information processing exemplified by novelty detection, encoding, pattern separation, pattern association, pattern completion, retrieval, short-term memory and intermediate-term memory. Based on anatomical neural network organization, electrophysiology of cellular activity, lesions, early gene activation, and computational modeling, it can be shown that there exists extensive cooperation among the three subregions of the hippocampus, but there also exists reliable specificity of function for each of the subregions of the hippocampus. The primary process supported by the DG subregion of the hippocampus can be characterized by orthogonalization of sensory inputs to create a metric spatial representation. Furthermore the DG participates in conjunction with CA3 in supporting spatial pattern separation. The CA3 subregion of the hippocampus supports processes associated with spatial pattern association, spatial pattern completion, novelty detection, and short-term memory. The CA1 subregion of the hippocampus supports processes associated with temporal pattern association, temporal pattern completion, and intermediate-term memory. Furthermore, the CA3 in conjunction with CA1 supports temporal pattern separation. All the above-mentioned processes are assumed to reflect intrinsic processing of information within the hippocampus. The diversity of functions associated with the different subregions of the hippocampus suggests that one should not treat the hippocampus as a single entity, but rather that one should concentrate on elucidating further the functions of both dorsal and ventral subregions of the hippocampus and pathways that directly connect each of the subregions as well as their connections with the entorhinal cortex.

Dissociating the role of the parietal cortex and dorsal hippocampus for spatial information processing.

“…These results suggest that the dHPC is responsible for metric information processing (Kesner, Lee, & Gilbert, 2004).…”

The role of the direct perforant path input to the CA1 subregion of the dorsal hippocampus in memory retention and retrieval

“…Given the observed selective deficits in retrieval of spatial cues necessary for navigation of a maze and previous evidence implicating CA1 in retrieval (Hasselmo, 1995;Hasselmo et al, 1995;Sybirska et al, 2000;Kesner et al, 2004;Lee and Kesner, 2004b;Jerman et al, 2006;Rolls and Kesner, 2006), we reasoned that similar selective deficits may be apparent in additional CA1-dependent tasks. It has been shown previously that CA3-lesioned rats are significantly impaired on the acquisition, but not retention of contextual fear-conditioning whereas, CA1 lesioned rats are significantly impaired on retention but not acquisition (Lee and Kesner, 2004a).…”

“…Contemporary analysis of hippocampal function has suggested that memory encoding and retrieval require unique computational processes that are independently supported by specific subregions and pathways projecting into this region (O'Reilly and McClelland, 1994;Treves and Rolls, 1994;Moser and Moser, 1998;Kesner et al, 2004;Daumas et al, 2005;Hasselmo, 2005;Rolls and Kesner, 2006). There is strong evidence suggesting the CA1 subregion plays a significant role in intermediate/long-term spatial memory and consolidation, but not short-term acquisition or encoding processes (O'Reilly and McClelland, 1994;Treves and Rolls, 1994;Maren et al, 1997;Bertaina-Anglade et al, 2000;Kesner et al, 2004;Lee and Kesner, 2004a;Remondes and Schuman, 2004;Daumas et al, 2005;Hasselmo, 2005;Sharifzadeh et al, 2006).…”

“…There is strong evidence suggesting the CA1 subregion plays a significant role in intermediate/long-term spatial memory and consolidation, but not short-term acquisition or encoding processes (O'Reilly and McClelland, 1994;Treves and Rolls, 1994;Maren et al, 1997;Bertaina-Anglade et al, 2000;Kesner et al, 2004;Lee and Kesner, 2004a;Remondes and Schuman, 2004;Daumas et al, 2005;Hasselmo, 2005;Sharifzadeh et al, 2006). Encoding of information acquired in a Hebb-Williams maze or in contextual fear conditioning, using a within-days analysis, is impaired by targeted lesions to the CA3 and dentate gyrus (DG) subregions, but not from targeted lesions to the CA1 subregion.…”

Neurobiological foundations of an attribute model of memory

“…Other studies have also shown that order judgments improve as the number of items in a sequence between the test items increases (Banks, 1978;Chiba, Kesner, & Reynolds, 1994;Madsen & Kesner, 1995). This phenomenon is referred to as a temporal distance effect [sometimes referred to as a temporal pattern separation effect (Kesner, Lee, & Gilbert, 2004)]. The temporal distance effect is assumed to occur because there is more interference for temporally proximal events than for temporally distant events.…”