A theory of hippocampal function in memory

Abstract

First, what is computed by the hippocampus is considered. Based on the effects of damage to the hippocampus and neuronal activity recorded in the primate hippocampus, it is suggested that it is involved in associating together information usually originating from different cortical regions, for example, about objects and their place in a spatial environment. The rapid formation of such context-dependent memories i s prototypical of memories of particular events or episodes. Second, a computational theory of how it performs this function, based on neuroanatomical and neurophysiological information about the different neuronal systems contained within the hippocampus, i s described. Key hypotheses are that the CA3 pyramidal cells operate as a single autoassociation network to store new episodic information as it arrives via a number of specialized preprocessing stages from many different association areas of the cerebral cortex, and that the dentate granule cell/mossy fiber system is important particularly during learning to help to produce a new pattern of firing in the CA3 cells for each episode. The computational analysis shows how many memories could be stored in the hippocampus, and how quickly the CA3 autoassociation system would operate during recall. The analysis i s then extended to show how the CA3 system could be used to recall the whole of an episodic memory when only a fragment of it is presented. It is shown how this retrieval within the hippocampus could lead to recall of neuronal activity in association areas of the cerebral neocortex similar to that present during the original episode, via modified synapses in backprojection pathways from fhe hippocampus to the cerebral neocortex. The recalled information in the cerebral neocortex could then by used by the neocortex in the formation of long-term memories and/or in the selection of appropriate actions.

Neurobiological foundations of an attribute model of memory

“…The results showed that rats with DG lesions spent significantly less time exploring the two objects that were displaced relative to controls, indicating that DG lesions impair the detection of metric distance changes. Rats with CA3 or CA1 lesions displayed mild impairments relative to controls, providing empirical validation for the role of DG in spatial pattern separation and support the predictions of computational models (Rolls, 1996;Rolls & Kesner, 2006). Stark, Yassa, and Stark (2010) used an analogous task to that used for rats (Goodrich-Hunsaker et al, 2005) to measure spatial pattern separation based on distance, and in this case angle as well, to test young and healthy aging humans.…”

“…This process is akin to the idea that the hippocampus is involved in orthogonalization of sensory input information (Rolls, 1989), in representational differentiation (Myers, Gluck, & Granger, 1995), and indirectly in the utilization of relationships (Cohen & Eichenbaum, 1993). Rolls' (1996) model proposes that pattern separation is facilitated by sparse connections in the mossy-fiber system, which connects DG granular cells to CA3 pyramidal neurons. Separation of patterns is accomplished based on the low probability that any two CA3 neurons will receive mossy fiber input synapses from a similar subset of DG cells.…”

The hippocampal debate: are we asking the right questions?

“…Detailed explanations of hippocampal roles in both spatial and non-spatial tasks are available [72,173,196,225]. The theories themselves have converged on a basic hippocampal functionality in which hippocampal cellular activity follows from an interaction of external cue representations, internal dead-reckoning (path-integration) representations, and contextual representations, all processed through an intrinsic autoassociator system within the hippocampus [76,108,171,173,177,185].…”

Conjoint Control of Hippocampal Place Cell Firing by Two Visual Stimuli

“…By activation, we mean that the hippocampus proper and especially CA3 becomes an environment-specific autoassociative network (Lisman 1999; Rolls 1996; Mizumori et al 1989). This network is environment specific because discharge is confined to an environment-specific subset of the pyramidal cells—those that are place cells in the environment.…”