The Temporal Context Model in Spatial Navigation and Relational Learning: Toward a Common Explanation of Medial Temporal Lobe Function Across Domains.

Abstract

The medial temporal lobe (MTL) has been studied extensively at all levels of analysis, yet its function remains unclear. Theory regarding the cognitive function of the MTL has centered along 3 themes. Different authors have emphasized the role of the MTL in episodic recall, spatial navigation, or relational memory. Starting with the temporal context model (M. W. Howard and M. J. , a distributed memory model that has been applied to benchmark data from episodic recall tasks, the authors propose that the entorhinal cortex supports a gradually changing representation of temporal context and the hippocampus proper enables retrieval of these contextual states. Simulation studies show this hypothesis explains the firing of place cells in the entorhinal cortex and the behavioral effects of hippocampal lesion in relational memory tasks. These results constitute a first step towards a unified computational theory of MTL function that integrates neurophysiological, neuropsychological and cognitive findings.The medial temporal lobe (MTL) is a region that includes the hippocampus proper, the subicular complex and parahippocampal cortical regions, including entorhinal, perirhinal, and parahippocampal/postrhinal cortices. A great deal of data from neuropsychology (e.g. Eichenbaum & Cohen, 2001;Scoville & Milner, 1957;Squire, 1992) and functional imaging (e.g. Fernandez, Effern, Grunwald, et al., 1999;Stern, Corkin, Gonzalez, et al., 1996;Wagner et al., 1998) has converged on the idea that the MTL is important in learning and memory. In order to bridge the gap between cognition and cellular-level physiology, we need a mechanistic, mesoscopic description of MTL computational function. We already have several successful verbally-formulated theories of the cognitive function of the MTL. These are described in turn in the following subsections. This paper will attempt to draw these multiple verbal theories together into a single computational framework that is consistent with known neurophysiological and neuroanatomical data.

Immediate memory for “when, where and what”: Short‐delay retrieval using dynamic naturalistic material

“…More recently, we have seen an expansion of evidence challenging this dissociation [Jonides et al, 2008; Nee et al, 2008; Ranganath and Blumenfeld, 2005]. For example, it has been put forward that different local circuits mediate STM vs. LTM processes within the same cortical area [Gaffan, 2002; Howard et al, 2005]. By these views, the distinction between STM and LTM can be explained through differences in the intraregional neuronal dynamics within the same memory areas [Fuster, 2006, 2009], or through differences in the level of activity within these common memory areas/networks [Jonides et al, 2005; Postle, 2006].…”

Place from time: Reconstructing position from a distributed representation of temporal context

“…Episodic recall depends on an intact medial temporal lobe, a region of the brain that also supports a place code. Howard, Fotedar, Datey, and Hasselmo (2005) demonstrated that the leaky integrator that supports a gradually-changing representation of temporal context in TCM is sufficient to describe properties of cells observed in ventromedial entorhinal cortex during spatial navigation if it is provided with input about the animal's current velocity. This representation of temporal context generates noisy place cells in the open field, unlike the clearly-defined place cells observed in the hippocampus.…”

“…1. The pattern of activity t i may be thought of as a pattern of sustained firing across cells in extrahippocampal MTL regions (Howard et al, 2005;Egorov, Hamam, Fransén, Hasselmo, & Alonso, 2002). The constraint that the length of t i is always equal to 1 means that t i lives on the surface of a hypersphere in a high-dimensional space.…”

“…O' Keefe & Nadel, 1978;Eichenbaum, Dudchenko, Wood, Shapiro, & Tanila, 1999). Recently Howard et al (2005) proposed that the temporal context model (TCM, Howard & Kahana, 2002) could provide a framework in which to describe aspects of both episodic recall and the construction and maintenance of a place code. We will review this work briefly here before presenting new results on the reconstruction of spatial position from a representation of temporal context.…”

“…We will review this work briefly here before presenting new results on the reconstruction of spatial position from a representation of temporal context. TCM (Howard & Kahana, 2002;Howard, 2004; Howard, Wingfield, & Kahana, Revised;Howard et al, 2005) provides a set of equations that describe a distributed representation of temporal context as a vector in a high-dimensional space. This model was developed to describe performance in situations in which a list of words are presented for a memory test.…”