Memory for spatial locations, motor responses, and objects: triple dissociation among the hippocampus, caudate nucleus, and extrastriate visual cortex

Abstract

Based on behavioral procedures aimed at measuring working or data-based memory for spatial location, response, and visual object information, it is shown that there is a triple dissociation among the hippocampus, caudate nucleus, and extrastriate visual cortex in mediating spatial location, response, and visual object information, respectively. The hippocampus appears to subserve only spatial location, the caudate nucleus only response, and the extrastriate visual cortex only visual object information. The results support the neurobiological foundation of the attribute memory model.

Neurobiological foundations of an attribute model of memory

“…Based on a subregional analysis of hippocampal function, it can be shown that the dorsal CA1 supports object-trace odor paired associate learning , but both the dorsal CA1 and CA3 support object trace-place paired associate learning and the ventral CA1 supports trace fear conditioning (Rogers et al, 2006). It should be noted that the hippocampus is not directly involved in representing memory information concerning specific objects (Bussey, Saksida, & Murray, 2002;Kesner, Bolland, & Dakis, 1993;Mumby & Pinel, 1994;Norman & Eacott, 2004).…”

“…With respect to response attribute information, it can be shown that with the use of the above mentioned paradigms to measure short-term memory, that for rats with caudateputamen lesions and humans with caudate-putamen damage due to Huntington's disease (HD), there are profound deficits for a right or left turn response or a list of hand motor movement responses (Cook & Kesner, 1988;Davis, Filoteo, Kesner, & Roberts, 2003;Kesner et al, 1993; Figure 3 depicts the location of the caudate nucleus in the rat). For example, it has been shown that electrolytic induced caudate lesions in rats impair short-term or working memory for a specific motor response (right-left turn) without any impairments in memory for a visual object or for a spatial location .…”

“…Figure 4 depicts the location of the perirhinal cortex in the rat. It can be shown that with the use of the above mentioned paradigms to measure short-term memory, that there are severe impairments in visual object information for rats and monkeys with extra-striate or perirhinal cortex lesions (Bussey et al, 2002;Gaffan & Murray, 1992;Horel, Pytko-Joiner, Boytko, & Salsbury, 1987;Kesner et al, 1993;Mumby & Pinel, 1994;Norman & Eacott, 2004;Suzuki, Zola-Morgan, Squire, & Amaral, 1993), suggesting that the extra-striate and perirhinal cortex play an important role in short-term memory representation for visual object information as an exemplar of the sensory-perceptual attribute. Further support derives from single unit studies in rats and monkeys which indicate that activity of neurons in the rhinal cortex reflect stimulus repetition which is an integral part of the delayed non-matching to sample tasks used to measure short-term recognition memory for objects (Zhu, Brown, & Aggleton, 1995).…”

“…Based on the empirical findings that all sensory inputs are processed by the DG subregion of the hippocampus ( (Aggleton, Hunt, & Rawlins, 1986;Jackson-Smith et al, 1993;Kesner et al, 1993;Mumby, Wood, & Pinel, 1992;Otto & Eichenbaum, 1992), it has been suggested that a possible role for the hippocampus might be to provide for sensory markers to demarcate a spatial location, so that the hippocampus can more efficiently mediate spatial information. It is thus possible that one of the main process functions of the hippocampus is to encode and separate spatial events from each other.…”

The hippocampal debate: are we asking the right questions?

“…This can be explained by postulating multiple navigation systems [88,105,150,159,173], some of which require the hippocampus, some of which do not. Those that do include navigation tasks that require the recall of a context, or a context-switch [173].…”