No effect of hippocampal lesions on perirhinal cortex-dependent feature-ambiguous visual discriminations

Abstract

Previous studies have shown that perirhinal cortex lesions in monkeys impair visual discriminations with a high degree of "feature ambiguity," a property of visual discriminations that can emerge when features are a part of both rewarded and unrewarded stimuli. The effects of damage to the hippocampus on these perirhinal-dependent feature-ambiguous tasks are, however, unknown. Prominent theories of medial temporal lobe function predict similar effects of perirhinal cortex and hippocampal lesions on cognitive tasks. In contrast, our hypothesis is that perirhinal cortex, and not the hippocampus, is important for nonspatial complex feature-ambiguous discriminations. We sought to distinguish between these competing theories in a straightforward way, by testing rhesus monkeys with hippocampal lesions on the same feature-ambiguous tasks shown previously to depend on perirhinal cortex. It was found that hippocampal lesions had no effects on any of these tasks. The findings support the perceptual-mnemonic/feature conjunction model of perirhinal cortex function, and provide further evidence for heterogeneity of function within the putative medial temporal lobe memory system.

Age-Related Regional Network of Magnetic Resonance Imaging Gray Matter in the Rhesus Macaque

“…Both the DR and DNMS tasks involve memory functions that have been associated with age effects in rhesus monkeys (Rapp and Amaral, 1989;Rapp and Gallagher, 1997;Shamy et al, 2006). Whereas the DR task has been mainly associated with frontal lobe mediated working memory processing, the DNMS task involves aspects of recognition memory and has been shown to be specifically impaired with selective lesions in the perirhinal cortex (Buffalo et al, 2000;Saksida et al, 2006). Our findings suggest that individual differences in the expression of the age-related gray matter pattern are strongly related to differences in DR task performance.…”

“…The DR task assesses working memory performance over varying delay intervals, thought to primarily depend on frontal brain functions and rhesus monkeys have previously shown age-related reductions in this task (O'Donnell et al, 1999). The DNMS task assesses aspects of recognition memory for rule-based learning that has been associated with reduced performance because of lesions localized to the temporal lobe, as well as in relation to aging effects (Moss et al, 1988;Rapp and Amaral, 1989;Herndon et al, 1997;Buffalo et al, 2000;Saksida et al, 2006). …”

A novel touchscreen-automated paired-associate learning (PAL) task sensitive to pharmacological manipulation of the hippocampus: a translational rodent model of cognitive impairments in neurodegenerative disease

“…In light of the requirement to associate an object with a spatial location, it is not surprising that in humans PAL has been found to be dependent upon the medial temporal lobe (Owen et al 1995). Based on an evolving body of literature in the rat and monkey, it might be expected that the hippocampus and entorhinal cortex may contribute to the spatial component (Burgess 2008;Gaffan 1977;O'Keefe et al 1975;Owen and Butler 1981;Parron et al 2004), whereas the perirhinal and perhaps entorhinal cortex would contribute to the object component of the task (Meunier et al 1993;Murray et al 2007;Saksida et al 2006;Winters et al 2004). It is likely that this dependency on multiple brain regions, all of which show pathologies very early in the progression of AD, makes PAL so predictive of who will eventually develop the disorder.…”

Invited Address at the Occasion of the Bertelson Award 2005 Impairments in visual discrimination in amnesia: Implications for theories of the role of medial temporal lobe regions in human memory

“…with selective hippocampal damage showed no impairment in any of the four conditions, even at the highest level of feature ambiguity (maximum condition) or on especially difficult discriminations, a finding that has now been replicated in monkeys with selective hippocampal damage using the original monkey stimuli (see Saksida et al, 2006). By contrast, patients with broader lesions including perirhinal cortex were impaired, but only when feature ambiguity was stressed (e.g., in the intermediate and maximum ambiguity conditions).…”

“…Although this paradigm required learning, deficits were particularly evident when the numbers of foils was high and there was greater spatial ambiguity between features, a finding consistent with the possibility that the hippocampus is processing spatial conjunctions. Notably, despite these impairments on tasks that result in the need to process multiple spatial features, monkeys with hippocampal lesions do not show the poor performance on feature ambiguous object discriminations, contrary to the pattern seen after perirhinal damage (Saksida, Bussey, Buckmaster, & Murray, 2006). A key outstanding question, however, is whether these findings*thus far only described in animal studies*can be extended to human amnesic patients, in whom perception is typically reported to be normal.…”