Neural Substrates of Stimulus Recognition and Association Memory

National Institute Of Mental Health

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Abstract

The hippocampus and perirhinal cortex are both broadly implicated in memory; nevertheless, their relative contributions to visual item recognition and location memory remain disputed. Neuropsychological studies that experimentally damage medial temporal lobe structures report various levels of memory impairment, ranging from minor deficits to profound amnesia. The discrepancies in published findings have complicated efforts to determine the magnitude of visual item recognition and location memory impairments that follow damage to the hippocampus and/or perirhinal cortex. To provide the most accurate estimate to date of the overall effect size, we used meta-analytic techniques on data aggregated from 26 publications that assess visual item recognition and/or location memory in animals with and without selective neurotoxic lesions of the hippocampus or perirhinal cortex. We estimated the overall effect size, evaluated the relation between lesion extent and effect size, and investigated factors that may account for between-study variation. Grouping studies by lesion target and testing method, separate meta-analyses were conducted. One meta-analysis indicated that impairments on tests of visual item recognition were larger after lesions of the perirhinal cortex than after lesions of the hippocampus. A separate meta-analysis showed that performance on tests of location memory was severely impaired in subjects with damage to the hippocampus. For the most part, meta-regressions indicated that greater impairment corresponds with greater lesion extent; paradoxically, however, more extensive hippocampal lesions predicted smaller impairments on tests of visual item recognition. We conclude the perirhinal cortex makes a larger contribution than the hippocampus to visual item recognition, and the hippocampus predominately contributes to spatial navigation. Dual-process accounts of item recognition posit two memory processes: slow but detailed recollection, and quick but vague familiarity. It has been proposed, based on prior work in rodents, that the amygdala is critical for the familiarity aspect of item recognition. Here, we evaluated this proposal in animals with selective bilateral excitotoxic amygdala damage. We used four established visual memory tests designed to assess different aspects of familiarity, all administered on touchscreen computers. Specifically, we assessed animals tendencies to make low-latency false alarms, to make false alarms to recently seen lures, to produce curvilinear receiver operating characteristic (ROC) curves, and to discriminate stimuli based on repetition across days. Three of the four tests showed no familiarity impairment and the fourth was explained by a deficit in reward processing. Consistent with this, amygdala damage did produce an anticipated deficit in reward processing in a three-arm-bandit gambling task, verifying the effectiveness of the lesions. Together, these results contradict prior rodent work and suggest that the amygdala is not critical for the familiarity aspect of item recognition.