There has been considerable debate as to whether the hippocampus and perirhinal cortex may subserve both memory and perception. We administered a series of oddity tasks, in which subjects selected the odd stimulus from a visual array, to amnesic patients with either selective hippocampal damage (HC group) or more extensive medial temporal damage, including the perirhinal cortex (MTL group). All patients performed normally when the stimuli could be discriminated using simple visual features, even if faces or complex virtual reality scenes were presented. Both patient groups were, however, severely impaired at scene discrimination when a significant demand was placed on processing spatial information across viewpoint independent representations, while only the MTL group showed a significant deficit in oddity judgments of faces and objects when object viewpoint independent perception was emphasized. These observations provide compelling evidence that the human hippocampus and perirhinal cortex are critical to processes beyond long-term declarative memory and may subserve spatial and object perception, respectively.
Impairments in visual discrimination beyond long-term declarative memory have been found in amnesic individuals, with hippocampal lesions resulting in deficits in scene discrimination and perirhinal cortex damage affecting object discrimination. To complement these findings, the present functional magnetic resonance imaging study found that in healthy participants oddity judgment for novel trial-unique scenes, compared with face or size oddity, was associated with increased posterior hippocampus and parahippocampal cortex activity. In contrast, perirhinal and anterior hippocampus activity was observed during unfamiliar trial-unique face oddity judgment, when contrasted with scene or size oddity tasks. Activity in all of these regions decreased as the stimuli were repeated across trials, reflecting the participants' increasing familiarity with the stimuli. This change was significant in all areas, with the exception of the perirhinal cortex, right anterior hippocampus, and to a lesser extent the left anterior hippocampus during face oddity judgment. One possibility is that the activity in these regions may not reflect entirely episodic memory encoding but, in part, processes beyond the mnemonic domain. Thus, the perirhinal cortex, and possibly anterior hippocampus, may play a more generic role in the discrimination and processing of objects.
Prevailing theory holds that the medial temporal lobe (MTL) subserves declarative memory exclusively, whereas nondeclarative memory is independent of this brain region. Recent studies in patients with amnesia, however, have shown that performance on declarative memory tasks may not always be dependent on a single MTL memory system, instead highlighting the critical role of anatomically distinct structures in processing different stimulus types. In particular, the hippocampus has been implicated in spatial memory, whereas perirhinal cortex seems critical for object memory. To assess whether stimulus type would also be a key dimension in nondeclarative memory, patients with selective hippocampal lesions were tested on simple categorization and perceptual learning of faces and virtual reality scenes. The patients demonstrated preserved categorization and perceptual learning of faces but abnormal performance when the stimuli to be discriminated were virtual reality scenes. These findings imply that stimulus type may be a more critical predictor of performance on memory tasks (declarative and nondeclarative) than previously thought. They also suggest that reports of good nondeclarative memory after MTL damage may, in some cases, simply reflect the use of stimuli that fail to tap the processes dependent on structures in this region, such as spatial processing in the case of the hippocampus.
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