A Critical Role for the Hippocampus and Perirhinal Cortex in Perceptual Learning of Scenes and Faces: Complementary Findings from Amnesia and fMRI

Abstract

It is debated whether subregions within the medial temporal lobe (MTL), in particular the hippocampus (HC) and perirhinal cortex (PrC), play domain-sensitive roles in learning. In the present study, two patients with differing degrees of MTL damage were first exposed to pairs of highly similar scenes, faces, and dot patterns and then asked to make repeated same/different decisions to preexposed and nonexposed (novel) pairs from the three categories (Experiment 1). We measured whether patients would show a benefit of prior exposure (preexposed Ͼ nonexposed) and whether repetition of nonexposed (and preexposed) pairs at test would benefit discrimination accuracy. Although selective HC damage impaired learning of scenes, but not faces and dot patterns, broader MTL damage involving the HC and PrC compromised discrimination learning of scenes and faces but left dot pattern learning unaffected. In Experiment 2, a similar task was run in healthy young participants in the MRI scanner. Functional region-of-interest analyses revealed that posterior HC and posterior parahippocampal gyrus showed greater activity during scene pattern learning, but not face and dot pattern learning, whereas PrC, anterior HC, and posterior fusiform gyrus were recruited during discrimination learning for faces, but not scenes and dot pattern learning. Critically, activity in posterior HC and PrC, but not the other functionalregion-of-interestanalyses,wasmodulatedbyaccuracy(correctϾincorrectwithinapreferredcategory).Therefore,bothapproaches revealedakeyrolefortheHCandPrCindiscriminationlearning,whichisconsistentwithrepresentationalaccountsinwhichsubregionsinthese MTL structures store complex spatial and object representations, respectively.

Evidencing a place for the hippocampus within the core scene processing network

“…We provide, therefore, the first detailed investigation of scene‐sensitivity within a large sample and across a range of regions. While we evaluate the response properties of the “core” scene processing network—namely PHG, RSC, and TOS—a novel aspect of this study was the inclusion of the HC as a component of this network, given its purported role in the representation of complex and conjunctive scenes [Barense et al, 2010; Lee et al, 2008; Mundy et al, 2013] and contributions to scene construction [Maguire and Mullally, 2013; Zeidman et al, 2015]. …”

“…Beyond the seminal work in both rats and non‐human primates—which identified HC cells attuned to allocentric location [O'Keefe and Nadel, 1978] and spatial view [Rolls, 1999]—recent models of human medial temporal lobe (MTL) function highlight the HC as an important structure for scene processing, via a proposed role in representing complex and conjunctive scene stimuli [Graham et al, 2010; Lee et al, 2012; Murray et al, 2007] and/or by contributions to viewpoint‐independent scene construction [Bird and Burgess, 2008; Maguire and Mullally, 2013; Zeidman et al, 2015]. These complex HC scene representations have been shown to support behavioural performance across a range of cognitive domains, including recognition memory [Bird et al, 2008; Taylor et al, 2007], short‐term memory [Hannula et al, 2006; Hartley et al, 2007], working memory [Lee and Rudebeck, 2010a, 2010b; Park et al, 2003], perceptual learning [Mundy et al, 2013], higher‐order perception [Aly et al, 2013; Barense et al, 2005, 2010; Kolarik et al, 2016; Lee et al, 2005b] and scene imagination [Hassabis et al, 2007]. …”

“…An important question, therefore, is whether the HC also responds preferentially and consistently to scenes, as seen in these other “core” scene processing regions. As previous fMRI studies investigating scene perception and memory in the HC have used anatomical or group‐defined regions‐of‐interest (ROIs), rather than functional ROIs defined within individual subjects [Barense et al, 2010; Lee et al, 2008; Mundy et al, 2013], it is currently unclear whether this is the case.…”

A Hippocampal Signature of Perceptual Learning in Object Recognition

“…Seitz et al, 2009), the effect of reward should be limited to trained exemplars, whereas a higher-level mechanism should enhance performance for the whole object category associated with reward. Finally, we hypothesized that category-related learning effects should lead to enhanced responses to trained object categories in the LOC (GrillSpector et al, 2000) or in medial-temporal lobe structures, such as the perirhinal cortex and the hippocampus, that have been implicated in high-level perception (Aly, Ranganath, & Yonelinas, 2013;Mundy, Downing, Dwyer, Honey, & Graham, 2013;Lee, Yeung, & Barense, 2012;Graham, Barense, & Lee, 2010;Lee, Buckley, et al, 2005;Lee, Bussey, et al, 2005).…”

Hyperbaric Oxygen Therapy Alleviates Carbon Monoxide Poisoning–Induced Delayed Memory Impairment by Preserving Brain-Derived Neurotrophic Factor–Dependent Hippocampal Neurogenesis

“…Our data of delayed impairments of both working and reference memory imply the normal hippocampal-prefrontal network for spatial learning and memory might be affected by acute CO poisoning, and early HBO therapy preserves this network. T2-weighted brain MRI of patients with delayed encephalopathy after CO poisoning shows damage to the hippocampus (62,63) and white-matter lesion in the frontal lobe and periventricular area (64,65), indicating the relevance of our animal model of acute CO poisoning to clinical manifestations. Our finding of no significant change in the spatial memory during the subacute phase (i.e., within the first week) after CO poisoning is also comparable with the clinical observations (66).…”