Medial temporal lobe activity during complex discrimination of faces, objects, and scenes: Effects of viewpoint

Abstract

The medial temporal lobe (MTL), a set of heavily interconnected structures including the hippocampus and underlying entorhinal, perirhinal and parahippocampal cortex, is traditionally believed to be part of a unitary system dedicated to declarative memory. Recent studies, however, demonstrated perceptual impairments in amnesic individuals with MTL damage, with hippocampal lesions causing scene discrimination deficits, and perirhinal lesions causing object and face discrimination deficits. The degree of impairment on these tasks was influenced by the need to process complex conjunctions of features: discriminations requiring the integration of multiple visual features caused deficits, whereas discriminations that could be solved on the basis of a single feature did not. Here, we address these issues with functional neuroimaging in healthy participants as they performed a version of the oddity discrimination task used previously in patients. Three different types of stimuli (faces, scenes, novel objects) were presented from either identical or different viewpoints. Consistent with studies in patients, we observed increased perirhinal activity when participants distinguished between faces and objects presented from different, compared to identical, viewpoints. The posterior hippocampus, by contrast, showed an effect of viewpoint for both faces and scenes. These findings provide convergent evidence that the MTL is involved in processes beyond long-term declarative memory and suggest a critical role for these structures in integrating complex features of faces, objects, and scenes into view-invariant, abstract representations.

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

“…Unlike several previous studies that have looked at HC responses during scene perception [Barense et al, 2010; Lee et al, 2008; Lee and Rudebeck, 2010b; Mundy et al, 2012; Zeidman et al, 2015], we found stronger group‐level (bilateral) activation in the anterior, rather than posterior, HC (although see Lee et al, 2013). As has been discussed elsewhere, spatial smoothing of EPI data can lead to “blurring” between adjacent anatomical ROIs, such as between PHG and posterior HC [Reber et al, 2002].…”

“…Critically, this one‐back localiser task, which involved rapidly presented scenes with minimal mnemonic demand, yielded strong ( Z  > 7) bilateral activation in the HC bilaterally, supporting a task‐independent role of the HC in complex scene processing [Barense et al, 2010; Lee et al, 2008; Lee and Rudebeck, 2010b]. Unlike several previous studies that have looked at HC responses during scene perception [Barense et al, 2010; Lee et al, 2008; Lee and Rudebeck, 2010b; Mundy et al, 2012; Zeidman et al, 2015], we found stronger group‐level (bilateral) activation in the anterior, rather than posterior, HC (although see Lee et al, 2013).…”

“…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.…”