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.

FIGURE 1

Schematic diagram of a single block of (A) different view face oddity; (B) different view scene oddity; (C) different view object oddity; (D) same view face oddity; (E) same view scene oddity; (F) same view object oddity; (G) difficult size oddity; and (H) easy size oddity trials (for illustrative purposes, the correct answer is always the bottom right stimulus). Subjects were told that of the three pictures presented per trial, two depicted the same stimulus, whereas the third picture was of a different stimulus. They were instructed to select the different stimulus. Note that for each oddity trial the three pictures were presented simultaneously, thus minimizing mnemonic demands of the task. All stimuli were trial-unique.

FIGURE 2

Significant viewpoint effects. fMRI signal change relative to size baseline (i.e., difficult size was subtracted from the different view conditions and easy size was subtracted from the same view conditions) in suprathreshold voxels from the perirhinal and hippocampal regions of interest. Signal change for the difficult and easy size conditions is also shown in the inset box for each voxel. Significance is shown for the comparison of different vs. same view within each stimulus type (as indicated by arrows) or the comparison of a given condition relative to size baseline; **P < 0.05 (FWE-corrected), *P < 0.001 (uncorrected). Error bars represent standard error of mean (SEM).

FIGURE 3

Mariginally significant viewpoint effects. fMRI signal change relative to size baseline (i.e., difficult size was subtracted from the different view conditions and easy size was subtracted from the same view conditions) in voxels from the perirhinal and hippocampal regions of interest that survive a threshold of P < 0.001 (uncorrected). Signal change for the difficult and easy size conditions is also shown in the inset box for each voxel. Significance is shown for the comparison of different vs. same view within each stimulus type (as indicated by arrows) or the comparison of a given condition relative to size baseline; **P < 0.05 (FWE-corrected), *P < 0.001 (uncorrected). Error bars represent SEM.

FIGURE 4

Regions of MTL activity in the whole-brain analysis of viewpoint for each of the three a priori contrasts. To show the spatial extent of the activations, these maps were thresholded at P < 0.01 (uncorrected). Statistical are superimposed on the mean structural image for all participants in the present study and the color bar reflects t-values. [Color figure can be viewed in the online issue which is available at www.interscience.wiley.com.]