Medial perirhinal cortex disambiguates confusable objects

Abstract

Our brain disambiguates the objects in our cluttered visual world seemingly effortlessly, enabling us to understand their significance and to act appropriately. The role of anteromedial temporal structures in this process, particularly the perirhinal cortex, is highly controversial. In some accounts, the perirhinal cortex is necessary for differentiating between perceptually and semantically confusable objects. Other models claim that the perirhinal cortex neither disambiguates perceptually confusable objects nor plays a unique role in semantic processing. One major hurdle to resolving this central debate is the fact that brain damage in human patients typically encompasses large portions of the anteromedial temporal lobe, such that the identification of individual substructures and precise neuroanatomical locus of the functional impairments has been difficult. We tested these competing accounts in patients with Alzheimer's disease with varying degrees of atrophy in anteromedial structures, including the perirhinal cortex. To assess the functional contribution of each anteromedial temporal region separately, we used a detailed region of interest approach. From each participant, we obtained magnetic resonance imaging scans and behavioural data from a picture naming task that contrasted naming performance with living and non-living things as a way of manipulating perceptual and semantic confusability; living things are more similar to one another than non-living things, which have more distinctive features. We manually traced neuroanatomical regions of interest on native-space cortical surface reconstructions to obtain mean thickness estimates for the lateral and medial perirhinal cortex and entorhinal cortex. Mean cortical thickness in each region of interest, and hippocampal volume, were submitted to regression analyses predicting naming performance. Importantly, atrophy of the medial perirhinal cortex, but not lateral perirhinal cortex, entorhinal cortex or hippocampus, significantly predicted naming performance on living relative to non-living things. These findings indicate that one specific anteromedial temporal lobe region-the medial perirhinal cortex-is necessary for the disambiguation of perceptually and semantically confusable objects. Taken together, these results support a hierarchical account of object processing, whereby the perirhinal cortex at the apex of the ventral object processing system is required to bind properties of not just perceptually, but also semantically confusable objects together, enabling their disambiguation from other similar objects and thus comprehension. Significantly, this model combining a hierarchical object processing architecture with a semantic feature statistic account explains why category-specific semantic impairments for living things are associated with anteromedial temporal lobe damage, and pinpoints the root of this syndrome to perirhinal cortex damage.

Figure 1

Anatomical border definitions of lateral perirhinal cortex (PRc), medial perirhinal cortex and entorhinal cortex (ERc) in two coronal MRI slices. The anatomical borders are indicated with solid lines perpindicular to the cortical surface. The dashed lines represent the collateral sulcus measurement (Taylor and Probst, 2008). Anatomical borders were adjusted according to the depth of the collateral sulcus, that is, (A) collateral sulcus <1.5 cm or (B) collateral sulcus >1.5 cm (see text for details). CS = collateral sulcus; D = dorsal; FG = fusiform gyrus; HC = hippocampus; ITG = inferior temporal gyrus; L = lateral; M = medial; MTG = middle temporal gyrus; PHG = parahippocampal gyrus; STG = superior temporal gyrus; Un = uncal notch; V = ventral.

Figure 2

The scatterplot represents the relationship between estimated medial perirhinal cortex (PRc) thickness and the domain index for no/mild and moderate global atrophy levels separately (all covariates held at their mean). At no/mild levels of global atrophy, thinner medial perirhinal cortices are associated with worse performance with living than non-living things (grey line). At moderate levels of global atrophy, this relationship reverses, such that thinner medial perirhinal cortices are associated with worse performance with non-living than living things (black line). The dashed line represents equivalent performance in both domains.