The perirhinal cortex and conceptual processing: Effects of feature-based statistics following damage to the anterior temporal lobes.
ABSTRACT: The anterior temporal lobe (ATL) plays a prominent role in models of semantic knowledge, although it remains unclear how the specific subregions within the ATL contribute to semantic memory. Patients with neurodegenerative diseases, like semantic dementia, have widespread damage to the ATL thus making inferences about the relationship between anatomy and cognition problematic. Here we take a detailed anatomical approach to ask which substructures within the ATL contribute to conceptual processing, with the prediction that the perirhinal cortex (PRc) will play a critical role for concepts that are more semantically confusable. We tested two patient groups, those with and without damage to the PRc, across two behavioural experiments - picture naming and word-picture matching. For both tasks, we manipulated the degree of semantic confusability of the concepts. By contrasting the performance of the two groups, along with healthy controls, we show that damage to the PRc results in worse performance in processing concepts with higher semantic confusability across both experiments. Further by correlating the degree of damage across anatomically defined regions of interest with performance, we find that PRc damage is related to performance for concepts with increased semantic confusability. Our results show that the PRc supports a necessary and crucial neurocognitve function that enables fine-grained conceptual processes to take place through the resolution of semantic confusability.
Project description: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.
Project description:The anterior temporal lobe (ATL) is considered a crucial area for the representation of transmodal concepts. Recent evidence suggests that specific regions within the ATL support the representation of individual object concepts, as shown by studies combining multivariate analysis methods and explicit measures of semantic knowledge. This research looks to further our understanding by probing conceptual representations at a spatially and temporally resolved neural scale. Representational similarity analysis was applied to human intracranial recordings from anatomically defined lateral to medial ATL sub-regions. Neural similarity patterns were tested against semantic similarity measures, where semantic similarity was defined by a hybrid corpus-based and feature-based approach. Analyses show that the perirhinal cortex, in the medial ATL, significantly related to semantic effects around 200 to 400 ms, and were greater than more lateral ATL regions. Further, semantic effects were present in low frequency (theta and alpha) oscillatory phase signals. These results provide converging support that more medial regions of the ATL support the representation of basic-level visual object concepts within the first 400 ms, and provide a bridge between prior fMRI and MEG work by offering detailed evidence for the presence of conceptual representations within the ATL.
Project description:Two distinct literatures have emerged on the functionality of the anterior temporal lobes (ATL): in one field, the ATLs are conceived of as a repository for semantic or conceptual knowledge. In another field, the ATLs are thought to play some undetermined role in social-emotional functions such as Theory of Mind. Here we attempted to reconcile these distinct functions by assessing whether social semantic processing can explain ATL activation in other social cognitive tasks. Social semantic functions refer to knowledge about social concepts and rules. In a first experiment we tested the idea that social semantic representations can account for activations in the ATL to social attribution stimuli such as Heider and Simmel animations. Left ATL activations to Heider and Simmel stimuli overlapped with activations to social words. In a second experiment we assessed the putative roles of the ATLs in the processing of narratives and theory of mind content and found evidence for a role of the ATLs in the processing of theory of mind but not narrative per se. These findings indicate that the ATLs are part of a neuronal network supporting social cognition and that they are engaged when tasks demand access to social conceptual knowledge.
Project description:The ability to represent concepts and the relationships between them is critical to human cognition. How does the brain code relationships between items that share basic conceptual properties (e.g., dog and wolf) while simultaneously representing associative links between dissimilar items that co-occur in particular contexts (e.g., dog and bone)? To clarify the neural bases of these semantic components in neurologically intact participants, both types of semantic relationship were investigated in an fMRI study optimized for anterior temporal lobe (ATL) coverage. The clear principal finding was that the same core semantic network (ATL, superior temporal sulcus, ventral prefrontal cortex) was equivalently engaged when participants made semantic judgments on the basis of association or conceptual similarity. Direct comparisons revealed small, weaker differences for conceptual similarity > associative decisions (e.g., inferior prefrontal cortex) and associative > conceptual similarity (e.g., ventral parietal cortex) which appear to reflect graded differences in task difficulty. Indeed, once reaction time was entered as a covariate into the analysis, no associative versus category differences remained. The paper concludes with a discussion of how categorical/feature-based and associative relationships might be represented within a single, unified semantic system.
Project description:Semantic cognition is underpinned by regions involved in representing conceptual knowledge and executive control areas that provide regulation of this information according to current task requirements. Using distortion-corrected fMRI, we investigated the contributions of these two systems to abstract and concrete word comprehension. We contrasted semantic decisions made either with coherent contextual support, which encouraged retrieval of a rich conceptual representation, or with irrelevant contextual information, which instead maximised demands on control processes. Inferior prefrontal cortex was activated more when decisions were made in the presence of irrelevant context, suggesting that this region is crucial for the semantic control functions required to select appropriate aspects of meaning in the face of competing information. It also exhibited greater activation for abstract words, which reflects the fact that abstract words tend to have variable, context-dependent meanings that place higher demands on control processes. In contrast, anterior temporal regions (ATL) were most active when decisions were made with the benefit of a coherent context, suggesting a representational role. There was a graded shift in concreteness effects in this region, with dorsolateral areas particularly active for abstract words and ventromedial areas preferentially activated by concrete words. This supports the idea that concrete concepts are closely associated with visual experience and abstract concepts with auditory-verbal information; and that sub-regions of the ATL display graded specialisation for these two types of knowledge. Between these two extremes, we identified significant activations for both word types in ventrolateral ATL. This area is known to be involved in representing knowledge for concrete concepts; here we established that it is also activated by abstract concepts. These results converge with data from rTMS and neuropsychological investigations in demonstrating that representational content and task demands influence recruitment of different areas in the semantic network.
Project description:One critical feature of any well-engineered system is its resilience to perturbation and minor damage. The purpose of the current study was to investigate how resilience is achieved in higher cognitive systems, which we explored through the domain of semantic cognition. Convergent evidence implicates the bilateral anterior temporal lobes (ATLs) as a conceptual knowledge hub. While bilateral damage to this region produces profound semantic impairment, unilateral atrophy/resection or transient perturbation has a limited effect. Two neural mechanisms might underpin this resilience to unilateral ATL damage: 1) the undamaged ATL upregulates its activation in order to compensate; and/or 2) prefrontal regions involved in control of semantic retrieval upregulate to compensate for the impoverished semantic representations that follow from ATL damage. To test these possibilities, 34 postsurgical temporal lobe epilepsy patients and 20 age-matched controls were scanned whilst completing semantic tasks. Pictorial tasks, which produced bilateral frontal and temporal activation, showed few activation differences between patients and control participants. Written word tasks, however, produced a left-lateralized activation pattern and greater differences between the groups. Patients with right ATL resection increased activation in left inferior frontal gyrus (IFG). Patients with left ATL resection upregulated both the right ATL and right IFG. Consistent with recent computational models, these results indicate that 1) written word semantic processing in patients with ATL resection is supported by upregulation of semantic knowledge and control regions, principally in the undamaged hemisphere, and 2) pictorial semantic processing is less affected, presumably because it draws on a more bilateral network.
Project description:Inappropriate social behaviours are early and distinctive symptoms of the temporal and frontal variants of frontotemporal lobar degeneration (FTLD). Knowledge of social behaviour is essential for appropriate social conduct. It is unknown, however, in what way this knowledge is degraded in FTLD. In a recent functional MRI study, we have identified a right-lateralized superior anterior temporal lobe (aTL) region showing selective activation for 'social concepts' (i.e. concepts describing social behaviour: e.g. 'polite', 'stingy') as compared with concepts describing less socially relevant animal behaviour ('animal function concepts': e.g. 'trainable', 'nutritious'). In a further fMRI study, superior aTL activation was independent of the context of actions and feelings associated with these social concepts. Here, we investigated whether the right superior sector of the aTL is necessary for context-independent knowledge of social concepts. We assessed neuronal glucose uptake using 18-fluoro-deoxy-glucose-positron emission tomography (FDG-PET) and a novel semantic discrimination task which probed knowledge of social and animal function concepts in patients with FTLD (n = 29) and corticobasal syndrome (n = 18). FTLD and corticobasal syndrome groups performed equally poorly on animal function concepts but FTLD patients showed more pronounced impairments on social concepts than corticobasal syndrome patients. FTLD patients with right superior aTL hypometabolism, as determined on individual ROI analyses, were significantly more impaired on social concepts than on animal function concepts. FTLD patients with selective impairments for social concepts, as determined on individual neuropsychological profiles, showed higher levels of inappropriate social behaviours ('disinhibition') and demonstrated more pronounced hypometabolism in the right superior aTL, the left temporal pole and the right lateral orbitofrontal and dorsomedial prefrontal cortex as compared with FTLD patients showing selective impairments of animal function concepts. Combining both FTLD subgroup analyses, based on anatomical and neuropsychological criteria, by using inclusive masks, revealed the right superior aTL as associated with selective impairments of social concepts in both analyses. These results corroborate the hypothesis that the right aTL is necessary for representing conceptual social knowledge. Further, we provide first evidence for the potential importance of conceptual social knowledge impairments as contributing to behavioural symptoms of FTLD.
Project description:Although it is well established that regions in the medial temporal lobes are critical for explicit memory, recent work has suggested that one medial temporal lobe subregion--the perirhinal cortex (PRC)--may also support conceptual priming, a form of implicit memory. Here, we sought to investigate whether activity reductions in PRC, previously linked to familiarity-based recognition, might also support conceptual implicit memory retrieval. Using a free association priming task, the current study tested the prediction that PRC indexes conceptual priming independent of contributions from perceptual and response repetition. Participants first completed an incidental semantic encoding task outside of the MRI scanner. Next, they were scanned during performance of a free association priming task, followed by a recognition memory test. Results indicated successful conceptual priming was associated with decreased PRC activity, and that an overlapping region within the PRC also exhibited activity reductions that covaried with familiarity during the recognition memory test. Our results demonstrate that the PRC contributes to both conceptual priming and familiarity-based recognition, which may reflect a common role of this region in implicit and explicit memory retrieval.
Project description:Retrieval of semantic representations is a central process during overt speech production. There is an increasing consensus that an amodal semantic 'hub' must exist that draws together modality-specific representations of concepts. Based on the distribution of atrophy and the behavioral deficit of patients with the semantic variant of fronto-temporal lobar degeneration, it has been proposed that this hub is localized within both anterior temporal lobes (ATL), and is functionally connected with verbal 'output' systems via the left ATL. An alternative view, dating from Geschwind's proposal in 1965, is that the angular gyrus (AG) is central to object-based semantic representations. In this fMRI study we examined the connectivity of the left ATL and parietal lobe (PL) with whole brain networks known to be activated during overt picture description. We decomposed each of these two brain volumes into 15 regions of interest (ROIs), using independent component analysis. A dual regression analysis was used to establish the connectivity of each ROI with whole brain-networks. An ROI within the left anterior superior temporal sulcus (antSTS) was functionally connected to other parts of the left ATL, including anterior ventromedial left temporal cortex (partially attenuated by signal loss due to susceptibility artifact), a large left dorsolateral prefrontal region (including 'classic' Broca's area), extensive bilateral sensory-motor cortices, and the length of both superior temporal gyri. The time-course of this functionally connected network was associated with picture description but not with non-semantic baseline tasks. This system has the distribution expected for the production of overt speech with appropriate semantic content, and the auditory monitoring of the overt speech output. In contrast, the only left PL ROI that showed connectivity with brain systems most strongly activated by the picture-description task, was in the superior parietal lobe (supPL). This region showed connectivity with predominantly posterior cortical regions required for the visual processing of the pictorial stimuli, with additional connectivity to the dorsal left AG and a small component of the left inferior frontal gyrus. None of the other PL ROIs that included part of the left AG were activated by Speech alone. The best interpretation of these results is that the left antSTS connects the proposed semantic hub (specifically localized to ventral anterior temporal cortex based on clinical neuropsychological studies) to posterior frontal regions and sensory-motor cortices responsible for the overt production of speech.
Project description:The semantic variant of primary progressive aphasia (PPA-S) is diagnosed based on impaired single-word comprehension, but nonverbal impairments in face and object recognition can also be present, particularly in later disease stages. PPA-S is associated with focal atrophy in the left anterior temporal lobe (ATL), often accompanied by a lesser degree of atrophy in the right ATL. According to a dual-route account, the left ATL is critical for verbal access to conceptual knowledge while nonverbal access to conceptual knowledge depends upon the integrity of right ATL. Consistent with this view, single-word comprehension deficits in PPA-S have consistently been linked to the degree of atrophy in left ATL. In the current study we examined object processing and cortical thickness in 19 patients diagnosed with PPA-S, to evaluate the hypothesis that nonverbal object impairments would instead be determined by the amount of atrophy in the right ATL. All patients demonstrated inability to access conceptual knowledge on standardized tests with word stimuli: they were unable to match spoken words with their corresponding pictures on the Peabody Picture Vocabulary Test. Only a minority of patients, however, performed abnormally on an experimental thematic verification task, which requires judgments as to whether pairs of object pictures are thematically-associated, and does not rely on auditory or visual word input. The entire PPA-S group showed cortical thinning in left ATL, but atrophy in right ATL was more prominent in the subgroup with low verification scores. Thematic verification scores were correlated with cortical thickness in the right rather than left ATL, an asymmetric mapping which persisted when controlling for the degree of atrophy in the contralateral hemisphere. These results are consistent with a dual-route account of conceptual knowledge: breakdown of the verbal left hemispheric route produces an aphasic syndrome, which is only accompanied by visual object processing impairments when the nonverbal right hemispheric route is also compromised.