Oscillatory Dynamics Supporting Semantic Cognition: MEG Evidence for the Contribution of the Anterior Temporal Lobe Hub and Modality-Specific Spokes

RESEARCH ARTICLE Oscillatory Dynamics Supporting Semantic Cognition: MEG Evidence for the Contribution of the Anterior Temporal Lobe Hub and Modality-Specific Spokes Giovanna Mollo1*, Piers L. Cornelissen2, Rebecca E. Millman3,4, Andrew W. Ellis1, Elizabeth Jefferies1 a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 1 Department of Psychology, University of York, York, United Kingdom, 2 Department of Psychology, School of Life Sciences, Northumbria University, Newcastle upon Tyne, United Kingdom, 3 York Neuroimaging Centre, University of York, York Science Park, York, United Kingdom, 4 Audiology and Deafness Group, School of Psychological Sciences, University of Manchester, Manchester, United Kingdom * Abstract OPEN ACCESS Citation: Mollo G, Cornelissen PL, Millman RE, Ellis AW, Jefferies E (2017) Oscillatory Dynamics Supporting Semantic Cognition: MEG Evidence for the Contribution of the Anterior Temporal Lobe Hub and Modality-Specific Spokes. PLoS ONE 12 (1): e0169269. doi:10.1371/journal.pone.0169269 Editor: Cosimo Urgesi, Universita degli Studi di Udine, ITALY Received: July 4, 2016 Accepted: December 14, 2016 Published: January 11, 2017 Copyright: © 2017 Mollo et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: Data are publicly available in accordance with the Data Protection policy of the York Neuroimaging Centre and University of York at the following link: http:// neurovault.org/collections/1937/. The “hub and spoke model” of semantic representation suggests that the multimodal features of objects are drawn together by an anterior temporal lobe (ATL) “hub”, while modality-specific “spokes” capture perceptual/action features. However, relatively little is known about how these components are recruited through time to support object identification. We used magnetoencephalography to measure neural oscillations within left ATL, lateral fusiform cortex (FC) and central sulcus (CS) during word-picture matching at different levels of specificity (employing superordinate vs. specific labels) for different categories (manmade vs. animal). This allowed us to determine (i) when each site was sensitive to semantic category and (ii) whether this was modulated by task demands. In ATL, there were two phases of response: from around 100 ms post-stimulus there were phasic bursts of low gamma activity resulting in reductions in oscillatory power, relative to a baseline period, that were modulated by both category and specificity; this was followed by more sustained power decreases across frequency bands from 250 ms onwards. In the spokes, initial power increases were not stronger for specific identification, while later power decreases were stronger for specific-level identification in FC for animals and in CS for manmade objects (from around 150 ms and 200 ms, respectively). These data are inconsistent with a temporal sequence in which early sensory-motor activity is followed by later retrieval in ATL. Instead, knowledge emerges from the rapid recruitment of both hub and spokes, with early specificity and category effects in the ATL hub. The balance between these components depends on semantic category and task, with visual cortex playing a greater role in the fine-grained identification of animals and motor cortex contributing to the identification of tools. Funding: The research was supported by BBSRC grant BB/J006963/1. Jefferies was supported by a grant from the European Research Council (SEMBIND - 283530). Competing Interests: The authors have declared that no competing interests exist. PLOS ONE | DOI:10.1371/journal.pone.0169269 January 11, 2017 1 / 25 Oscillatory Dynamics in the Semantic Hub and Spokes Introduction Conceptual processing plays a crucial role in our lives, allowing us to understand the significance of words and objects and to guide our behaviour accordingly [1, 2]. However, the question of how conceptual knowledge is represented and retrieved remains controversial, with different theories and research methods variously suggesting a crucial role for (i) an anterior temporal lobe (ATL) ‘hub’ across categories and modalities [3–5] and (ii) modality-specific perceptual and motor regions of cortex (‘spokes’), reflecting the visual, auditory and action features of the concept being retrieved [6–8]. Since both these components are engaged during conceptual retrieval, it becomes important to consider (i) when hub and spoke regions are engaged following the presentation of a stimulus and (ii) how their recruitment is modulated by task demands–including the type of object to be identified (i.e., animal vs. manmade object) and the level of identification required (i.e., coarse- vs. fine-grained identification). This study uses magnetoencephalography (MEG) to address these questions. The view that knowledge is captured in the links between different motor and sensory representations is supported by a wealth of neuroimaging studies that have shown differential patterns of activation for concepts that draw on different types of features: thinking of a rose produces activation in cortical regions linked to colour and smell processing (alongside other regions), while thinking of a tennis racquet elicits additional areas of activity in regions linked to action and praxis [6, 9– 11]. This principle may underpin category-specific effects in conceptual processing, since visual and motor/praxis features are likely to be important for differentiating animals and manipulable manmade objects respectively [12–14]. Animals are visually complex yet have highly overlapping visual features (e.g., four legs, tails, eyes, ears)–thus specific visual features are important in differentiating one animal concept from another, e.g., the stripes on a zebra distinguish it from a horse [15, 16]. Manmade objects have more diverse visual features at the superordinate level, and thus might not show the same interaction between visual processing and specificity [17–20], instead, when artefacts must be identified as a ‘nut-cracker’ or a ‘knife’, the different actions and grips associated with these objects may be crucial for distinguishing them [17, 21–23]. Following the presentation of words denoting action concepts, activation within motor cortex occurs rapidly (within 150ms): activity of the motor hand area is seen for words such as “pick”, while the leg area shows activation for “kick” [24–26]. Given this rapid activation, links between words and their motor/perceptual referents are likely to play an important role in accessing meanings [7]; however, the recruitment of motor ‘spokes’ is also modulated by their relevance to the task [27–29]. In addition, similarities in any given sensory/motor region do not always predict deeper semantic relationships [1, (...truncated)