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Binney, R. J.

Publications and source records attributed to Binney, R. J..

8 recordsLinked to original sources

Social Experience and Motivated Cognition Shape the Representation of Concepts: A Behavioural and Functional Neuroimaging Study

The ventrolateral anterior temporal lobe (vlATL), including the anterior inferior temporal and fusiform gyri, is the centre of a supramodal and category-general hub for semantic representation. Dorsolateral ATL regions, such as the temporal pole (TP) and anterior middle temporal gyrus (aMTG), have been associated with more specialised semantic function, including social concept processing, although the precise location and laterality of these effects vary across studies, prohibiting firm conclusions. The socialness of concepts has been defined in numerous different ways which, along with uncontrolled effects of other semantic dimensions, could explain inconsistencies in previous behavioural and neuroimaging findings. Therefore, we used a new set of validated socialness norms to compare social and non-social concept processing, while controlling for other important semantic variables, including concreteness and valence. Moreover, we report the first investigation of a potential link between socialness and motivation. This was aimed at unpacking the informational content or processes that make social concepts unique, and particularly a putative role of reward processing. We report two pre-registered experiments, one behavioural (N = 89) and one using fMRI (N = 30), examining the orthogonal effects of socialness and motivation on semantic decisions. Consistent with other recent findings, social concepts were processed more accurately than non-social concepts. Left TP activation was driven by social concepts but not non-social concepts, and some evidence suggests there is also right TP selectivity for social concepts. All concept types engaged the left vlATL and bilateral aMTG suggestive of a category-general semantic function. Multivariate pattern analyses found distinguishable local activation patterns associated with social vs non-social concepts in the left TP, aMTG, and vlATL, and for high vs low motivation concepts in the left TP and aMTG. The activation patterns encoding socialness in the aMTG generalized across levels of motivation, suggesting that socialness is encoded independently of motivation-related information. These findings align with multiple representation theories that claim social and reward-related experiences contribute to semantic representation. They also particularly pinpoint the left TP as having a preference for social concepts.

neuroscience↗

Subclinical anxiety is associated with reduced self-distancing and enhanced guilt-related connectivity between anterior temporal and subgenual cingulate cortices

Excessive self-blaming emotions are commonly observed in anxiety disorders, with qualitatively similar symptomatology reported in subclinical populations. Interpretation of moral information requires assessing the social conceptual information, a process overseen by the superior anterior temporal lobe (sATL). Feelings of self-blame evoke interactions of sATL and socio-affective regions, and previous research shows that subclinical anxiety modulates the organisation of the self-blame circuitry. This study aimed to extend these findings by exploring links of trait-anxiety with (i) self-blaming emotions and associated behaviours in an experimental task, and (ii) self-blame-dependent neural activity and connectivity, as observed during reliving of autobiographical guilt memories. We also explored the role of resting-state fMRI in linking these phenomena. Increased anxiety was linked to stronger self-blaming emotions, and more pronounced self-attacking and hiding. When experiencing negative emotions about themselves (i.e. shame and self-anger), anxious individuals were also less likely to disengage from self-focused thoughts. These behavioural findings were paralleled by enhanced self-blame-related connectivity between the left sATL and bilateral posterior subgenual cingulate cortex. Distinct patterns of activity and connectivity within the ATL-related circuitry were furthermore linked to individual differences in intensity of the self-blaming emotions and approach-avoidance motivation towards the guilt memories. As such, the results of the current study link stronger self-blaming emotions in anxious individuals with specific maladaptive patterns of behaviour. Furthermore, the work provides robust evidence for the important role of ATL-related circuitry in self-blame processing, supporting its broader involvement in social conceptual processing and its alterations in subclinical anxiety.

neuroscience↗

Mapping Contributions of the Anterior Temporal Semantic Hub to the Processing of Abstract and Concrete Verbs

Multiple representation theories of semantic processing propose that word meaning is supported by simulated sensorimotor experience in modality-specific neural regions, as well as in cognitive systems that involve processing of linguistic, emotional, and introspective information. According to the Hub and Spoke Model of Semantic Memory, activity from these distributed cortical areas feeds into a primary semantic hub located in the ventral anterior temporal lobe (vATL). Though a substantial amount of research has tested this model in terms of concrete noun representation, there is less known about how this model can account for the representation of verb meaning, and in particular the meaning of abstract verbs which convey important information, for example, about socioemotional dynamics. In the present pre-registered study, we examined whether different types of abstract verbs (mental, emotional, nonembodied) and concrete (embodied) verbs all engage the vATL, and also whether they differentially recruit a broader set of distributed neurocognitive systems (consistent with multiple representation theories). Finally, we investigated whether there is information about different verb types distributed across the broader ATL region, consistent with a Graded Semantic Hub Hypothesis. We collected data from 30 participants who completed a syntactic classification task (is it a verb? Yes or no) and a numerical judgement task which served as an active but less semantic baseline task. Whole brain univariate analyses revealed consistent BOLD signal throughout the canonical semantic network, including the left inferior frontal gyrus, left middle temporal gyrus, and the vATL. All types of abstract verbs engaged the vATL except for mental state verbs. Finally, a multivariate pattern analysis revealed clusters within the ATL that were differentially engaged when processing each type of abstract verb. Our findings extend previous research and suggest that the hub-and-spoke hypothesis and the graded semantic hub hypothesis provide a neurobiologically constrained model of semantics that can account for abstract verb representation and processing.

neuroscience↗

Overlapping Neural Correlates Underpin Theory of Mind and Semantic Cognition: Evidence from a Meta-Analysis of 344 Functional Neuroimaging Studies

Key unanswered questions for cognitive neuroscience include whether social cognition is underpinned by specialised brain regions and to what extent it simultaneously depends on more domain-general systems. Until we glean a better understanding of the full set of contributions made by various systems, theories of social cognition will remain fundamentally limited. In the present study, we evaluate a recent proposal that semantic cognition plays a crucial role in supporting social cognition. While previous brain-based investigations have focused on dissociating these two systems, our primary aim was to assess the degree to which the neural correlates are overlapping, particularly within two key regions, the anterior temporal lobe (ATL) and the temporoparietal junction (TPJ). We focus on activation associated with theory of mind (ToM) and adopt a meta-analytic activation likelihood approach to synthesise a large set of functional neuroimaging studies and compare their results with studies of semantic cognition. As a key consideration, we sought to account for methodological differences across the two sets of studies, including the fact that ToM studies tend to use nonverbal stimuli while the semantics literature is dominated by language-based tasks. Overall, we observed consistent overlap between the two sets of brain regions, especially in the ATL and TPJ. This supports the claim that tasks involving ToM draw upon more general semantic retrieval processes. We also identified activation specific to ToM in the right TPJ, bilateral anterior mPFC, and right precuneus. This is consistent with the view that, nested amongst more domain-general systems, there is specialised circuitry that is tuned to social processes.

neuroscience↗

Graded functional organisation in the left inferior frontal gyrus: evidence from task-free and task-based functional connectivity

The left inferior frontal gyrus (LIFG) has been ascribed key roles in numerous cognitive domains, including language, executive function and social cognition. However, its functional organisation, and how the specific areas implicated in these cognitive domains relate to each other, is unclear. Possibilities include that the LIFG underpins a domain-general function or, alternatively, that it is characterized by functional differentiation, which might occur in either a discrete or a graded pattern. The aim of the present study was to explore the topographical organisation of the LIFG using a bimodal data-driven approach. To this end, we extracted functional connectivity (FC) gradients from 1) the resting-state fMRI time-series of 150 participants (77 female), and 2) patterns of co-activation derived meta-analytically from task data across a diverse set of cognitive domains. We then sought to characterize the FC differences driving these gradients with seed-based resting-state FC and meta-analytic co-activation modelling analyses. Both analytic approaches converged on an FC profile that shifted in a graded fashion along two main organisational axes. An anterior-posterior gradient shifted from being preferentially associated with high-level control networks (anterior LIFG) to being more tightly coupled with perceptually-driven networks (posterior). A second dorsal-ventral axis was characterized by higher connectivity with domain-general control networks on one hand (dorsal LIFG), and with the semantic network, on the other (ventral). These results provide novel insights into a graded functional organisation of the LIFG underpinning both task-free and task-constrained mental states, and suggest that the LIFG is an interface between distinct large-scale functional networks. Significance statementTo understand how function varies across the LIFG, we conducted a detailed, bimodal exploration of the spatial transitions in its voxel-wise FC patterns. We provide novel evidence of graded changes along two main organisational axes. Specifically, the LIFG was characterized by an anterior-posterior gradient, which could reflect a shift in function from perceptually-driven processing to task-oriented control processes. Moreover, we revealed a dorsal-ventral shift in FC that is consistent with the idea that domain-specificity is a core principle underpinning functional organisation of the LIFG. These gradients were replicated across task-free and task-constrained FC measures, suggesting that a similar fundamental organisation underpins both mental states.

neuroscience↗

The Ventrolateral Anterior Temporal Lobe is Commonly Engaged by Both Mental State Inference and Semantic Association Tasks

A key challenge for neurobiological models of social cognition is to elucidate whether brain regions are specialised for that domain. In recent years, discussion surrounding the role of anterior temporal regions epitomises such debates; some argue the anterior temporal lobe (ATL) is part of a domain-specific network for social processing, while others claim it comprises a domain-general hub for semantic representation. In the present study, we used ATL-optimised fMRI to map the contribution of different ATL structures to a variety of paradigms frequently used to probe a crucial social ability, namely theory of mind (ToM). Using multiple tasks enables a clearer attribution of activation to ToM as opposed to idiosyncratic features of stimuli. Further, we directly explored whether these same structures are also activated by a non-social task probing semantic representations. We revealed that common to all of the tasks was activation of a key ventrolateral ATL region that is often invisible to standard fMRI. This constitutes novel evidence in support of the view that the ventrolateral ATL contributes to social cognition via a domain-general role in semantic processing, and against claims of a specialised social function.

neuroscience↗

Establishing a Role of the Semantic Control Network in Social Cognitive Processing: A Meta-analysis of Functional Neuroimaging Studies

Most leading models of socio-cognitive processing devote little discussion to the nature and neuroanatomical correlates of cognitive control mechanisms. Recently, it has been proposed that the regulation of social behaviours could rely on brain regions specialised in the controlled retrieval of semantic information, namely the anterior inferior frontal gyrus (IFG) and posterior middle temporal gyrus. Accordingly, we set out to investigate whether the neural activation commonly found in social functional neuroimaging studies extends to these semantic control regions. We conducted five coordinate-based meta-analyses to combine results of over 500 fMRI/PET experiments and identified the brain regions consistently involved in semantic control, as well as four social abilities: theory of mind, trait inference, empathy and moral reasoning. This allowed an unprecedented parallel review of the neural networks associated with each of these cognitive domains. The results confirmed that the anterior left IFG region involved in semantic control is reliably engaged in all four social domains. This suggests that social cognition could be partly regulated by the neurocognitive system underpinning semantic control.

neuroscience↗

The Coherent Default Mode Network is not involved in Episodic Recall or Social Cognition

Resting-state network research is extremely influential, yet the functions of many networks remain unknown. In part, this is due to typical (e.g., univariate) analyses testing the function of individual regions and not the full set of co-activated regions that form a network. Connectivity is dynamic and the function of a region may change based on its current connections. Therefore, determining the function of a network requires assessment at the network-level. Yet popular theories implicating the default mode network (DMN) in episodic memory and social cognition, rest principally upon analyses performed at the level of individual brain regions. Here we use independent component analysis to formally test the role of the DMN in episodic and social processing at the network level. As well as an episodic retrieval task, two independent datasets were employed to assess DMN function across the breadth of social cognition; a person knowledge judgement and a theory of mind task. Each task dataset was separated into networks of co-activated regions. In each, the co-activated DMN, was identified through comparison to an a priori template and its relation to the task model assessed. This co-activated DMN did not show greater activity in episodic or social tasks than high-level baseline conditions. Thus, no evidence was found to support hypotheses that the co-activated DMN is involved in explicit episodic or social processing tasks at a network-level. The networks associated with these processes are described. Implications for prior univariate findings and the functional significance of the co-activated DMN are considered.

neuroscience↗