Abstract
The neural architecture of semantic knowledge comprises two key structures: (i) A set of widely dispersed regions, located adjacent to the sensorimotor cortices, serve as spokes that represent various modality-specific and context-dependent contents. (ii) The anterior-temporal lobe (ATL) serves as a hub that computes the nonlinear mappings required to transform modality-specific information into pan-modality, multifaceted concepts. Little is understood regarding whether neural dynamics between the hub and spokes might flexibly alter depending on the nature of a concept and how it impinges upon behaviour. Using fMRI, we demonstrate for the first time that the ATL serves as a ‘pivot’ which dynamically forms flexible long-range networks with cortical modules specialised for different domains (in the present case, the knowledge about actions and places). In two experiments, we manipulated semantic congruity and asked participants to recognise visually presented items. In Experiment 1 (dual-object displays), the ATL increased its functional coupling with the bilateral frontoparietal action-sensitive system when the objects formed a pair that permitted semantically meaningful action. In Experiment 2 (objects embedded in a scene), the ATL augmented its coupling with the retrosplenial cortex of the place-sensitive system when the objects and scene formed a semantically coherent ensemble. Causative connectivity revealed that, while communication between the hub and spokes was bidirectional, the hub's directional impact on spokes dwarfed the strength of the inverse spoke-to-hub connectivity. Furthermore, the size of behavioural congruity effects co-varied with the strength of neural coupling between the ATL hub and action- / place-related spokes, evident both at the within-individual level (the behavioural fluctuation across scanning runs) and between-individual level (the behavioural variation of between participants). Together, these findings have important implications for understanding the machinery that links neural dynamics with semantic cognition.
Highlights
The neurobiological substrates of semantic knowledge have always been the primary focus of cognitive neuroscience
While prior studies have identified these separable functionally-specific systems for action and place knowledge, the role of the anterior-temporal lobe (ATL) has long been ignored due presumably to signal dropout (Visser, Jefferies, & Lambon Ralph, 2010) or a selective focus on the action- or place-specific regions. It remains unclear whether these apparently separable systems would be integrated by the ATL, and whether the extent of integration impinges upon behavioural performance. These questions directly put the hub-and-spoke hypothesis to the test – we investigated whether both action and place knowledge recruits the ATL-structure as a common nexus, as well as whether connectivity analysis would reveal any change in the alliance between the hub and spokes when participants retrieve different types of knowledge
While congruency did not modulate reaction time (RT) (t(19) = -1.24, p = 0.23; Cohen’s d = 0.28; related: 759 ms, unrelated: 776 ms), it drove a significant effect in accuracy (t(19) = 3.94, p = 0.001, d = 0.88), with object identification being more accurate for related objects that allowed meaningful actions (96%) than unrelated pairs (93%
Summary
The neurobiological substrates of semantic knowledge have always been the primary focus of cognitive neuroscience. A prominent theory fractionates the neural underpinning of semantic knowledge into two key constituents: the anterior-temporal lobe (ATL) as the hub and multiple modality- or category-specific regions as the spokes (Lambon Ralph, Jefferies, Patterson, & Rogers, 2017; Patterson & Lambon Ralph, 2015; Patterson, Nestor, & Rogers, 2007; Rogers et al, 2004). The semantic attributes of a steering-wheel comprise its motoric attribute (to rotate), its locative attribute (inside a vehicle), and visual attribute (circular in shape) Such modality- or featurespecific information is hypothesised to be handled by cortical ‘spokes’ specialised in processing action, place, and shape, respectively. Over and above these fragments of semantic information, the ATL is assumed to aggregate neural processing from different sources and enable the formation of a unified concept about ‘steering-wheel’. Its proposed ‘hub’ component enables this theory to offer explanations for a plethora of observations that the embodied cognition theory struggles to tackle (for discussion about the insufficiency of strong embodied cognition views, see Lambon Ralph, 2014; Lambon Ralph et al, 2017)
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