Charlotte Murphy

Exploring the role of the posterior middle temporal gyrus in semantic cognition : Integration of anterior temporal lobe with executive processes

Making sense of the world around us depends upon selectively retrieving information relevant to our current goal or context. However, it is unclear whether selective semantic retrieval relies exclusively on general control mechanisms recruited in demanding non-semantic tasks, or instead on systems specialised for the control of meaning. One hypothesis is that the left posterior middle temporal gyrus (pMTG) is important in the controlled retrieval of semantic (not non-semantic) information; however this view remains controversial since a parallel literature links this site to event and relational semantics. In a functional neuroimaging study, we demonstrated that an area of pMTG implicated in semantic control by a recent meta-analysis was activated in a conjunction of (i) semantic association over size judgements and (ii) action over colour feature matching. Under these circumstances the same region showed functional coupling with the inferior frontal gyrus — another crucial site for semantic control. Structural and functional connectivity analyses demonstrated that this site is at the nexus of networks recruited in automatic semantic processing (the default mode network) and executively demanding tasks (the multiple-demand network). Moreover, in both task and task-free contexts, pMTG exhibited functional properties that were more similar to ventral parts of inferior frontal cortex, implicated in controlled semantic retrieval, than more dorsal inferior frontal sulcus, implicated in domain-general control. Finally, the pMTG region was functionally correlated at rest with other regions implicated in control-demanding semantic tasks, including inferior frontal gyrus and intraparietal sulcus. We suggest that pMTG may play a crucial role within a large-scale network that allows the integration of automatic retrieval in the default mode network with executively-demanding goal-oriented cognition, and that this could support our ability to understand actions and non-dominant semantic associations, allowing semantic retrieval to be ‘shaped’ to suit a task or context.

Fractionating the anterior temporal lobe : MVPA reveals differential responses to input and conceptual modality

ABSTRACT Words activate cortical regions in accordance with their modality of presentation (i.e., written vs. spoken), yet there is a long‐standing debate about whether patterns of activity in any specific brain region capture modality‐invariant conceptual information. Deficits in patients with semantic dementia highlight the anterior temporal lobe (ATL) as an amodal store of semantic knowledge but these studies do not permit precise localisation of this function. The current investigation used multiple imaging methods in healthy participants to examine functional dissociations within ATL. Multi‐voxel pattern analysis identified spatially segregated regions: a response to input modality in anterior superior temporal gyrus (aSTG) and a response to meaning in more ventral anterior temporal lobe (vATL). This functional dissociation was supported by resting‐state connectivity that found greater coupling for aSTG with primary auditory cortex and vATL with the default mode network. A meta‐analytic decoding of these connectivity patterns implicated aSTG in processes closely tied to auditory processing (such as phonology and language) and vATL in meaning‐based tasks (such as comprehension or social cognition). Thus we provide converging evidence for the segregation of meaning and input modality in the ATL. HIGHLIGHTSMulti‐voxel pattern analysis identified spatially segregated regions in the anterior temporal lobe.Anterior superior temporal gyrus (aSTG) responded to modality input.Ventral anterior temporal lobe (vATL) responded to semantic meaning.Converging findings from resting‐state connectivity supports this functional dissociation.

Varieties of semantic cognition revealed through simultaneous decomposition of intrinsic brain connectivity and behaviour

Contemporary theories assume that semantic cognition emerges from a neural architecture in which different component processes are combined to produce aspects of conceptual thought and behaviour. In addition to the state-level, momentary variation in brain connectivity, individuals may also differ in their propensity to generate particular configurations of such components, and these trait-level differences may relate to individual differences in semantic cognition. We tested this view by exploring how variation in intrinsic brain functional connectivity between semantic nodes in fMRI was related to performance on a battery of semantic tasks in 154 healthy participants. Through simultaneous decomposition of brain functional connectivity and semantic task performance, we identified distinct components of semantic cognition at rest. In a subsequent validation step, these data-driven components demonstrated explanatory power for neural responses in an fMRI-based semantic localiser task and variation in self-generated thoughts during the resting-state scan. Our findings showed that good performance on harder semantic tasks was associated with relative segregation at rest between frontal brain regions implicated in controlled semantic retrieval and the default mode network. Poor performance on easier tasks was linked to greater coupling between the same frontal regions and the anterior temporal lobe; a pattern associated with deliberate, verbal thematic thoughts at rest. We also identified components that related to qualities of semantic cognition: relatively good performance on pictorial semantic tasks was associated with greater separation of angular gyrus from frontal control sites and greater integration with posterior cingulate and anterior temporal cortex. In contrast, good speech production was linked to the separation of angular gyrus, posterior cingulate and temporal lobe regions. Together these data show that quantitative and qualitative variation in semantic cognition across individuals emerges from variations in the interaction of nodes within distinct functional brain networks.

An individual differences analysis of the neurocognitive architecture of the semantic system at rest.

Highlights • Variations in semantic performance are reflected in resting-state networks.• Inferior frontal connectivity predicts verbal fluency performance.• Connectivity between visual and anterior temporal areas predicts synonym judgement.

Distant from input: Evidence of regions within the default mode network supporting perceptually-decoupled and conceptually-guided cognition

&NA; The default mode network supports a variety of mental operations such as semantic processing, episodic memory retrieval, mental time travel and mind‐wandering, yet the commonalities between these functions remains unclear. One possibility is that this system supports cognition that is independent of the immediate environment; alternatively or additionally, it might support higher‐order conceptual representations that draw together multiple features. We tested these accounts using a novel paradigm that separately manipulated the availability of perceptual information to guide decision‐making and the representational complexity of this information. Using task based imaging we established regions that respond when cognition combines both stimulus independence with multi‐modal information. These included left and right angular gyri and the left middle temporal gyrus. Although these sites were within the default mode network, they showed a stronger response to demanding memory judgements than to an easier perceptual task, contrary to the view that they support automatic aspects of cognition. In a subsequent analysis, we showed that these regions were located at the extreme end of a macroscale gradient, which describes gradual transitions from sensorimotor to transmodal cortex. This shift in the focus of neural activity towards transmodal, default mode, regions might reflect a process of where the functional distance from specific sensory enables conceptually rich and detailed cognitive states to be generated in the absence of input. HighlightsBrain regions supporting meaning overlap with stimulus independence.Bilateral angular gyri and left MTG respond strongly to both features of cognition.These patterns reflect a shift in activity towards regions of transmodal cortex.Complex memory representations may emerge in cortical areas distant from input.

Dimensions of Experience : Exploring the Heterogeneity of the Wandering Mind

The tendency for the mind to wander to concerns other than the task at hand is a fundamental feature of human cognition, yet the consequences of variations in its experiential content for psychological functioning are not well understood. Here, we adopted multivariate pattern analysis to simultaneously decompose experience-sampling data and neural functional-connectivity data, which revealed dimensions that simultaneously describe individual variation in self-reported experience and default-mode-network connectivity. We identified dimensions corresponding to traits of positive-habitual thoughts and spontaneous task-unrelated thoughts. These dimensions were uniquely related to aspects of cognition, such as executive control and the ability to generate information in a creative fashion, and independently distinguished well-being measures. These data provide the most convincing evidence to date for an ontological view of the mind-wandering state as encompassing a broad range of different experiences and show that this heterogeneity underlies mind wandering’s complex relationship to psychological functioning.

Isolated from input: Evidence of default mode network support for perceptually-decoupled and conceptually-guided cognition

The default mode network supports a variety of mental operations such as semantic processing, episodic memory retrieval, mental time travel and mind-wandering, yet the commonalities between these functions remains unclear. One possibility is that the default mode network supports cognition that is independent of the immediate environment; alternatively or additionally, it might support higher-order conceptual representations that draw together multiple features. We tested these accounts using a novel paradigm that contrasted decisions based on perceptual and conceptual features, while separately manipulating whether these decisions were driven by features in the environment or recovered from memory. Task-based fMRI identified regions that responded when stimulus independence and semantic retrieval were combined: these included left and right angular gyri and left middle temporal gyrus. Although these sites were within the default mode network, they showed a stronger response to demanding memory judgements than to an easier perceptual task, contrary to the view that they support automatic aspects of cognition. In a subsequent analysis, we showed that these regions were located at the extreme end of a macroscale gradient, which describes gradual transitions from sensorimotor to transmodal cortex. This shift in the focus of neural activity towards transmodal default mode regions might reflect isolation from specific sensory inputs, both when decisions are guided by conceptual as opposed to perceptual features and when cognitive states are generated in the absence of input. Highlights Brain regions supporting meaning overlap with stimulus independence. Bilateral angular gyri and left MTG respond strongly to both features of cognition. These patterns reflect a shift in activity towards regions of transmodal cortex. Complex memory representations may emerge in cortical areas distant from input.

Default mode network can support the level of detail in experience during active task states

Significance Accounts of the default mode network (DMN) as task negative are partly based on evidence for a role of this system in off-task thought. We revisited the evidence for this assumption in a study combining experience sampling with functional neuroimaging. Whether thoughts were related or unrelated to an ongoing task was associated with patterns of neural activity in regions adjacent to unimodal sensorimotor cortex. In contrast, during periods of working-memory maintenance, activity patterns in the DMN were associated with whether thoughts were detailed. These results demonstrate that activity within the DMN encodes information associated with ongoing cognition that goes beyond whether attention is directed to the task, including detailed experiences during active task states. Regions of transmodal cortex, in particular the default mode network (DMN), have historically been argued to serve functions unrelated to task performance, in part because of associations with naturally occurring periods of off-task thought. In contrast, contemporary views of the DMN suggest it plays an integrative role in cognition that emerges from its location at the top of a cortical hierarchy and its relative isolation from systems directly involved in perception and action. The combination of these topographical features may allow the DMN to support abstract representations derived from lower levels in the hierarchy and so reflect the broader cognitive landscape. To investigate these contrasting views of DMN function, we sampled experience as participants performed tasks varying in their working-memory load while inside an fMRI scanner. We used self-report data to establish dimensions of thought that describe levels of detail, the relationship to a task, the modality of thought, and its emotional qualities. We used representational similarity analysis to examine correspondences between patterns of neural activity and each dimension of thought. Our results were inconsistent with a task-negative view of DMN function. Distinctions between on- and off-task thought were associated with patterns of consistent neural activity in regions adjacent to unimodal cortex, including motor and premotor cortex. Detail in ongoing thought was associated with patterns of activity within the DMN during periods of working-memory maintenance. These results demonstrate a contribution of the DMN to ongoing cognition extending beyond task-unrelated processing that can include detailed experiences occurring under active task conditions.

Meaningful inhibition: Exploring the role of meaning and modality in response inhibition

ABSTRACT We frequently guide our decisions about when and how to act based on the meanings of perceptual inputs: we might avoid treading on a flower, but not on a leaf. However, most research on response inhibition has used simple perceptual stimuli devoid of meaning. In two Go/No‐Go experiments, we examined whether the neural mechanisms supporting response inhibition are influenced by the relevance of meaning to the decision, and by presentation modality (whether concepts were presented as words or images). In an on‐line fMRI experiment, we found common regions for response inhibition across perceptual and conceptual decisions. These included the bilateral intraparietal sulcus and the right inferior frontal sulcus, whose neural responses have been linked to diverse cognitive demands in previous studies. In addition, we identified a cluster in ventral lateral occipital cortex that was sensitive to the modality of input, with a stronger response to No‐Go than Go trials for meaningful images, compared to words with the same semantic content. In a second experiment, using resting‐state fMRI, we explored how individual variation in the intrinsic connectivity of these activated regions related to variation in behavioural performance. Participants who showed stronger connectivity between common inhibition regions and limbic areas in medial temporal and subgenual anterior cingulate cortex were better at inhibition when this was driven by the meaning of the items. In addition, regions with a specific role in picture inhibition were more connected to a cluster in the thalamus/caudate for participants who were better at performing the picture task outside of the scanner. Together these studies indicate that the capacity to appropriately withhold action depends on interactions between common control regions, which are important across multiple types of input and decision, and other brain regions linked to specific inputs (i.e., visual features) or representations (e.g., memory).

Imagining Sounds and Images: Decoding the Contribution of Unimodal and Transmodal Brain Regions to Semantic Retrieval in the Absence of Meaningful Input

In the absence of sensory information, we can generate meaningful images and sounds from representations in memory. However, it remains unclear which neural systems underpin this process and whether tasks requiring the top–down generation of different kinds of features recruit similar or different neural networks. We asked people to internally generate the visual and auditory features of objects, either in isolation (car, dog) or in specific and complex meaning-based contexts (car/dog race). Using an fMRI decoding approach, in conjunction with functional connectivity analysis, we examined the role of auditory/visual cortex and transmodal brain regions. Conceptual retrieval in the absence of external input recruited sensory and transmodal cortex. The response in transmodal regions—including anterior middle temporal gyrus—was of equal magnitude for visual and auditory features yet nevertheless captured modality information in the pattern of response across voxels. In contrast, sensory regions showed greater activation for modality-relevant features in imagination (even when external inputs did not differ). These data are consistent with the view that transmodal regions support internally generated experiences and that they play a role in integrating perceptual features encoded in memory.