Default mode network shows distinct emotional and contextual responses yet common effects of retrieval demands across tasks.

The default mode network (DMN) lies towards the heteromodal end of the principal gradient of intrinsic connectivity, maximally separated from the sensory-motor cortex. It supports memory-based cognition, including the capacity to retrieve conceptual and evaluative information from sensory inputs, and to generate meaningful states internally; however, the functional organisation of DMN that can support these distinct modes of retrieval remains unclear. We used fMRI to examine whether activation within subsystems of DMN differed as a function of retrieval demands, or the type of association to be retrieved, or both. In a picture association task, participants retrieved semantic associations that were either contextual or emotional in nature. Participants were asked to avoid generating episodic associations. In the generate phase, these associations were retrieved from a novel picture, while in the switch phase, participants retrieved a new association for the same image. Semantic context and emotion trials were associated with dissociable DMN subnetworks, indicating that a key dimension of DMN organisation relates to the type of association being accessed. The frontotemporal and medial temporal DMN showed a preference for emotional and semantic contextual associations, respectively. Relative to the generate phase, the switch phase recruited clusters closer to the heteromodal apex of the principal gradient-a cortical hierarchy separating unimodal and heteromodal regions. There were no differences in this effect between association types. Instead, memory switching was associated with a distinct subnetwork associated with controlled internal cognition. These findings delineate distinct patterns of DMN recruitment for different kinds of associations yet common responses across tasks that reflect retrieval demands.

Dissecting the neuroanatomy of creativity and curiosity: The subdivisions within networks matter.

Ivancovsky et al. argue that the neurocognitive mechanisms of creativity and curiosity both rely on the interplay among brain networks. Research to date demonstrates that such inter-network dynamics are further complicated by functional fractionation within networks. Investigating how networks subdivide and reconfigure in service of a task offers insights about the precise anatomy that underpins creative and curious behaviour.

Distinctive and Complementary Roles of Default Mode Network Subsystems in Semantic Cognition.

The default mode network (DMN) typically deactivates to external tasks, yet supports semantic cognition. It comprises medial temporal (MT), core, and frontotemporal (FT) subsystems, but its functional organization is unclear: the requirement for perceptual coupling versus decoupling, input modality (visual/verbal), type of information (social/spatial), and control demands all potentially affect its recruitment. We examined the effect of these factors on activation and deactivation of DMN subsystems during semantic cognition, across four task-based human functional magnetic resonance imaging (fMRI) datasets, and localized these responses in whole-brain state space defined by gradients of intrinsic connectivity. FT showed activation consistent with a central role across domains, tasks, and modalities, although it was most responsive to abstract, verbal tasks; this subsystem uniquely showed more "tuned" states characterized by increases in both activation and deactivation when semantic retrieval demands were higher. MT also activated to both perceptually coupled (scenes) and decoupled (autobiographical memory) tasks and showed stronger responses to picture associations, consistent with a role in scene construction. Core DMN consistently showed deactivation, especially to externally oriented tasks. These diverse contributions of DMN subsystems to semantic cognition were related to their location on intrinsic connectivity gradients: activation was closer to the sensory-motor cortex than deactivation, particularly for FT and MT, while activation for core DMN was distant from both visual cortex and cognitive control. These results reveal distinctive yet complementary DMN responses: MT and FT support different memory-based representations that are accessed externally and internally, while deactivation in core DMN is associated with demanding, external semantic tasks.

The Brain's Topographical Organization Shapes Dynamic Interaction Patterns That Support Flexible Behavior Based on Rules and Long-Term Knowledge.

Adaptive behavior relies both on specific rules that vary across situations and stable long-term knowledge gained from experience. The frontoparietal control network (FPCN) is implicated in the brain's ability to balance these different influences on action. Here, we investigate how the topographical organization of the cortex supports behavioral flexibility within the FPCN. Functional properties of this network might reflect its juxtaposition between the dorsal attention network (DAN) and the default mode network (DMN), two large-scale systems implicated in top-down attention and memory-guided cognition, respectively. Our study tests whether subnetworks of FPCN are topographically proximal to the DAN and the DMN, respectively, and how these topographical differences relate to functional differences: the proximity of each subnetwork is anticipated to play a pivotal role in generating distinct cognitive modes relevant to working memory and long-term memory. We show that FPCN subsystems share multiple anatomical and functional similarities with their neighboring systems (DAN and DMN) and that this topographical architecture supports distinct interaction patterns that give rise to different patterns of functional behavior. The FPCN acts as a unified system when long-term knowledge supports behavior but becomes segregated into discrete subsystems with different patterns of interaction when long-term memory is less relevant. In this way, our study suggests that the topographical organization of the FPCN and the connections it forms with distant regions of cortex are important influences on how this system supports flexible behavior.

Graded and sharp transitions in semantic function in left temporal lobe.

Recent work has focussed on how patterns of functional change within the temporal lobe relate to whole-brain dimensions of intrinsic connectivity variation (Margulies et al., 2016). We examined two such 'connectivity gradients' reflecting the separation of (i) unimodal versus heteromodal and (ii) visual versus auditory-motor cortex, examining visually presented verbal associative and feature judgments, plus picture-based context and emotion generation. Functional responses along the first dimension sometimes showed graded change between modality-tuned and heteromodal cortex (in the verbal matching task), and other times showed sharp functional transitions, with deactivation at the extremes and activation in the middle of this gradient (internal generation). The second gradient revealed more visual than auditory-motor activation, regardless of content (associative, feature, context, emotion) or task process (matching/generation). We also uncovered subtle differences across each gradient for content type, which predominantly manifested as differences in relative magnitude of activation or deactivation.

Healthy ageing has divergent effects on verbal and non-verbal semantic cognition.

Semantic cognition refers to the storage and appropriate use of knowledge acquired over the lifespan and underpins our everyday verbal and non-verbal behaviours. Successful semantic cognition requires representation of knowledge and control processes which ensure that currently relevant aspects of knowledge are retrieved and selected. Although these abilities have been widely studied in healthy young populations and semantically impaired patients, it is unclear how they change as a function of healthy ageing, especially for non-verbal semantic processing. Here, we addressed this issue by comparing the performance profiles of young and older people on a semantic knowledge task and a semantic control task, across verbal (word) and non-verbal (picture) versions. The results revealed distinct patterns of change during adulthood for semantic knowledge and semantic control. Older people performed better in both verbal and non-verbal knowledge tasks than young people. However, although the older group showed preserved controlled retrieval for verbal semantics, they demonstrated a specific impairment for non-verbal semantic control. These findings indicate that the effects of ageing on semantic cognition are more complex than previously assumed, and that input modality plays an important role in the shifting cognitive architecture of semantics in later life.

Creativity in verbal associations is linked to semantic control.

Although memory is known to play a key role in creativity, previous studies have not isolated the critical component processes and networks. We asked participants to generate links between words that ranged from strongly related to completely unrelated in long-term memory, delineating the neurocognitive processes that underpin more unusual versus stereotypical patterns of retrieval. More creative responses to strongly associated word-pairs were associated with greater engagement of episodic memory: in highly familiar situations, semantic, and episodic stores converge on the same information enabling participants to form a personal link between items. This pattern of retrieval was associated with greater engagement of core default mode network (DMN). In contrast, more creative responses to weakly associated word-pairs were associated with the controlled retrieval of less dominant semantic information and greater recruitment of the semantic control network, which overlaps with the dorsomedial subsystem of DMN. Although both controlled semantic and episodic patterns of retrieval are associated with activation within DMN, these processes show little overlap in activation. These findings demonstrate that controlled aspects of semantic cognition play an important role in verbal creativity.

Physical distance to sensory-motor landmarks predicts language function.

Auditory language comprehension recruits cortical regions that are both close to sensory-motor landmarks (supporting auditory and motor features) and far from these landmarks (supporting word meaning). We investigated whether the responsiveness of these regions in task-based functional MRI is related to individual differences in their physical distance to primary sensorimotor landmarks. Parcels in the auditory network, that were equally responsive across story and math tasks, showed stronger activation in individuals who had less distance between these parcels and transverse temporal sulcus, in line with the predictions of the "tethering hypothesis," which suggests that greater proximity to input regions might increase the fidelity of sensory processing. Conversely, language and default mode parcels, which were more active for the story task, showed positive correlations between individual differences in activation and sensory-motor distance from primary sensory-motor landmarks, consistent with the view that physical separation from sensory-motor inputs supports aspects of cognition that draw on semantic memory. These results demonstrate that distance from sensorimotor regions provides an organizing principle of functional differentiation within the cortex. The relationship between activation and geodesic distance to sensory-motor landmarks is in opposite directions for cortical regions that are proximal to the heteromodal (DMN and language network) and unimodal ends of the principal gradient of intrinsic connectivity.

Flexing the principal gradient of the cerebral cortex to suit changing semantic task demands.

Understanding how thought emerges from the topographical structure of the cerebral cortex is a primary goal of cognitive neuroscience. Recent work has revealed a principal gradient of intrinsic connectivity capturing the separation of sensory-motor cortex from transmodal regions of the default mode network (DMN); this is thought to facilitate memory-guided cognition. However, studies have not explored how this dimension of connectivity changes when conceptual retrieval is controlled to suit the context. We used gradient decomposition of informational connectivity in a semantic association task to establish how the similarity in connectivity across brain regions changes during familiar and more original patterns of retrieval. Multivoxel activation patterns at opposite ends of the principal gradient were more divergent when participants retrieved stronger associations; therefore, when long-term semantic information is sufficient for ongoing cognition, regions supporting heteromodal memory are functionally separated from sensory-motor experience. In contrast, when less related concepts were linked, this dimension of connectivity was reduced in strength as semantic control regions separated from the DMN to generate more flexible and original responses. We also observed fewer dimensions within the neural response towards the apex of the principal gradient when strong associations were retrieved, reflecting less complex or varied neural coding across trials and participants. In this way, the principal gradient explains how semantic cognition is organised in the human cerebral cortex: the separation of DMN from sensory-motor systems is a hallmark of the retrieval of strong conceptual links that are culturally shared.

Mapping lesion, structural disconnection, and functional disconnection to symptoms in semantic aphasia.

Patients with semantic aphasia have impaired control of semantic retrieval, often accompanied by executive dysfunction following left hemisphere stroke. Many but not all of these patients have damage to the left inferior frontal gyrus, important for semantic and cognitive control. Yet semantic and cognitive control networks are highly distributed, including posterior as well as anterior components. Accordingly, semantic aphasia might not only reflect local damage but also white matter structural and functional disconnection. Here, we characterise the lesions and predicted patterns of structural and functional disconnection in individuals with semantic aphasia and relate these effects to semantic and executive impairment. Impaired semantic cognition was associated with infarction in distributed left-hemisphere regions, including in the left anterior inferior frontal and posterior temporal cortex. Lesions were associated with executive dysfunction within a set of adjacent but distinct left frontoparietal clusters. Performance on executive tasks was also associated with interhemispheric structural disconnection across the corpus callosum. In contrast, poor semantic cognition was associated with small left-lateralized structurally disconnected clusters, including in the left posterior temporal cortex. Little insight was gained from functional disconnection symptom mapping. These results demonstrate that while left-lateralized semantic and executive control regions are often damaged together in stroke aphasia, these deficits are associated with distinct patterns of structural disconnection, consistent with the bilateral nature of executive control and the left-lateralized yet distributed semantic control network.

Perceptual coupling and decoupling of the default mode network during mind-wandering and reading.

While reading, our mind can wander to unrelated autobiographical information, creating a perceptually decoupled state detrimental to narrative comprehension. To understand how this mind-wandering state emerges, we asked whether retrieving autobiographical content necessitates functional disengagement from visual input. In Experiment 1, brain activity was recorded using functional magnetic resonance imaging (fMRI) in an experimental situation mimicking naturally occurring mind-wandering, allowing us to precisely delineate neural regions involved in memory and reading. Individuals read expository texts and ignored personally relevant autobiographical memories, as well as the opposite situation. Medial regions of the default mode network (DMN) were recruited during memory retrieval. In contrast, left temporal and lateral prefrontal regions of the DMN, as well as ventral visual cortex, were recruited when reading for comprehension. Experiment two used functional connectivity both at rest and during tasks to establish that (i) DMN regions linked to memory are more functionally decoupled from regions of ventral visual cortex than regions in the same network engaged when reading; and (ii) individuals with more self-generated mental contents and poorer comprehension, while reading in the lab, showed more decoupling between visually connected DMN sites important for reading and primary visual cortex. A similar pattern of connectivity was found in Experiment 1, with greater coupling between this DMN site and visual cortex when participants reported greater focus on reading in the face of conflict from autobiographical memory cues; moreover, the retrieval of personally relevant memories increased the decoupling of these sites. These converging data suggest we lose track of the narrative when our minds wander because generating autobiographical mental content relies on cortical regions within the DMN which are functionally decoupled from ventral visual regions engaged during reading.

As your eyes scan these words, you may be thinking about what to make for dinner, how to address an unexpected hurdle at work, or how many emails are sitting, unread, in your inbox. This type of mind-wandering disrupts our focus and limits how much information we comprehend, whilst also being conducive to creative thinking and problem-solving. Despite being an everyday occurrence, exactly how our mind wanders remains elusive. One possible explanation is that the brain disengages from visual information from the external world and turns its attention inwards. A greater understanding of which neural circuits are involved in this process could reveal insights about focus, attention, and reading comprehension. Here, Zhang et al. investigated whether the brain becomes disengaged from visual input when our mind wanders while reading. Recalling personal events was used as a proxy for mind-wandering. Brain activity was recorded as participants were shown written statements; sometimes these were preceded by cues to personal memories. People were asked to focus on reading the statements or they were instructed to concentrate on their memories while ignoring the text. The analyses showed that recalling memories and reading stimulated distinct parts of the brain, which were in direct competition during mind-wandering. Further work examined how these regions were functionally connected. In individuals who remained focused on reading despite memory cues, the areas activated by reading showed strong links to the visual cortex. Conversely, these reading-related areas became 'decoupled' from visual processing centres in people who were focusing more on their internal thoughts. These results shed light on why we lose track of what we are reading when our mind wanders: recalling personal memories activates certain brain areas which are functionally decoupled from the regions involved in processing external information ­ such as the words on a page. In summary, the work by Zhang et al. builds a mechanistic understanding of mind-wandering, a natural feature of our daily brain activity. These insights may help to inform future interventions in education to improve reading, comprehension and focus.

Individual differences in gradients of intrinsic connectivity within the semantic network relate to distinct aspects of semantic cognition.

Semantic cognition allows us to make sense of our varied experiences, including the words we hear and the objects we see. Contemporary accounts identify multiple interacting components that underpin semantic cognition, including diverse unimodal "spoke" systems that are integrated by a heteromodal "hub", and control processes that allow us to access weakly-encoded as well as dominant aspects of knowledge to suit the circumstances. The current study examined how these dimensions of semantic cognition might be related to whole-brain-derived components (or gradients) of connectivity. A nonlinear dimensionality reduction technique was applied to resting-state functional magnetic resonance imaging from 176 participants to characterise the strength of two key connectivity gradients in each individual: the principal gradient captured the separation between unimodal and heteromodal cortex, while the second gradient corresponded to the distinction between motor and visual cortex. We then examined whether the magnitude of these gradients within the semantic network was related to specific aspects of semantic cognition by examining individual differences in semantic and non-semantic tasks. Participants whose intrinsic connectivity showed a better fit with Gradient 1 had faster identification of weak semantic associations. Furthermore, a better fit with Gradient 2 was linked to faster performance on picture semantic judgements. These findings show that individual differences in aspects of semantic cognition can be related to components of connectivity within the semantic network.

Context free and context-dependent conceptual representation in the brain.

How concepts are coded in the brain is a core issue in cognitive neuroscience. Studies have focused on how individual concepts are processed, but the way in which conceptual representation changes to suit the context is unclear. We parametrically manipulated the association strength between words, presented in pairs one word at a time using a slow event-related fMRI design. We combined representational similarity analysis and computational linguistics to probe the neurocomputational content of these trials. Individual word meaning was maintained in supramarginal gyrus (associated with verbal short-term memory) when items were judged to be unrelated, but not when a linking context was retrieved. Context-dependent meaning was instead represented in left lateral prefrontal gyrus (associated with controlled retrieval), angular gyrus, and ventral temporal lobe (regions associated with integrative aspects of memory). Analyses of informational connectivity, examining the similarity of activation patterns across trials between sites, showed that control network regions had more similar multivariate responses across trials when association strength was weak, reflecting a common controlled retrieval state when the task required more unusual associations. These findings indicate that semantic control and representational sites amplify contextually relevant meanings in trials judged to be related.

Distinct and common neural coding of semantic and non-semantic control demands.

The flexible retrieval of knowledge is critical in everyday situations involving problem solving, reasoning and social interaction. Current theories emphasise the importance of a left-lateralised semantic control network (SCN) in supporting flexible semantic behaviour, while a bilateral multiple-demand network (MDN) is implicated in executive functions across domains. No study, however, has examined whether semantic and non-semantic demands are reflected in a common neural code within regions specifically implicated in semantic control. Using functional MRI and univariate parametric modulation analysis as well as multivariate pattern analysis, we found that semantic and non-semantic demands gave rise to both similar and distinct neural responses across control-related networks. Though activity patterns in SCN and MDN could decode the difficulty of both semantic and verbal working memory decisions, there was no shared common neural coding of cognitive demands in SCN regions. In contrast, regions in MDN showed common patterns across manipulations of semantic and working memory control demands, with successful cross-classification of difficulty across tasks. Therefore, SCN and MDN can be dissociated according to the information they maintain about cognitive demands.

Intrinsic connectivity of anterior temporal lobe relates to individual differences in semantic retrieval for landmarks.

Contemporary neuroscientific accounts suggest that ventral anterior temporal lobe (ATL) acts as a bilateral heteromodal semantic hub, which is particularly critical for the specific-level knowledge needed to recognise unique entities, such as familiar landmarks and faces. There may also be graded functional differences between left and right ATL, relating to effects of modality (linguistic versus non-linguistic) and category (e.g., knowledge of people and places). Individual differences in intrinsic connectivity from left and right ATL might be associated with variation in semantic categorisation performance across these categories and modalities. We recorded resting-state fMRI in 74 individuals and, in a separate session, examined semantic categorisation. People with greater connectivity between left and right ATL were more efficient at categorising landmarks (e.g., Eiffel Tower), especially when these were presented visually. In addition, participants who showed stronger connectivity from right than left ATL to medial occipital cortex showed more efficient semantic categorisation of landmarks regardless of modality of presentation. These results can be interpreted in terms of graded differences in the patterns of connectivity across left and right ATL, which give rise to a bilateral yet partially segregated semantic 'hub'. More specifically, right ATL connectivity supports the efficient semantic categorisation of landmarks.

Knowing what you need to know in advance: The neural processes underpinning flexible semantic retrieval of thematic and taxonomic relations.

Semantic retrieval is flexible, allowing us to focus on subsets of features and associations that are relevant to the current task or context: for example, we use taxonomic relations to locate items in the supermarket (carrots are a vegetable), but thematic associations to decide which tools we need when cooking (carrot goes with peeler). We used fMRI to investigate the neural basis of this form of semantic flexibility; in particular, we asked how retrieval unfolds differently when participants have advanced knowledge of the type of link to retrieve between concepts (taxonomic or thematic). Participants performed a semantic relatedness judgement task: on half the trials, they were cued to search for a taxonomic or thematic link, while on the remaining trials, they judged relatedness without knowing which type of semantic relationship would be relevant. Left inferior frontal gyrus showed greater activation when participants knew the trial type in advance. An overlapping region showed a stronger response when the semantic relationship between the items was weaker, suggesting this structure supports both top-down and bottom-up forms of semantic control. Multivariate pattern analysis further revealed that the neural response in left inferior frontal gyrus reflects goal information related to different conceptual relationships. Top-down control specifically modulated the response in visual cortex: when the goal was unknown, there was greater deactivation to the first word, and greater activation to the second word. We conclude that top-down control of semantic retrieval is primarily achieved through the gating of task-relevant 'spoke' regions.

Controlled semantic summation correlates with intrinsic connectivity between default mode and control networks.

The capacity to identify aspects of meaning that overlap across multiple concepts may relate to individual differences in the strength of intrinsic connectivity within and between distinct brain networks supporting semantic cognition. This study examined a semantic summation task, which tested the capacity to detect weak overlapping aspects of meaning, in 76 participants who were also scanned with resting-state fMRI. We examined associations between summation and the intrinsic connectivity of semantically-relevant default mode and control network regions. These networks are implicated in information integration and controlled retrieval respectively. We found higher intrinsic connectivity between default and control networks was associated with better performance in the summation task. The same pattern of coupling between semantic default mode and control networks was not associated with more efficient retrieval of individual weak as opposed to strong associations in an additional cohort of around 200 participants, suggesting this pattern is specific to the summation of multiple concepts, rather than semantic task difficulty. Finally, higher connectivity within the default mode network was associated with better performance when selecting a word that was strongly-related to a single probe item, supporting the role of this network in more automatic aspects of semantic retrieval.

Reduced semantic control in older adults is linked to intrinsic DMN connectivity.

Ageing provides an interesting window into semantic cognition: while younger adults generally outperform older adults on many cognitive tasks, knowledge continues to accumulate over the lifespan and consequently, the semantic store (i.e., vocabulary size) remains stable (or even improves) during healthy ageing. Semantic cognition involves the interaction of at least two components - a semantic store and control processes that interact to ensure efficient and context-relevant use of representations. Given older adults perform less well on tasks measuring executive control, their ability to access the semantic store in a goal driven manner may be compromised. Older adults also consistently show reductions in intrinsic brain connectivity, and we examined how these brain changes relate to age-related changes in semantic performance. We found that while older participants outperformed their younger counterparts on tests of vocabulary size (i.e., NART), younger participants were faster and more accurate in tasks requiring semantic control, and these age differences correlated with measures of intrinsic connectivity between the anterior temporal lobe (ATL) and medial prefrontal cortex (mPFC), within the default mode network. Higher intrinsic connectivity from right ATL to mPFC at rest related to better performance on verbal (but not picture) semantic tasks, and older adults showed an exaggerated version of this pattern, suggesting that this within-DMN connectivity may become more important for conceptual access from words as we age. However, this appeared to be at the expense of control over semantic retrieval - there was little relationship between connectivity and performance for strong associations in either group, but older adults with stronger connectivity showed particularly inefficient retrieval of weak associations. Older adults may struggle to harness the default mode network to support demanding patterns of semantic retrieval, resulting in a performance cost.

Distinct neural systems recruited when speech production is modulated by different masking sounds.

When talkers speak in masking sounds, their speech undergoes a variety of acoustic and phonetic changes. These changes are known collectively as the Lombard effect. Most behavioural research and neuroimaging research in this area has concentrated on the effect of energetic maskers such as white noise on Lombard speech. Previous fMRI studies have argued that neural responses to speaking in noise are driven by the quality of auditory feedback-that is, the audibility of the speaker's voice over the masker. However, we also frequently produce speech in the presence of informational maskers such as another talker. Here, speakers read sentences over a range of maskers varying in their informational and energetic content: speech, rotated speech, speech modulated noise, and white noise. Subjects also spoke in quiet and listened to the maskers without speaking. When subjects spoke in masking sounds, their vocal intensity increased in line with the energetic content of the masker. However, the opposite pattern was found neurally. In the superior temporal gyrus, activation was most strongly associated with increases in informational, rather than energetic, masking. This suggests that the neural activations associated with speaking in noise are more complex than a simple feedback response.

Down but not out in posterior cingulate cortex: Deactivation yet functional coupling with prefrontal cortex during demanding semantic cognition.

The posterior cingulate cortex (pCC) often deactivates during complex tasks, and at rest is often only weakly correlated with regions that play a general role in the control of cognition. These observations led to the hypothesis that pCC contributes to automatic aspects of memory retrieval and cognition. Recent work, however, has suggested that the pCC may support both automatic and controlled forms of memory processing and may do so by changing its communication with regions that are important in the control of cognition across multiple domains. The current study examined these alternative views by characterising the functional coupling of the pCC in easy semantic decisions (based on strong global associations) and in harder semantic tasks (matching words on the basis of specific non-dominant features). Increasingly difficult semantic decisions led to the expected pattern of deactivation in the pCC; however, psychophysiological interaction analysis revealed that, under these conditions, the pCC exhibited greater connectivity with dorsolateral prefrontal cortex (PFC), relative to both easier semantic decisions and to a period of rest. In a second experiment using different participants, we found that functional coupling at rest between the pCC and the same region of dorsolateral PFC was stronger for participants who were more efficient at semantic tasks when assessed in a subsequent laboratory session. Thus, although overall levels of activity in the pCC are reduced during external tasks, this region may show greater coupling with executive control regions when information is retrieved from memory in a goal-directed manner.