Publications by authors named "Jonathan Smallwood"

174 Publications

Differences in subcortico-cortical interactions identified from connectome and microcircuit models in autism.

Nat Commun 2021 04 13;12(1):2225. Epub 2021 Apr 13.

McConnell Brain Imaging Centre, Montreal Neurological Institute and Hospital, McGill University, Montreal, QC, Canada.

The pathophysiology of autism has been suggested to involve a combination of both macroscale connectome miswiring and microcircuit anomalies. Here, we combine connectome-wide manifold learning with biophysical simulation models to understand associations between global network perturbations and microcircuit dysfunctions in autism. We studied neuroimaging and phenotypic data in 47 individuals with autism and 37 typically developing controls obtained from the Autism Brain Imaging Data Exchange initiative. Our analysis establishes significant differences in structural connectome organization in individuals with autism relative to controls, with strong between-group effects in low-level somatosensory regions and moderate effects in high-level association cortices. Computational models reveal that the degree of macroscale anomalies is related to atypical increases of recurrent excitation/inhibition, as well as subcortical inputs into cortical microcircuits, especially in sensory and motor areas. Transcriptomic association analysis based on postmortem datasets identifies genes expressed in cortical and thalamic areas from childhood to young adulthood. Finally, supervised machine learning finds that the macroscale perturbations are associated with symptom severity scores on the Autism Diagnostic Observation Schedule. Together, our analyses suggest that atypical subcortico-cortical interactions are associated with both microcircuit and macroscale connectome differences in autism.
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http://dx.doi.org/10.1038/s41467-021-21732-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8044226PMC
April 2021

Varying demands for cognitive control reveals shared neural processes supporting semantic and episodic memory retrieval.

Nat Commun 2021 04 9;12(1):2134. Epub 2021 Apr 9.

Department of Psychology, University of York, York, UK.

The categorisation of long-term memory into semantic and episodic systems has been an influential catalyst for research on human memory organisation. However, the impact of variable cognitive control demands on this classical distinction remains to be elucidated. Across two independent experiments, here we directly compare neural processes for the controlled versus automatic retrieval of semantic and episodic memory. In a multi-session functional magnetic resonance imaging experiment, we first identify a common cluster of cortical activity centred on the left inferior frontal gyrus and anterior insular cortex for the retrieval of both weakly-associated semantic and weakly-encoded episodic memory traces. In an independent large-scale individual difference study, we further reveal a common neural circuitry in which reduced functional interaction between the identified cluster and ventromedial prefrontal cortex, a default mode network hub, is linked to better performance across both memory types. Our results provide evidence for shared neural processes supporting the controlled retrieval of information from functionally distinct long-term memory systems.
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http://dx.doi.org/10.1038/s41467-021-22443-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8035200PMC
April 2021

Atypical neural topographies underpin dysfunctional pattern separation in temporal lobe epilepsy.

Brain 2021 Mar 17. Epub 2021 Mar 17.

Multimodal Imaging and Connectome Analysis Laboratory, McConnell Brain Imaging Centre, Montreal Neurological Institute and Hospital, McGill University, Montreal, Canada.

Episodic memory is the ability to accurately remember events from our past. The process of pattern separation is hypothesized to underpin this ability and is defined as the ability to orthogonalize memory traces, to maximize the features that make them unique. Contemporary cognitive neuroscience suggests that pattern separation entails complex interactions between the hippocampus and the neocortex, where specific hippocampal subregions shape neural reinstatement in the neocortex. To test this hypothesis, the current work studied both healthy controls and patients with temporal lobe epilepsy (TLE) who present with hippocampal structural anomalies. In all participants, we measured neural activity using functional magnetic resonance imaging (fMRI) while they retrieved memorized items compared to lure items which share features with the target. Behaviorally, TLE patients were less able to exclude lures than controls, and showed a reduction in pattern separation. To assess the hypothesized relationship between neural patterns in the hippocampus and the neocortex, we identified topographic gradients of intrinsic connectivity along neocortical and hippocampal subfield surfaces and identified the topographic profile of the neural activity accompanying pattern separation. In healthy controls, pattern separation followed a graded pattern of neural activity, both along the hippocampal long axis (and peaked in anterior segments that are more heavily engaged in transmodal processing) and along the neocortical hierarchy running from unimodal to transmodal regions (peaking in transmodal default mode regions). In TLE patients, however, this concordance between task-based functional activations and topographic gradients was markedly reduced. Furthermore, person specific measures of concordance between task-related activity and connectivity gradients in patients and controls related to inter-individual differences in behavioral measures of pattern separation and episodic memory, highlighting the functional relevance of the observed topographic motifs. Our work is consistent with an emerging understanding that successful discrimination between memories with similar features entails a shift in the locus of neural activity away from sensory systems, a pattern that is mirrored along the hippocampal long axis and with respect to neocortical hierarchies. More broadly, our study establishes topographic profiling using intrinsic connectivity gradients captures the functional underpinnings of episodic memory processes in manner that is sensitive to their reorganization in pathology.
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http://dx.doi.org/10.1093/brain/awab121DOI Listing
March 2021

Training flexible conceptual retrieval in post-stroke aphasia.

Neuropsychol Rehabil 2021 Mar 14:1-27. Epub 2021 Mar 14.

Department of Psychology and York Neuroimaging Centre, University of York, York, UK.

Semantic therapy in post-stroke aphasia typically focusses on strengthening links between conceptual representations and their lexical-articulatory forms to aid word retrieval. However, research has shown that semantic deficits in this group can affect both verbal and non-verbal tasks, particularly in patients with deregulated retrieval as opposed to degraded knowledge. This study, therefore, aimed to facilitate semantic cognition in a sample of such patients with post-stroke semantic aphasia (SA) by training the identification of both strong and weak semantic associations and providing explicit pictorial feedback that demonstrated both common and more unusual ways of linking concepts together. We assessed the effects of this training on (i) trained and untrained items; and (ii) trained and untrained tasks in eleven individuals with SA. In the training task, the SA group showed improvement with practice, particularly for trained items. A similar untrained task using pictorial stimuli (Camel and Cactus Test) also improved. Together, these results suggest that semantic training can be beneficial in patients with SA and may show some degree of generalization to untrained situations. Future research should seek to understand which patients are most likely to benefit from this type of training.
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http://dx.doi.org/10.1080/09602011.2021.1895847DOI Listing
March 2021

A Structure-Function Substrate of Memory for Spatial Configurations in Medial and Lateral Temporal Cortices.

Cereb Cortex 2021 Feb 27. Epub 2021 Feb 27.

McConnell Brain Imaging Centre, Montreal Neurological Institute and Hospital, McGill University, Montreal, Quebec H3A 2B4, Canada.

Prior research has shown a role of the medial temporal lobe, particularly the hippocampal-parahippocampal complex, in spatial cognition. Here, we developed a new paradigm, the conformational shift spatial task (CSST), which examines the ability to encode and retrieve spatial relations between unrelated items. This task is short, uses symbolic cues, incorporates two difficulty levels, and can be administered inside the scanner. A cohort of 48 healthy young adults underwent the CSST, together with a set of behavioral measures and multimodal magnetic resonance imaging (MRI). Inter-individual differences in CSST performance correlated with scores on an established spatial memory paradigm, but neither with episodic memory nor mnemonic discrimination, supporting specificity. Analyzing high-resolution structural MRI data, individuals with better spatial memory showed thicker medial and lateral temporal cortices. Functional relevance of these findings was supported by task-based functional MRI analysis in the same participants and ad hoc meta-analysis. Exploratory resting-state functional MRI analyses centered on clusters of morphological effects revealed additional modulation of intrinsic network integration, particularly between lateral and medial temporal structures. Our work presents a novel spatial memory paradigm and supports an integrated structure-function substrate in the human temporal lobe. Task paradigms are programmed in python and made open access.
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http://dx.doi.org/10.1093/cercor/bhab001DOI Listing
February 2021

The neural correlates of ongoing conscious thought.

iScience 2021 Mar 1;24(3):102132. Epub 2021 Feb 1.

Department of Psychology / York Imaging Centre, University of York, York, England.

A core goal in cognitive neuroscience is identifying the physical substrates of the patterns of thought that occupy our daily lives. Contemporary views suggest that the landscape of ongoing experience is heterogeneous and can be influenced by features of both the person and the context. This perspective piece considers recent work that explicitly accounts for both the heterogeneity of the experience and context dependence of patterns of ongoing thought. These studies reveal that systems linked to attention and control are important for organizing experience in response to changing environmental demands. These studies also establish a role of the default mode network beyond task-negative or purely episodic content, for example, implicating it in the level of vivid detail in experience in both task contexts and in spontaneous self-generated experiential states. Together, this work demonstrates that the landscape of ongoing thought is reflected in the activity of multiple neural systems, and it is important to distinguish between processes contributing to how the experience unfolds from those linked to how these experiences are regulated.
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http://dx.doi.org/10.1016/j.isci.2021.102132DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7907463PMC
March 2021

Both Default and Multiple-Demand Regions Represent Semantic Goal Information.

J Neurosci 2021 Apr 4;41(16):3679-3691. Epub 2021 Mar 4.

Department of Psychology, University of York, York YO10 5DD, United Kingdom

We used a semantic feature-matching task combined with multivoxel pattern decoding to test contrasting accounts of the role of the default mode network (DMN) in cognitive flexibility. By one view, DMN and multiple-demand cortex have opposing roles in cognition, with DMN and multiple-demand regions within the dorsal attention network (DAN) supporting internal and external cognition, respectively. Consequently, while multiple-demand regions can decode current goal information, semantically relevant DMN regions might decode conceptual similarity regardless of task demands. Alternatively, DMN regions, like multiple-demand cortex, might show sensitivity to changing task demands, since both networks dynamically alter their patterns of connectivity depending on the context. Our task required human participants (any sex) to integrate conceptual knowledge with changing task goals, such that successive decisions were based on different features of the items (color, shape, and size). This allowed us to simultaneously decode semantic category and current goal information using whole-brain searchlight decoding. As expected, multiple-demand cortex, including DAN and frontoparietal control network, represented information about currently relevant conceptual features. Similar decoding results were found in DMN, including in angular gyrus and posterior cingulate cortex, indicating that DMN and multiple-demand regions can support the same function rather than being strictly competitive. Semantic category could be decoded in lateral occipital cortex independently of task demands, but not in most regions of DMN. Conceptual information related to the current goal dominates the multivariate response within DMN, which supports flexible retrieval by modulating its response to suit the task demands, alongside regions of multiple-demand cortex. We tested contrasting accounts of default mode network (DMN) function using multivoxel pattern analysis. By one view, semantically relevant parts of DMN represent conceptual similarity, regardless of task context. By an alternative view, DMN tracks changing task demands. Our semantic feature-matching task required participants to integrate conceptual knowledge with task goals, such that successive decisions were based on different features of the items. We demonstrate that DMN regions can decode the current goal, as it is applied, alongside multiple-demand regions traditionally associated with cognitive control, speaking to how DMN supports flexible cognition.
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http://dx.doi.org/10.1523/JNEUROSCI.1782-20.2021DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8055078PMC
April 2021

Interactions between the neural correlates of dispositional internally directed thought and visual imagery.

Philos Trans R Soc Lond B Biol Sci 2021 Feb 14;376(1817):20190691. Epub 2020 Dec 14.

Department of Psychology, York Neuroimaging Centre, University of York, York YO10 5DD, UK.

Cognition is not always directed to the events in the here and now and we often self-generate thoughts and images in imagination. Important aspects of these self-generated experiences are associated with various dispositional traits. In this study, we explored whether these psychological associations relate to a common underlying neurocognitive mechanism. We acquired resting state functional magnetic resonance imaging data from a large cohort of participants and asked them to retrospectively report their experience during the scan. Participants also completed questionnaires reflecting a range of dispositional traits. We found thoughts emphasizing visual imagery at rest were associated with dispositional tendency towards internally directed attention (self-consciousness and attentional problems) and linked to a stronger correlation between a posterior parietal network and a lateral fronto-temporal network. Furthermore, decoupling between the brainstem and a lateral visual network was associated with dispositional internally directed attention. Critically, these brain-cognition associations were related: the correlation between parietal-frontal regions and reports of visual imagery was stronger for individuals with increased connectivity between brainstem and visual cortex. Our results highlight neural mechanisms linked to the dispositional basis for patterns of self-generated thought, and suggest that accounting for dispositional traits is important when exploring the neural substrates of self-generated experience (and ). This article is part of the theme issue 'Offline perception: voluntary and spontaneous perceptual experiences without matching external stimulation'.
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http://dx.doi.org/10.1098/rstb.2019.0691DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7741082PMC
February 2021

The psychological correlates of distinct neural states occurring during wakeful rest.

Sci Rep 2020 12 3;10(1):21121. Epub 2020 Dec 3.

Department of Psychology, York Neuroimaging Centre, University of York, York, YO10 5DD, UK.

When unoccupied by an explicit external task, humans engage in a wide range of different types of self-generated thinking. These are often unrelated to the immediate environment and have unique psychological features. Although contemporary perspectives on ongoing thought recognise the heterogeneity of these self-generated states, we lack both a clear understanding of how to classify the specific states, and how they can be mapped empirically. In the current study, we capitalise on advances in machine learning that allow continuous neural data to be divided into a set of distinct temporally re-occurring patterns, or states. We applied this technique to a large set of resting state data in which we also acquired retrospective descriptions of the participants' experiences during the scan. We found that two of the identified states were predictive of patterns of thinking at rest. One state highlighted a pattern of neural activity commonly seen during demanding tasks, and the time individuals spent in this state was associated with descriptions of experience focused on problem solving in the future. A second state was associated with patterns of activity that are commonly seen under less demanding conditions, and the time spent in it was linked to reports of intrusive thoughts about the past. Finally, we found that these two neural states tended to fall at either end of a neural hierarchy that is thought to reflect the brain's response to cognitive demands. Together, these results demonstrate that approaches which take advantage of time-varying changes in neural function can play an important role in understanding the repertoire of self-generated states. Moreover, they establish that important features of self-generated ongoing experience are related to variation along a similar vein to those seen when the brain responds to cognitive task demands.
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http://dx.doi.org/10.1038/s41598-020-77336-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7712889PMC
December 2020

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

Cortex 2021 01 31;134:76-91. Epub 2020 Oct 31.

Department of Psychology, University of York, UK; York Neuroimaging Centre, Innovation Way, York, UK. Electronic address:

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.
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http://dx.doi.org/10.1016/j.cortex.2020.10.007DOI Listing
January 2021

A multi-scale cortical wiring space links cellular architecture and functional dynamics in the human brain.

PLoS Biol 2020 11 30;18(11):e3000979. Epub 2020 Nov 30.

Multimodal Imaging and Connectome Analysis Lab, McConnell Brain Imaging Centre, Montreal Neurological Institute and Hospital, McGill University, Montreal, Quebec, Canada.

The vast net of fibres within and underneath the cortex is optimised to support the convergence of different levels of brain organisation. Here, we propose a novel coordinate system of the human cortex based on an advanced model of its connectivity. Our approach is inspired by seminal, but so far largely neglected models of cortico-cortical wiring established by postmortem anatomical studies and capitalises on cutting-edge in vivo neuroimaging and machine learning. The new model expands the currently prevailing diffusion magnetic resonance imaging (MRI) tractography approach by incorporation of additional features of cortical microstructure and cortico-cortical proximity. Studying several datasets and different parcellation schemes, we could show that our coordinate system robustly recapitulates established sensory-limbic and anterior-posterior dimensions of brain organisation. A series of validation experiments showed that the new wiring space reflects cortical microcircuit features (including pyramidal neuron depth and glial expression) and allowed for competitive simulations of functional connectivity and dynamics based on resting-state functional magnetic resonance imaging (rs-fMRI) and human intracranial electroencephalography (EEG) coherence. Our results advance our understanding of how cell-specific neurobiological gradients produce a hierarchical cortical wiring scheme that is concordant with increasing functional sophistication of human brain organisation. Our evaluations demonstrate the cortical wiring space bridges across scales of neural organisation and can be easily translated to single individuals.
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http://dx.doi.org/10.1371/journal.pbio.3000979DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7728398PMC
November 2020

Convergence of cortical types and functional motifs in the human mesiotemporal lobe.

Elife 2020 11 4;9. Epub 2020 Nov 4.

Multimodal Imaging and Connectome Analysis Lab, McConnell Brain Imaging Centre, Montreal Neurological Institute and Hospital, McGill University, Montreal, Canada.

The mesiotemporal lobe (MTL) is implicated in many cognitive processes, is compromised in numerous brain disorders, and exhibits a gradual cytoarchitectural transition from six-layered parahippocampal isocortex to three-layered hippocampal allocortex. Leveraging an ultra-high-resolution histological reconstruction of a human brain, our study showed that the dominant axis of MTL cytoarchitectural differentiation follows the iso-to-allocortical transition and depth-specific variations in neuronal density. Projecting the histology-derived MTL model to in-vivo functional MRI, we furthermore determined how its cytoarchitecture underpins its intrinsic effective connectivity and association to large-scale networks. Here, the cytoarchitectural gradient was found to underpin intrinsic effective connectivity of the MTL, but patterns differed along the anterior-posterior axis. Moreover, while the iso-to-allocortical gradient parametrically represented the multiple-demand relative to task-negative networks, anterior-posterior gradients represented transmodal versus unimodal networks. Our findings establish that the combination of micro- and macrostructural features allow the MTL to represent dominant motifs of whole-brain functional organisation.
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http://dx.doi.org/10.7554/eLife.60673DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7671688PMC
November 2020

Missing the forest because of the trees: slower alternations during binocular rivalry are associated with lower levels of visual detail during ongoing thought.

Neurosci Conscious 2020 5;2020(1):niaa020. Epub 2020 Oct 5.

Department of Psychology, University of York, York YO10 5DD, UK.

Conscious awareness of the world fluctuates, either through variation in how vividly we perceive the environment, or when our attentional focus shifts away from information in the external environment towards information that we generate via imagination. Our study combined individual differences in experience sampling, psychophysical reports of perception and neuroimaging descriptions of structural connectivity to better understand these changes in conscious awareness. In particular, we examined (i) whether aspects of ongoing thought-indexed via multi-dimensional experience sampling during a sustained attention task-are associated with the white matter fibre organization of the cortex as reflected by their relative degree of anisotropic diffusion and (ii) whether these neurocognitive descriptions of ongoing experience are related to a more constrained measure of visual consciousness through analysis of bistable perception during binocular rivalry. Individuals with greater fractional anisotropy in right hemisphere white matter regions involving the inferior fronto-occipital fasciculus, the superior longitudinal fasciculus and the cortico-spinal tract, described their ongoing thoughts as lacking external details. Subsequent analysis indicated that the combination of low fractional anisotropy in these right hemisphere regions, with reports of thoughts with high levels of external details, was associated with the shortest periods of dominance during binocular rivalry. Since variation in binocular rivalry reflects differences between bottom-up and top-down influences on vision, our study suggests that reports of ongoing thoughts with vivid external details may occur when conscious precedence is given to bottom-up representation of perceptual information.
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http://dx.doi.org/10.1093/nc/niaa020DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7533427PMC
October 2020

Signal diffusion along connectome gradients and inter-hub routing differentially contribute to dynamic human brain function.

Neuroimage 2021 01 7;224:117429. Epub 2020 Oct 7.

Multimodal Imaging and Connectome Analysis Lab, McConnell Brain Imaging Centre, Montreal Neurological Institute and Hospital, McGill University, Montreal, Quebec, Canada. Electronic address:

Human cognition is dynamic, alternating over time between externally-focused states and more abstract, often self-generated, patterns of thought. Although cognitive neuroscience has documented how networks anchor particular modes of brain function, mechanisms that describe transitions between distinct functional states remain poorly understood. Here, we examined how time-varying changes in brain function emerge within the constraints imposed by macroscale structural network organization. Studying a large cohort of healthy adults (n = 326), we capitalized on manifold learning techniques that identify low dimensional representations of structural connectome organization and we decomposed neurophysiological activity into distinct functional states and their transition patterns using Hidden Markov Models. Structural connectome organization predicted dynamic transitions anchored in sensorimotor systems and those between sensorimotor and transmodal states. Connectome topology analyses revealed that transitions involving sensorimotor states traversed short and intermediary distances and adhered strongly to communication mechanisms of network diffusion. Conversely, transitions between transmodal states involved spatially distributed hubs and increasingly engaged long-range routing. These findings establish that the structure of the cortex is optimized to allow neural states the freedom to vary between distinct modes of processing, and so provides a key insight into the neural mechanisms that give rise to the flexibility of human cognition.
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http://dx.doi.org/10.1016/j.neuroimage.2020.117429DOI Listing
January 2021

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

Neuroimage 2021 01 28;224:117405. Epub 2020 Sep 28.

Department of Psychology, University of York, Heslington, York, UK, YO10 5DD. Electronic address:

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.
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http://dx.doi.org/10.1016/j.neuroimage.2020.117405DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7779371PMC
January 2021

Shaping brain structure: Genetic and phylogenetic axes of macroscale organization of cortical thickness.

Sci Adv 2020 Sep 25;6(39). Epub 2020 Sep 25.

Institute of Neuroscience and Medicine (INM-7: Brain and Behavior), Research Centre Jülich, Jülich, Germany.

The topology of the cerebral cortex has been proposed to provide an important source of constraint for the organization of cognition. In a sample of twins ( = 1113), we determined structural covariance of thickness to be organized along both a posterior-to-anterior and an inferior-to-superior axis. Both organizational axes were present when investigating the genetic correlation of cortical thickness, suggesting a strong genetic component in humans, and had a comparable organization in macaques, demonstrating they are phylogenetically conserved in primates. In both species, the inferior-superior dimension of cortical organization aligned with the predictions of dual-origin theory, and in humans, we found that the posterior-to-anterior axis related to a functional topography describing a continuum of functions from basic processes involved in perception and action to more abstract features of human cognition. Together, our study provides important insights into how functional and evolutionary patterns converge at the level of macroscale cortical structural organization.
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http://dx.doi.org/10.1126/sciadv.abb3417DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7518868PMC
September 2020

Distinct patterns of thought mediate the link between brain functional connectomes and well-being.

Netw Neurosci 2020 1;4(3):637-657. Epub 2020 Jul 1.

Department of Psychology, University of York, York, United Kingdom.

Ongoing thought patterns constitute important aspects of both healthy and abnormal human cognition. However, the neural mechanisms behind these daily experiences and their contribution to well-being remain a matter of debate. Here, using resting-state fMRI and retrospective thought sampling in a large neurotypical cohort ( = 211), we identified two distinct patterns of thought, broadly describing the participants' current concerns and future plans, that significantly explained variability in the individual functional connectomes. Consistent with the view that ongoing thoughts are an emergent property of multiple neural systems, network-based analysis highlighted the central importance of both unimodal and transmodal cortices in the generation of these experiences. Importantly, while state-dependent current concerns predicted better psychological health, mediating the effect of functional connectomes, trait-level future plans were related to better social health, yet with no mediatory influence. Collectively, we show that ongoing thoughts can influence the link between brain physiology and well-being.
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http://dx.doi.org/10.1162/netn_a_00137DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7462429PMC
July 2020

Toward a connectivity gradient-based framework for reproducible biomarker discovery.

Neuroimage 2020 12 1;223:117322. Epub 2020 Sep 1.

Center for Biomedical Imaging and Neuromodulation, Nathan Kline Institute, NY, USA. Electronic address:

Despite myriad demonstrations of feasibility, the high dimensionality of fMRI data remains a critical barrier to its utility for reproducible biomarker discovery. Recent efforts to address this challenge have capitalized on dimensionality reduction techniques applied to resting-state fMRI, identifying principal components of intrinsic connectivity which describe smooth transitions across different cortical systems, so called "connectivity gradients". These gradients recapitulate neurocognitively meaningful organizational principles that are present in both human and primate brains, and also appear to differ among individuals and clinical populations. Here, we provide a critical assessment of the suitability of connectivity gradients for biomarker discovery. Using the Human Connectome Project (discovery subsample=209; two replication subsamples= 209 × 2) and the Midnight scan club (n = 9), we tested the following key biomarker traits - reliability, reproducibility and predictive validity - of functional gradients. In doing so, we systematically assessed the effects of three analytical settings, including i) dimensionality reduction algorithms (i.e., linear vs. non-linear methods), ii) input data types (i.e., raw time series, [un-]thresholded functional connectivity), and iii) amount of the data (resting-state fMRI time-series lengths). We found that the reproducibility of functional gradients across algorithms and subsamples is generally higher for those explaining more variances of whole-brain connectivity data, as well as those having higher reliability. Notably, among different analytical settings, a linear dimensionality reduction (principal component analysis in our study), more conservatively thresholded functional connectivity (e.g., 95-97%) and longer time-series data (at least ≥20mins) was found to be preferential conditions to obtain higher reliability. Those gradients with higher reliability were able to predict unseen phenotypic scores with a higher accuracy, highlighting reliability as a critical prerequisite for validity. Importantly, prediction accuracy with connectivity gradients exceeded that observed with more traditional edge-based connectivity measures, suggesting the added value of a low-dimensional and multivariate gradient approach. Finally, the present work highlights the importance and benefits of systematically exploring the parameter space for new imaging methods before widespread deployment.
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http://dx.doi.org/10.1016/j.neuroimage.2020.117322DOI Listing
December 2020

Joint embedding: A scalable alignment to compare individuals in a connectivity space.

Neuroimage 2020 11 7;222:117232. Epub 2020 Aug 7.

Computational Imaging Research Lab, Department of Biomedical Imaging and Image-guided Therapy, Medical University of Vienna, Vienna, Austria; Computer Science and Artificial Intelligence Laboratory, Massachusetts Institute of Technology, Cambridge, MA, USA. Electronic address:

A common coordinate space enabling comparison across individuals is vital to understanding human brain organization and individual differences. By leveraging dimensionality reduction algorithms, high-dimensional fMRI data can be represented in a low-dimensional space to characterize individual features. Such a representative space encodes the functional architecture of individuals and enables the observation of functional changes across time. However, determining comparable functional features across individuals in resting-state fMRI in a way that simultaneously preserves individual-specific connectivity structure can be challenging. In this work we propose scalable joint embedding to simultaneously embed multiple individual brain connectomes within a common space that allows individual representations across datasets to be aligned. Using Human Connectome Project data, we evaluated the joint embedding approach by comparing it to the previously established orthonormal alignment model. Alignment using joint embedding substantially increased the similarity of functional representations across individuals while simultaneously capturing their distinct profiles, allowing individuals to be more discriminable from each other. Additionally, we demonstrated that the common space established using resting-state fMRI provides a better overlap of task-activation across participants. Finally, in a more challenging scenario - alignment across a lifespan cohort aged from 6 to 85 - joint embedding provided a better prediction of age (r2 = 0.65) than the prior alignment model. It facilitated the characterization of functional trajectories across lifespan. Overall, these analyses establish that joint embedding can simultaneously capture individual neural representations in a common connectivity space aligning functional data across participants and populations and preserve individual specificity.
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http://dx.doi.org/10.1016/j.neuroimage.2020.117232DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7779372PMC
November 2020

Neurocognitive patterns dissociating semantic processing from executive control are linked to more detailed off-task mental time travel.

Sci Rep 2020 07 17;10(1):11904. Epub 2020 Jul 17.

Department of Psychology, University of York, York, UK.

Features of ongoing experience are common across individuals and cultures. However, certain people express specific patterns of thought to a greater extent than others. Contemporary psychological theory assumes that individual differences in thought patterns occur because different types of experience depend on the expression of different neurocognitive processes. Consequently, individual variation in the underlying neurocognitive architecture is hypothesised to determine the ease with which certain thought patterns are generated or maintained. Our study (N = 178) tested this hypothesis using multivariate pattern analysis to infer shared variance among measures of cognitive function and neural organisation and examined whether these latent variables explained reports of the patterns of on-going thoughts people experienced in the lab. We found that relatively better performance on tasks relying primarily on semantic knowledge, rather than executive control, was linked to a neural functional organisation associated, via meta-analysis, with task labels related to semantic associations (sentence processing, reading and verbal semantics). Variability of this functional mode predicted significant individual variation in the types of thoughts that individuals experienced in the laboratory: neurocognitive patterns linked to better performance at tasks that required guidance from semantic representation, rather than those dependent on executive control, were associated with patterns of thought characterised by greater subjective detail and a focus on time periods other than the here and now. These relationships were consistent across different days and did not vary with level of task demands, indicating they are relatively stable features of an individual's cognitive profile. Together these data confirm that individual variation in aspects of ongoing experience can be inferred from hidden neurocognitive architecture and demonstrate that performance trade-offs between executive control and long-term semantic knowledge are linked to a person's tendency to imagine situations that transcend the here and now.
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http://dx.doi.org/10.1038/s41598-020-67605-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7368037PMC
July 2020

The relationship between individual variation in macroscale functional gradients and distinct aspects of ongoing thought.

Neuroimage 2020 10 22;220:117072. Epub 2020 Jun 22.

Department of Psychology, York Neuroimaging Centre, University of York, United Kingdom.

Contemporary accounts of ongoing thought recognise it as a heterogeneous and multidimensional construct, varying in both form and content. An emerging body of evidence demonstrates that distinct types of experience are associated with unique neurocognitive profiles, that can be described at the whole-brain level as interactions between multiple large-scale networks. The current study sought to explore the possibility that whole-brain functional connectivity patterns at rest may be meaningfully related to patterns of ongoing thought that occurred over this period. Participants underwent resting-state functional magnetic resonance imaging (rs-fMRI) followed by a questionnaire retrospectively assessing the content and form of their ongoing thoughts during the scan. A non-linear dimension reduction algorithm was applied to the rs-fMRI data to identify components explaining the greatest variance in whole-brain connectivity patterns. Using these data, we examined whether specific types of thought measured at the end of the scan were predictive of individual variation along the first three low-dimensional components of functional connectivity at rest. Multivariate analyses revealed that individuals for whom the connectivity of the sensorimotor system was maximally distinct from the visual system were most likely to report thoughts related to finding solutions to problems or goals and least likely to report thoughts related to the past. These results add to an emerging literature that suggests that unique patterns of experience are associated with distinct distributed neurocognitive profiles and highlight that unimodal systems may play an important role in this process.
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http://dx.doi.org/10.1016/j.neuroimage.2020.117072DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7573534PMC
October 2020

A gradient from long-term memory to novel cognition: Transitions through default mode and executive cortex.

Neuroimage 2020 10 20;220:117074. Epub 2020 Jun 20.

Department of Psychology, University of York, Heslington, York, YO10 5DD, United Kingdom. Electronic address:

Human cognition flexibly guides decision-making in familiar and novel situations. Although these decisions are often treated as dichotomous, in reality, situations are neither completely familiar, nor entirely new. Contemporary accounts of brain organization suggest that neural function is organized along a connectivity gradient from unimodal regions of sensorimotor cortex, through executive regions to transmodal default mode network. We examined whether this graded view of neural organization helps to explain how decision-making changes across situations that vary in their alignment with long-term knowledge. We used a semantic judgment task, which parametrically varied the global semantic similarity of items within a feature matching task to create a 'task gradient', from conceptual combinations that were highly overlapping in long-term memory to trials that only shared the goal-relevant feature. We found the brain's response to the task gradient varied systematically along the connectivity gradient, with the strongest response in default mode network when the probe and target items were highly overlapping conceptually. This graded functional change was seen in multiple brain regions and within individual brains, and was not readily explained by task difficulty. Moreover, the gradient captured the spatial layout of networks involved in semantic processing, providing an organizational principle for controlled semantic cognition across the cortex. In this way, the cortex is organized to support semantic decision-making in both highly familiar and less familiar situations.
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http://dx.doi.org/10.1016/j.neuroimage.2020.117074DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7573535PMC
October 2020

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

Cortex 2020 08 25;129:356-375. Epub 2020 May 25.

Department of Psychology, University of York, York, UK.

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.
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http://dx.doi.org/10.1016/j.cortex.2020.04.032DOI Listing
August 2020

Reductions in task positive neural systems occur with the passage of time and are associated with changes in ongoing thought.

Sci Rep 2020 06 18;10(1):9912. Epub 2020 Jun 18.

Department of Psychology, University of York, York, UK.

Cognition is dynamic and involves both the maintenance of and transitions between neurocognitive states. While recent research has identified some of the neural systems involved in sustaining task states, it is less well understood how intrinsic influences on cognition emerge over time. The current study uses fMRI and Multi-Dimensional Experience Sampling (MDES) to chart how cognition changes over time from moments in time when external attention was established. We found that the passage of time was associated with brain regions associated with external attention decreasing in activity over time. Comparing this pattern of activity to defined functional hierarchies of brain organization, we found that it could be best understood as movement away from systems involved in task performance. Moments where the participants described their thoughts as off-task showed a significant similarity to the task-negative end of the same hierarchy. Finally, the greater the similarity of a participant's neural dynamics to this hierarchy the faster their rate of increasing off-task thought over time. These findings suggest topographical changes in neural processing that emerge over time and those seen during off-task thought can both be understood as a common shift away from neural motifs seen during complex task performance.
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http://dx.doi.org/10.1038/s41598-020-66698-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7303126PMC
June 2020

The role of default mode network in semantic cue integration.

Neuroimage 2020 10 6;219:117019. Epub 2020 Jun 6.

Department of Psychology, University of York, UK. Electronic address:

Recent accounts of large-scale cortical organisation suggest that the default mode network (DMN) is positioned at the top of a principal gradient, reflecting the separation between heteromodal and unimodal sensory-motor regions in patterns of connectivity and in geodesic distance along the cortical surface (Margulies et al., 2016). This isolation of DMN from external inputs might allow the integration of disparate sources of information that can constrain subsequent cognition. We tested this hypothesis by manipulating the degree to which semantic decisions for ambiguous words (e.g. jam) were constrained by preceding visual cues depicting relevant spatial contexts (e.g. supermarket or road) and/or facial emotions (e.g. happy vs. frustrated). We contrasted (i) the effects of a single preceding cue with a no-cue condition employing scrambled images, and (ii) convergent spatial and emotion cues with single cues. Single cues elicited stronger activation in the multiple demand network relative to no cues, consistent with the requirement to maintain information in working memory. The availability of two convergent cues elicited stronger activation within DMN regions (bilateral angular gyrus, middle temporal gyrus, medial prefrontal cortex, and posterior cingulate), even though behavioural performance was unchanged by cueing - consequently task difficulty is unlikely to account for the observed differences in brain activation. A regions-of-interest analysis along the unimodal-to-heteromodal principal gradient revealed maximal activation for the convergent cue condition at the heteromodal end, corresponding to the DMN. Our findings are consistent with the view that regions of DMN support states of information integration that constrain ongoing cognition and provide a framework for understanding the location of these effects at the heteromodal end of the principal gradient.
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http://dx.doi.org/10.1016/j.neuroimage.2020.117019DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7443705PMC
October 2020

A role for the ventromedial prefrontal cortex in self-generated episodic social cognition.

Neuroimage 2020 09 22;218:116977. Epub 2020 May 22.

Department of Psychology and York Neuroimaging Centre, University of York, UK.

The human mind is equally fluent in thoughts that involve self-generated mental content as it is with information in the immediate environment. Previous research has shown that neural systems linked to executive control (i.e. the dorsolateral prefrontal cortex) are recruited when perceptual and self-generated thoughts are balanced in line with the demands imposed by the external world. Contemporary theories (Smallwood and Schooler, 2015) assume that differentiable processes are important for self-generated mental content than for its regulation. The current study used functional magnetic resonance imaging in combination with multidimensional experience sampling to address this possibility. We used a task with minimal demands to maximise our power at identifying correlates of self-generated states. Principal component analysis showed consistent patterns of self-generated thought when participants performed the task in either the lab or in the scanner (ICC ranged from 0.68 to 0.86). In a whole brain analyses we found that neural activity in the ventromedial prefrontal cortex (vMPFC) increases when participants are engaged in experiences which emphasise episodic and socio-cognitive features. Our study suggests that neural activity in the vMPFC is linked to patterns of ongoing thought, particularly those with episodic or social features.
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http://dx.doi.org/10.1016/j.neuroimage.2020.116977DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7422831PMC
September 2020

Word up - Experiential and neurocognitive evidence for associations between autistic symptomology and a preference for thinking in the form of words.

Cortex 2020 07 27;128:88-106. Epub 2020 Mar 27.

Department of Psychology, University of York, York, United Kingdom.

Autism symptomology has a profound impact on cognitive and affective functioning, yet we know relatively little about how it shapes patterns of ongoing thought. In an exploratory study in a large population of neurotypical individuals, we used experience sampling to characterise the relationship between ongoing cognition and self-reported autistic traits. We found that with increasing autistic symptom score, cognition was characterised by thinking more in words than images. Analysis of structural neuroimaging data found that autistic traits linked to social interaction were associated with greater cortical thickness in a region of lingual gyrus (LG) within the occipital cortex. Analysis of resting state functional neuroimaging data found autistic traits were associated with stronger connectivity between the LG and a region of motor cortex. Importantly, the strength of connectivity between the LG and motor cortex moderated the link between autistic symptoms and thinking in words: individuals showing higher connectivity showed a stronger association between autistic traits and thinking in words. Together we provide behavioural and neural evidence linking autistic traits to the tendency to think in words which may be rooted in underlying cortical organisation. These observations lay the groundwork for research into the form and content of self-generated thoughts in individuals with the established diagnosis of autism.
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http://dx.doi.org/10.1016/j.cortex.2020.02.019DOI Listing
July 2020