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Mattingley, J. B.

Publications and source records attributed to Mattingley, J. B..

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Increased cognitive complexity reveals abnormal brain network activity in individuals with corpus callosum dysgenesis

Cognitive reasoning is thought to require functional interactions between whole-brain networks. Such networks rely on both cerebral hemispheres, with the corpus callosum providing cross-hemispheric communication. Here we used high-field functional magnetic resonance imaging (7T fMRI), a well validated cognitive task, and brain network analyses to investigate the functional networks underlying cognitive reasoning in individuals with corpus callosum dysgenesis (CCD), an anatomical abnormality that affects the corpus callosum. Participants with CCD were asked to solve cognitive reasoning problems while their brain activity was measured using fMRI. The complexity of these problems was parametrically varied by changing the complexity of relations that needed to be established between shapes within each problem matrix. Behaviorally, participants showed a typical reduction in task performance as problem complexity increased. Task-evoked neural activity was observed in brain regions known to constitute two key cognitive control systems: the fronto-parietal and cingulo-opercular networks. Under low complexity demands, network topology and the patterns of local neural activity in the CCD group closely resembled those observed in neurotypical controls. By contrast, when asked to solve more complex problems, participants with CCD showed a reduction in neural activity and connectivity within the fronto-parietal network. These complexity-induced, as opposed to resting-state, differences in functional network activity help resolve the apparent paradox between preserved network architecture found at rest in CCD individuals, and the heterogeneous deficits they display in response to cognitive task demands [preprint: https://doi.org/10.1101/312629].

neuroscience

An afferent subcortical white matter pathway to the amygdala facilitates fear recognition

Our ability to rapidly detect threats is thought to be subserved by a subcortical pathway that quickly conveys visual information to the amygdala. This neural shortcut has been demonstrated in animals but has rarely been shown in the human brain. Importantly, it remains unclear whether such a pathway might influence neural activity and behaviour. We conducted a multimodal neuroimaging study of 622 participants from the Human Connectome Project. We applied probabilistic tractography to diffusion-weighted images, reconstructing a subcortical pathway to the amygdala from the superior colliculus via the pulvinar. We then computationally modelled the flow of neural activity during a face-viewing task and found strong evidence for a functionally-afferent subcortical pathway. Critically, individuals with greater fibre density in this pathway also had stronger dynamic coupling and enhanced fearful face recognition. Our findings provide converging evidence for the recruitment of an afferent subcortical route to the amygdala in the human brain that facilitates fear recognition.

neuroscience

Flexible information coding in frontoparietal cortex across the functional stages of cognitive processing.

Neural activity in frontoparietal cortex shows overlap across cognitive domains and has been proposed to reflect flexible information processing according to current task demands (Dosenbach et al., 2007; Duncan, 2001). However, a strong assertion of flexibility requires investigating activity across stages of cognitive processing. The current study assessed neural activity in Multiple Demand (MD) regions across the stages of processing that form the core of long-standing cognitive models (Welford, 1952). Specifically, many complex tasks share a comparable structure of subsequent operations: target selection, stimulus-response (SR) mapping, and response execution. We independently manipulated the difficulty of target selection and SR mapping in identical stimulus displays and assessed changes in frontoparietal activity with increased demands in either stage. The results confirmed flexibility in MD regions, with enhanced information representation during difficult target selection as well as SR mapping. Additionally, anterior insula (AI) and anterior cingulate cortex (ACC) showed preferential representation of SR stage information, whereas the medial frontal gyrus (MFG) and inferior parietal sulcus (IPS) showed preferential representation of target selection-stage information. Together these results suggest that MD regions dynamically alter the information they represent with changing task demands. This is the first study to demonstrate that MD regions support flexible goal-directed cognition across multiple processing stages. At the same time we show a preference for the representation of information from a specific processing stage in a subset of MD regions.\n\nSignificance StatementGoal-directed cognition in complex tasks is critical to key life outcomes including longevity and academic performance. Nevertheless, the mechanisms underlying cognition in complex tasks are not well understood. Distinct neural networks are critical to the navigation of specific cognitive domains (e.g. attention), but frontoparietal activity shows cross-domain and -task overlap and supports flexible representation of goal-critical information. This study links flexible frontoparietal processing to longstanding models of meta-cognition that propose a unifying structure of operations underlying most tasks: target selection, SR mapping, and response execution. Our results demonstrate that flexible information representation in frontoparietal cortex is not limited to the SR mapping stage, but applies across the functional stages of cognitive processing, thus maximizing neural efficiency and supporting flexible cognition.

neuroscience

Prediction Error and Repetition Suppression Have Distinct Effects on Neural Representations of Visual Information

Predictive coding theories argue that recent experience establishes expectations in the brain that generate prediction errors when violated. Prediction errors provide a possible explanation for repetition suppression, where evoked neural activity is attenuated across repeated presentations of the same stimulus. The predictive coding account argues repetition suppression arises because repeated stimuli are expected, whereas non-repeated stimuli are unexpected and thus elicit larger neural responses. Here we employed electroencephalography in humans to test the predictive coding account of repetition suppression by presenting sequences of visual gratings with orientations that were expected either to repeat or change in separate blocks of trials. We applied multivariate forward modelling to determine how orientation selectivity was affected by repetition and prediction. Unexpected stimuli were associated with significantly enhanced orientation selectivity, whereas selectivity was unaffected for repeated stimuli. Our results suggest that repetition suppression and expectation have separable effects on neural representations of visual feature information.

neuroscience

Reconfiguration of brain network architectures between resting state and complexity-dependent cognitive reasoning

Our capacity for higher cognitive reasoning has a measureable limit. This limit is thought to arise from the brains capacity to flexibly reconfigure interactions between spatially distributed networks. Recent work, however, has suggested that reconfigurations of task-related networks are modest when compared with intrinsic resting state network architecture. Here we combined resting state and task-driven functional magnetic resonance imaging to examine how flexible, task-specific reconfigurations associated with increasing reasoning demands are integrated within a stable intrinsic brain topology. Human participants (21 males and 28 females) underwent an initial resting state scan, followed by a cognitive reasoning task involving different levels of complexity, followed by a second resting state scan. The reasoning task required participants to deduce the identity of a missing element in a 4 x 4 matrix, and item difficulty was scaled parametrically as determined by relational complexity theory. Analyses revealed that external task engagement was characterized by a significant change in functional brain modules. Specifically, resting state and null-task demand conditions were associated with more segregated brain network topology, whereas increases in reasoning complexity resulted in merging of resting state modules. Further increments in task complexity did not change the established modular architecture, but impacted selective patterns of connectivity between fronto-parietal, subcortical, cingulo-opercular and default-mode networks. Larger increases in network efficiency within the newly established task modules were associated with higher reasoning accuracy. Our results shed light on the network architectures that underlie external task engagement, and highlight selective changes in brain connectivity supporting increases in task complexity.\n\nSignificance StatementHumans have clear limits in their ability to solve complex reasoning problems. It is thought that such limitations arise from flexible, moment-to-moment reconfigurations of functional brain networks. It is less clear how such task-driven adaptive changes in connectivity relate to stable, intrinsic networks of the brain and behavioral performance. We found that increased reasoning demands rely on selective patterns of connectivity within cortical networks that emerged in addition to a more general, task-induced modular architecture. This task-driven architecture reverted to a more segregated resting state architecture both immediately before and after the task. These findings reveal how flexibility in human brain networks is integral to achieving successful reasoning performance across different levels of cognitive demand.

neuroscience

Neurobehavioral dynamics of drowsiness

Transcranial magnetic stimulation (TMS) has been widely used in human cognitive neuroscience to examine the causal role of distinct cortical areas in perceptual, cognitive and motor functions. However, it is widely acknowledged that the effects of focal cortical stimulation on behaviour can vary substantially between participants and even from trial to trial within individuals. Here we asked whether spontaneous fluctuations in alertness can account for the variability in behavioural and neurophysiological responses to TMS. We combined single-pulse TMS with neural recording via electroencephalography (EEG) to quantify changes in motor and cortical reactivity with fluctuating levels of alertness defined objectively on the basis of ongoing brain activity. We observed rapid, non-linear changes in TMS-evoked neural responses - specifically, motor evoked potentials and TMS-evoked cortical potentials - as EEG activity indicated decreasing levels of alertness, even while participants remained awake and responsive in the behavioural task.\n\nIMPACT STATEMENTA substantial proportion of inter-trial variability in neurophysiological responses to TMS is due to spontaneous fluctuations in alertness, which should be controlled for during experimental and clinical applications of TMS.

neuroscience

Neural decoding of visual stimuli varies with fluctuations in global network efficiency

Functional magnetic resonance imaging (fMRI) studies have shown that neural activity fluctuates spontaneously between different states of global synchronization over a timescale of several seconds. Such fluctuations generate transient states of high and low correlation across distributed cortical areas. It has been hypothesized that such fluctuations in global efficiency might alter patterns of activity in local neuronal populations elicited by changes in incoming sensory stimuli. To test this prediction, we used a linear decoder to discriminate patterns of neural activity elicited by face and motion stimuli presented periodically while participants underwent time-resolved fMRI. As predicted, decoding was reliably higher during states of high global efficiency than during states of low efficiency, and this difference was evident across both visual and non-visual cortical regions. The results indicate that slow fluctuations in global network efficiency are associated with variations in the pattern of activity across widespread cortical regions responsible for representing distinct categories of visual stimulus. More broadly, the findings highlight the importance of understanding the impact of global fluctuations in functional connectivity on specialised, stimulus driven neural processes.

neuroscience

Spatial Attention Enhances the Neural Representation of Invisible Signals Embedded in Noise

Recent evidence suggests that voluntary spatial attention can affect neural processing of visual stimuli that do not enter conscious awareness (i.e. invisible stimuli), supporting the notion that attention and awareness are dissociable processes (Watanabe et al., 2011; Wyart, Dehaene, & Tallon-Baudry, 2012). To date, however, no study has demonstrated that these effects reflect enhancement of the neural representation of invisible stimuli per se, as opposed to other neural processes not specifically tied to the stimulus in question. In addition, it remains unclear whether spatial attention can modulate neural representations of invisible stimuli in direct competition with highly salient and visible stimuli. Here we developed a novel electroencephalography (EEG) frequency-tagging paradigm to obtain a continuous readout of human brain activity associated with visible and invisible signals embedded in dynamic noise. Participants (N = 23) detected occasional contrast changes in one of two flickering image streams on either side of fixation. Each image stream contained a visible or invisible signal embedded in every second noise image, the visibility of which was titrated and checked using a two-interval forced-choice detection task. Steady-state visual-evoked potentials (SSVEPs) were computed from EEG data at the signal and noise frequencies of interest. Cluster-based permutation analyses revealed significant neural responses to both visible and invisible signals across posterior scalp electrodes. Control analyses revealed that these responses did not reflect a subharmonic response to noise stimuli. In line with previous findings, spatial attention increased the neural representation of visible signals. Crucially, spatial attention also increased the neural representation of invisible signals. As such, the present results replicate and extend previous studies by demonstrating that attention can modulate the neural representation of invisible signals that are in direct competition with highly salient masking stimuli.

neuroscience

Structural and functional brain changes following four weeks of unimanual motor training: evidence from behaviour, neural stimulation, cortical thickness and functional MRI

Although different aspects of neuroplasticity can be quantified with behavioural probes, brain stimulation, and brain imaging assessments, no study to date has combined all these approaches into one comprehensive assessment of brain plasticity. Here, 24 healthy right-handed participants practised a sequence of finger-thumb opposition movements for 10 minutes each day with their left hand. After four weeks, performance for the practised sequence improved significantly (p < 0.05 FWE) relative to a matched control sequence, with both the left (mean increase: 53.0% practised, 6.5% control) and right (21.0%; 15.8%) hands. Training also induced significant (cluster p-FWE < 0.001) reductions in functional MRI activation for execution of the learned sequence, relative to the control sequence. These changes were observed as clusters in the premotor and supplementary motor cortices (right hemisphere, 301 voxel cluster; left hemisphere 700 voxel cluster), as well as sensorimotor cortices and superior parietal lobules (right hemisphere 864 voxel cluster; left hemisphere, 1947 voxel cluster). Transcranial magnetic stimulation over the right ( trained) primary motor cortex yielded a 58.6% mean increase in a measure of motor evoked potential amplitude, as recorded at the left abductor pollicis brevis muscle. Cortical thickness analyses based on structural MRI suggested changes in the right precentral gyrus, right post central gyrus, right dorsolateral prefrontal cortex and potentially the right supplementary motor area. Such findings are consistent with LTP-like neuroplastic changes in areas that were already responsible for finger sequence execution, rather than improved recruitment of previously non-utilised tissue.

neuroscience

Structural and functional brain changes following four weeks of unimanual motor training: evidence from fMRI-guided diffusion MRI tractography

We have reported reliable changes in behaviour, brain structure and function in 24 healthy right-handed adults who practiced a finger-thumb opposition sequence task with their left hand for 10 mins daily, over four weeks. Here we extend these findings by employing diffusion MRI to investigate white-matter changes in the corticospinal tract, basal-ganglia, and connections of the dorsolateral prefrontal cortex. Twenty-three participant datasets were available with pre-training and post-training scans. Task performance improved in all participants (mean: 52.8%, SD: 20.0%; group p<0.01 FWE) and widespread microstructural changes were detected across the motor system of the trained hemisphere. Specifically, region-of-interest based analyses of diffusion MRI (n=21) revealed significantly increased fractional anisotropy in the right caudate nucleus (4.9%; p<0.05 FWE), and decreased mean diffusivity in the left nucleus accumbens (-1.3%; p<0.05 FWE). Diffusion MRI tractography (n=22), seeded by sensorimotor cortex fMRI activation, also revealed increased fractional anisotropy in the right corticomotor tract (mean 3.28%; p<0.05 FWE) predominantly reflecting decreased radial diffusivity. These changes were consistent throughout the entire length of the tract. The left corticomotor tract did not show any changes. FA also increased in white matter connections between the right middle frontal gyrus and both right caudate nucleus (17/22 participants; p<0.05 FWE) and right supplementary motor area (18/22 participants; p<0.05 FWE). Equivalent changes in FA were not seen in the left ( non-trained) hemisphere. In combination with our functional and structural findings, this study provides detailed, multifocal evidence for widespread neuroplastic changes in the human brain resulting from motor training.

neuroscience