The disengagement deficit after right-hemisphere damage: Distinct roles of lateral frontal and parietal damage.

An influential model of spatial attention postulates three main attention-orienting mechanisms: disengagement, shifting, and engagement. Early research linked disengagement deficits with superior parietal damage, regardless of hemisphere or presence of spatial neglect. Subsequent studies supported the involvement of more ventral parietal regions, especially in the right hemisphere, and linked spatial neglect to deficient disengagement from ipsilateral cues. However, previous lesion studies faced serious limitations, such as small sample sizes and the lack of brain-injured controls without neglect. Additionally, some studies employed symbolic cues or used long cue-target intervals, which may fail to reveal impaired disengagement. We here used a machine-learning approach to conduct lesion-symptom mapping (LSM) on 89 patients with focal cerebral lesions to the left (LH) or right (RH) cerebral hemisphere. A group of 54 healthy participants served as controls. The paradigm used to uncover disengagement deficits employed non-predictive cues presented in the visual periphery and at short cue-target intervals, targeting exogenous attention. The main factors of interest were group (healthy participants, LH, RH), target position (left, right hemifield) and cue validity (valid, invalid). LSM-analyses were performed on two indices: the validity effect, computed as the absolute difference between reaction times (RTs) following invalid compared to valid cues, and the disengagement deficit, determined by the difference between contralesional and ipsilesional validity effects. While LH patients showed general slowing of RTs to contralesional targets, only RH patients exhibited a disengagement deficit from ipsilesional cues. LSM associated the validity effect with a right lateral frontal cluster, which additionally affected subcortical white matter of the right arcuate fasciculus, the corticothalamic pathway, and the superior longitudinal fasciculus. In contrast, the disengagement deficit was related to damage involving the right temporoparietal junction. Thus, our results support the crucial role of right inferior parietal and posterior temporal regions for attentional disengagement, but also emphasize the importance of lateral frontal regions, for the reorienting of attention.

Anatomical predictors of mental rotation with bodily and non-bodily stimuli: A lesion-symptom study.

Mental rotation (MR) is widely regarded as a quintessential example of an embodied cognitive process. This viewpoint stems from the functional parallels between MR and the physical rotation of tangible objects, as well as participants' inclination to employ motor-based strategies when tackling MR tasks involving bodily stimuli. These commonalities imply that MR may depend on brain regions crucial for the planning and execution of motor programs. However, there is disagreement regarding the anatomy of MR between findings from functional imaging and lesion studies involving brain-injured patients. The former indicate the involvement of the right-hemispheric parietal cortex, while the latter underscore the significance of posterior areas in the left hemisphere. In this study, we aimed to discern the neural underpinnings of MR using lesion-symptom mapping (LSM) for both bodily (hands) and non-bodily (letters) stimuli. Behavioral results from the two MR tasks revealed impaired MR of bodily stimuli in patients with left hemisphere damage. LSM results pinpointed the left primary motor and somatosensory cortices, along with the superior parietal lobule, as the anatomical substrates of MR for both bodily and non-bodily stimuli. Furthermore, damage to the left angular gyrus, supramarginal gyrus, supplementary motor area, and retrosplenial cortex was associated with MR of non-bodily stimuli. These findings support the causal involvement of the left hemisphere in MR and underscore the existence of a common anatomical substrate in brain regions pertinent to motor planning and execution.

How embodied is cognition? fMRI and behavioral evidence for common neural resources underlying motor planning and mental rotation of bodily stimuli.

Functional neuroimaging shows that dorsal frontoparietal regions exhibit conjoint activity during various motor and cognitive tasks. However, it is unclear whether these regions serve several, computationally independent functions, or underlie a motor "core process" that is reused to serve higher-order functions. We hypothesized that mental rotation capacity relies on a phylogenetically older motor process that is rooted within these areas. This hypothesis entails that neural and cognitive resources recruited during motor planning predict performance in seemingly unrelated mental rotation tasks. To test this hypothesis, we first identified brain regions associated with motor planning by measuring functional activations to internally-triggered vs externally-triggered finger presses in 30 healthy participants. Internally-triggered finger presses yielded significant activations in parietal, premotor, and occipitotemporal regions. We then asked participants to perform two mental rotation tasks outside the scanner, consisting of hands or letters as stimuli. Parietal and premotor activations were significant predictors of individual reaction times when mental rotation involved hands. We found no association between motor planning and performance in mental rotation of letters. Our results indicate that neural resources in parietal and premotor cortex recruited during motor planning also contribute to mental rotation of bodily stimuli, suggesting a common core component underlying both capacities.

Task-based functional connectivity identifies two segregated networks underlying intentional action.

While much of motor behavior is automatic, intentional action is necessary for the selection and initiation of controlled motor acts and is thus an essential part of goal-directed behavior. Neuroimaging studies have shown that self-generated action implicates several dorsal and ventral frontoparietal areas. However, knowledge of the functional coupling between these brain regions during intentional action remains limited. We here studied brain activations and functional connectivity (FC) of thirty right-handed healthy participants performing a finger pressing task instructed to use a specific finger (externally-triggered action) or to select one of four fingers randomly (internally-generated action). Participants performed the task in alternating order either with their dominant right hand or the left hand. Consistent with previous studies, we observed stronger involvement of posterior parietal cortex and premotor regions when contrasting internally-generated with externally-triggered action. Interestingly, this contrast also revealed significant engagement of medial occipitotemporal regions including the left lingual and right fusiform gyrus. Task-based FC analysis identified increased functional coupling among frontoparietal regions as well as increased and decreased coupling between occipitotemporal regions, thus differentiating between two segregated networks. When comparing results of the dominant and nondominant hand we found less activation, but stronger connectivity for the former, suggesting increased neural efficiency when participants use their dominant hand. Taken together, our results reveal that two segregated networks that encompass the frontoparietal and occipitotemporal cortex contribute independently to intentional action.

From Action to Cognition: Neural Reuse, Network Theory and the Emergence of Higher Cognitive Functions.

The aim of this article is to discuss the logic and assumptions behind the concept of neural reuse, to explore its biological advantages and to discuss the implications for the cognition of a brain that reuses existing circuits and resources. We first address the requirements that must be fulfilled for neural reuse to be a biologically plausible mechanism. Neural reuse theories generally take a developmental approach and model the brain as a dynamic system composed of highly flexible neural networks. They often argue against domain-specificity and for a distributed, embodied representation of knowledge, which sets them apart from modular theories of mental processes. We provide an example of reuse by proposing how a phylogenetically more modern mental capacity (mental rotation) may appear through the reuse and recombination of existing resources from an older capacity (motor planning). We conclude by putting arguments into context regarding functional modularity, embodied representation, and the current ontology of mental processes.

Discrete Patterns of Cross-Hemispheric Functional Connectivity Underlie Impairments of Spatial Cognition after Stroke.

Despite intense research, the neural correlates of stroke-induced deficits of spatial cognition remain controversial. For example, several cortical regions and white-matter tracts have been designated as possible anatomic predictors of spatial neglect. However, many studies focused on local anatomy, an approach that does not harmonize with the notion that brain-behavior relationships are flexible and may involve interactions among distant regions. We studied in humans of either sex resting-state fMRI connectivity associated with performance in line bisection, reading and visual search, tasks commonly used for he clinical diagnosis of neglect. We defined left and right frontal, parietal, and temporal areas as seeds (or regions of interest, ROIs), and measured whole-brain seed-based functional connectivity (FC) and ROI-to-ROI connectivity in subacute right-hemisphere stroke patients. Performance on the line bisection task was associated with decreased FC between the right fusiform gyrus and left superior occipital cortex. Complementary increases and decreases of connectivity between both temporal and occipital lobes predicted reading errors. In addition, visual search deficits were associated with modifications of FC between left and right inferior parietal lobes and right insular cortex. These distinct connectivity patterns were substantiated by analyses of FC between left- and right-hemispheric ROIs, which revealed that decreased interhemispheric and right intrahemispheric FC was associated with higher levels of impairment. Together, these findings indicate that intrahemispheric and interhemispheric cooperation between brain regions lying outside the damaged area contributes to spatial deficits in a way that depends on the different cognitive components recruited during reading, spatial judgments, and visual exploration.SIGNIFICANCE STATEMENT Focal damage to the right cerebral hemisphere may result in a variety of deficits, often affecting the domain of spatial cognition. The neural correlates of these disorders have traditionally been studied with lesion-symptom mapping, but this method fails to capture the network dynamics that underlie cognitive performance. We studied functional connectivity in patients with right-hemisphere stroke and found a pattern of correlations between the left and right temporo-occipital, inferior parietal, and right insular cortex that were distinctively predictive of deficits in reading, spatial judgment, and visual exploration. This finding reveals the importance of interhemispheric interactions and network adaptations for the manifestation of spatial deficits after damage to the right hemisphere.

Modulating functional connectivity after stroke with neurofeedback: Effect on motor deficits in a controlled cross-over study.

Synchronization of neural activity as measured with functional connectivity (FC) is increasingly used to study the neural basis of brain disease and to develop new treatment targets. However, solid evidence for a causal role of FC in disease and therapy is lacking. Here, we manipulated FC of the ipsilesional primary motor cortex in ten chronic human stroke patients through brain-computer interface technology with visual neurofeedback. We conducted a double-blind controlled crossover study to test whether manipulation of FC through neurofeedback had a behavioral effect on motor performance. Patients succeeded in increasing FC in the motor cortex. This led to improvement in motor function that was significantly greater than during neurofeedback training of a control brain area and proportional to the degree of FC enhancement. This result provides evidence that FC has a causal role in neurological function and that it can be effectively targeted with therapy.