Abstract The degree to which mental representations of the body can be established and maintained without somatosensory input remains unclear. We contrast two “deafferented” adults, one who acquired large fibre sensory loss as an adult (IW) and another who was born without somatosensation (KS). We compared their responses to those of matched controls in three perceptual tasks: first accuracy of their mental image of their hands (assessed by testing recognition of correct hand length/width ratio in distorted photographs and by locating landmarks on the unseen hand); then accuracy of arm length judgements (assessed by judgement of reaching distance), and finally, we tested for an attentional bias towards peri-personal space (assessed by reaction times to visual target presentation). We hypothesised that IW would demonstrate responses consistent with him accessing conscious knowledge, whereas KS might show evidence of responses dependent on non-conscious mechanisms. In the first two experiments, both participants were able to give consistent responses about hand shape and arm length, but IW displayed a better awareness of hand shape than KS (and controls). KS demonstrated poorer spatial accuracy in reporting hand landmarks than both IW and controls, and appears to have less awareness of her hands. Reach distance was overestimated by both IW and KS, as it was for controls; the precision of their judgements was slightly lower than that of the controls. In the attentional task, IW showed no reaction time differences across conditions in the visual detection task, unlike controls, suggesting that he has no peri-personal bias of attention. In contrast, KS did show target location-dependent modulation of reaction times, when her hands were visible. We suggest that both IW and KS can access a conscious body image, although its accuracy may reflect their different experience of hand action. Acquired sensory loss has deprived IW of any subconscious body awareness, but the congenital absence of somatosensation may have led to its partial replacement by a form of visual proprioception in KS.
Neuroimaging studies have improved our understanding of which brain structures are involved in motor learning. Despite this, questions remain regarding the areas that contribute consistently across paradigms with different task demands. For instance, sensorimotor tasks focus on learning novel movement kinematics and dynamics, while serial response time task (SRTT) variants focus on sequence learning. These differing task demands are likely to elicit quantifiably different patterns of neural activity on top of a potentially consistent core network. The current study identified consistent activations across 70 motor learning experiments using activation likelihood estimation (ALE) meta-analysis. A global analysis of all tasks revealed a bilateral cortical-subcortical network consistently underlying motor learning across tasks. Converging activations were revealed in the dorsal premotor cortex, supplementary motor cortex, primary motor cortex, primary somatosensory cortex, superior parietal lobule, thalamus, putamen and cerebellum. These activations were broadly consistent across task specific analyses that separated sensorimotor tasks and SRTT variants. Contrast analysis indicated that activity in the basal ganglia and cerebellum was significantly stronger for sensorimotor tasks, while activity in cortical structures and the thalamus was significantly stronger for SRTT variants. Additional conjunction analyses then indicated that the left dorsal premotor cortex was activated across all analyses considered, even when controlling for potential motor confounds. The highly consistent activation of the left dorsal premotor cortex suggests it is a critical node in the motor learning network.
SummaryFunctionally related brain networks are engaged even in the absence of an overt behavior. The role of this resting state activity, evident as low-frequency fluctuations of BOLD (see [1] for review, [2–4]) or electrical [5, 6] signals, is unclear. Two major proposals are that resting state activity supports introspective thought or supports responses to future events [7]. An alternative perspective is that the resting brain actively and selectively processes previous experiences [8]. Here we show that motor learning can modulate subsequent activity within resting networks. BOLD signal was recorded during rest periods before and after an 11 min visuomotor training session. Motor learning but not motor performance modulated a fronto-parietal resting state network (RSN). Along with the fronto-parietal network, a cerebellar network not previously reported as an RSN was also specifically altered by learning. Both of these networks are engaged during learning of similar visuomotor tasks [9–22]. Thus, we provide the first description of the modulation of specific RSNs by prior learning—but not by prior performance—revealing a novel connection between the neuroplastic mechanisms of learning and resting state activity. Our approach may provide a powerful tool for exploration of the systems involved in memory consolidation.
Late in his life Rodin produced many thousand “instant drawings.” He asked models to make natural energetic movements, and he would draw them at high speed without looking at his hand or paper. To help understand his “blind drawing” process, the authors tracked the eye and hand movements of art students while they drew blind, copying complex lines presented to them as static images. The study found that line shape was correctly reproduced, but scaling could show major deficiencies not seen in Rodin's sketches. The authors propose that Rodin's direct vision-to-motor strategy, coupled with his high expertise, allowed him to accurately depict in one sweep the entire model, without “thoughts arresting the flow of sensations.”
SummaryThe human cerebellum plays an important role in language, amongst other cognitive and motor functions [1], but a unifying theoretical framework about cerebellar language function is lacking. In an established model of motor control, the cerebellum is seen as a predictive machine, making short-term estimations about the outcome of motor commands. This allows for flexible control, on-line correction, and coordination of movements [2]. The homogeneous cytoarchitecture of the cerebellar cortex suggests that similar computations occur throughout the structure, operating on different input signals and with different output targets [3]. Several authors have therefore argued that this 'motor' model may extend to cerebellar nonmotor functions [3–5], and that the cerebellum may support prediction in language processing [6]. However, this hypothesis has never been directly tested. Here, we used the 'Visual World' paradigm [7], where on-line processing of spoken sentence content can be assessed by recording the latencies of listeners' eye movements towards objects mentioned. Repetitive transcranial magnetic stimulation (rTMS) was used to disrupt function in the right cerebellum, a region implicated in language [8]. After cerebellar rTMS, listeners showed delayed eye fixations to target objects predicted by sentence content, while there was no effect on eye fixations in sentences without predictable content. The prediction deficit was absent in two control groups. Our findings support the hypothesis that computational operations performed by the cerebellum may support prediction during both motor control and language processing.
Abstract The oculomotor and spatial attention systems are interconnected. Whereas a link between motor commands and spatial shifts in visual attention is demonstrated, it is still unknown whether the recently discovered proprioceptive signal in somatosensory cortex impacts on visual attention, too. This study investigated whether visual targets near the perceived direction of gaze are detected more accurately than targets further away, despite the equal eccentricity of their retinal projections. We dissociated real and perceived eye position using left somatosensory repetitive transcranial magnetic stimulation (rTMS), which decreases cortical processing of eye muscle proprioceptive inflow and produces an underestimation of the rotation of the right eye. Participants detected near-threshold visual targets presented in the left or right visual hemifield at equal distance from fixation. We have previously shown that when the right eye is rotated to the left of the parasagittal plane, TMS produces an underestimation of this rotation, shifting perceived eye position to the right. Here we found that, in this condition, TMS also decreased target detection in the left visual hemifield and increased it in the right. This effect depended on the direction of rotation of the right eye. When the right eye was rotated rightward and TMS, we assume, shifted perceived gaze direction in opposite direction, leftward, visual accuracy decreased now in the right hemifield. We suggest that the proprioceptive eye position signal modulates the spatial distribution of visual processing resources, producing “pseudo-neglect” for objects located far relative to near the perceived direction of gaze.
Abstract Transcranial direct current stimulation (tDCS) is attracting increasing interest as a potential therapeutic route for unresponsive patients with prolonged disorders of consciousness (PDOC). However, research to date has had mixed results. Here, we propose a new direction by directly addressing the mechanisms underlying lack of responsiveness in PDOC, and using these to define our targets and the success of our intervention in the healthy brain first. We report 2 experiments that assess whether tDCS to the primary motor cortex (M1-tDCS; Experiment 1 ) and the cerebellum (cb-tDCS; Experiment 2 ) administered at rest modulate thalamo-cortical coupling in a subsequent command following task typically used to clinically assess awareness. Both experiments use sham- and polarity-controlled, randomised, double-blind, crossover designs. In Experiment 1 , 22 participants received anodal, cathodal, and sham M1-tDCS sessions while in the MRI scanner. A further 22 participants received the same protocol with cb-tDCS in Experiment 2 . We use Dynamic Causal Modelling of fMRI to characterise the effects of tDCS on brain activity and dynamics during simple thumb movements in response to command. We found that M1-tDCS increased thalamic excitation and that Cathodal cb-tDCS increased excitatory coupling from thalamus to M1. All these changes were polarity specific. Combined, our experiments demonstrate that tDCS can successfully modulate long range thalamo-cortical dynamics during command following via targeting of cortical regions. This suggests that M1- and cb-tDCS may allow PDOC patients to overcome the motor deficits at the root of their reduced responsiveness, improving their rehabilitation options and quality of life as a result.