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Disruption of functional organization within the primary motor cortex in children with autism.

ABSTRACT: Accumulating evidence suggests that motor impairments are prevalent in autism spectrum disorder (ASD), relate to the social and communicative deficits at the core of the diagnosis and may reflect abnormal connectivity within brain networks underlying motor control and learning. Parcellation of resting-state functional connectivity data using spectral clustering approaches has been shown to be an effective means of visualizing functional organization within the brain but has most commonly been applied to explorations of normal brain function. This article presents a parcellation of a key area of the motor network, the primary motor cortex (M1), a key area of the motor control network, in adults, typically developing (TD) children and children with ASD and introduces methods for selecting the number of parcels, matching parcels across groups and testing group differences. The parcellation is based solely on patterns of connectivity between individual M1 voxels and all voxels outside of M1, and within all groups, a gross dorsomedial to ventrolateral organization emerged within M1 which was left-right symmetric. Although this gross organizational scheme was present in both groups of children, statistically significant group differences in the size and segregation of M1 parcels within regions of the motor homunculus corresponding to the upper and lower limbs were observed. Qualitative comparison of the M1 parcellation for children with ASD with that of younger and older TD children suggests that these organizational differences, with a lack of differentiation between lower limb/trunk regions and upper limb/hand regions, may be due, at least in part, to a delay in functional specialization within the motor cortex.

SUBMITTER: Nebel MB

PROVIDER: S-EPMC3864146 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The integration of sensory inputs in the motor cortex is crucial for dexterous movement. We recently demonstrated that a closed-loop control based on the feedback provided through intraneural multichannel electrodes implanted in the median and ulnar nerves of a participant with upper limb amputation improved manipulation skills and increased prosthesis embodiment. Here we assessed, in the same participant, whether and how selective intraneural sensory stimulation also elicits a measurable cortical activation and affects sensorimotor cortical circuits. After estimating the activation of the primary somatosensory cortex evoked by intraneural stimulation, sensorimotor integration was investigated by testing the inhibition of primary motor cortex (M1) output to transcranial magnetic stimulation, after both intraneural and perineural stimulation. Selective sensory intraneural stimulation evoked a low-amplitude, 16 ms-latency, parietal response in the same area of the earliest component evoked by whole-nerve stimulation, compatible with fast-conducting afferent fibre activation. For the first time, we show that the same intraneural stimulation was also capable of decreasing M1 output, at the same time range of the short-latency afferent inhibition effect of whole-nerve superficial stimulation. The inhibition generated by the stimulation of channels activating only sensory fibres was stronger than that due to intraneural or perineural stimulation of channels activating mixed fibres. We demonstrate in a human subject that the cortical sensorimotor integration inhibiting M1 output previously described after the experimental whole-nerve stimulation is present also with a more ecological selective sensory fibre stimulation. KEY POINTS: Cortical integration of sensory inputs is crucial for dexterous movement. Short-latency somatosensory afferent inhibition of motor cortical output is typically produced by peripheral whole-nerve stimulation. We exploited intraneural multichannel electrodes used to provide sensory feedback for prosthesis control to assess whether and how selective intraneural sensory stimulation affects sensorimotor cortical circuits in humans. Activation of the primary somatosensory cortex (S1) was explored by recording scalp somatosensory evoked potentials. Sensorimotor integration was tested by measuring the inhibitory effect of the afferent stimulation on the output of the primary motor cortex (M1) generated by transcranial magnetic stimulation. We demonstrate in humans that selective intraneural sensory stimulation elicits a measurable activation of S1 and that it inhibits the output of M1 at the same time range of whole-nerve superficial stimulation.

Project description:Previous research suggests that meaning-laden gestures, even when produced in the absence of language (i.e., pantomimed gestures), influence lexical retrieval. Yet, little is known about the neural mechanisms that underlie this process. Based on embodied cognition theories, many studies have demonstrated motor cortex involvement in the representation of action verbs and in the understanding of actions. The present study aimed to investigate whether the motor system plays a critical role in the behavioral influence of pantomimed gestures on action naming. Continuous theta burst stimulation (cTBS) was applied over the hand area of the left primary motor cortex and to a control site (occipital cortex). An action-picture naming task followed cTBS. In the naming task, participants named action pictures that were preceded by videos of congruent pantomimed gestures, unrelated pantomimed gestures or a control video with no movement (as a neutral, non-gestural condition). In addition to behavioral measures of performance, cTBS-induced changes in corticospinal activity were assessed. We replicated previous finding that exposure to congruent pantomimed gestures facilitates word production, compared to unrelated or neutral primes. However, we found no evidence that the left primary motor area is crucially involved in the mechanism underlying behavioral facilitation effects of gesture on verb production. Although, at the group level, cTBS induced motor cortex suppression, at the individual level we found remarkable variability of cTBS effects on the motor cortex. We found cTBS induction of both inhibition of corticospinal activity (with slower behavioral of responses) and enhancement (with faster behavioral responses). Our findings cast doubt on assumptions that the motor cortex is causally involved in the impact of gestures on action-word processing. Our results also highlight the importance of careful consideration of interindividual variability for the interpretation of cTBS effects.

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Disruption of functional organization within the primary motor cortex in children with autism.

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