The neural antecedents to voluntary action: Response to commentaries

Cognitive neuroscience must attend to the conceptual coherence of its hypotheses as well as to their empirical support. Examining the most influential studies of the neural antecedents to voluntary action, our Discussion Paper sought to identify the real-world consequences of neglecting the former in what we argued has been too narrow a pursuit of the latter. Though conceptual in form, our analysis is sharply empirical in its conclusions, revealing what have long been thought to be momentous experimental observations-such as the readiness potential-as the outcome of previously unidentified confounds that rob them of significance. Conversely, we suggested that experimental studies of two-way control, amongst other defining features of the voluntary, have been given less emphasis than the subject demands. Here, we ramify our analysis down the paths identified by others in the commentaries we received

The Neuroanatomical Correlates of Training-Related Perceptuo-Reflex Uncoupling in Dancers

Sensory input evokes low-order reflexes and higher-order perceptual responses. Vestibular stimulation elicits vestibular-ocular reflex (VOR) and self-motion perception (e.g., vertigo) whose response durations are normally equal. Adaptation to repeated whole-body rotations, for example, ballet training, is known to reduce vestibular responses. We investigated the neuroanatomical correlates of vestibular perceptuo-reflex adaptation in ballet dancers and controls. Dancers' vestibular-reflex and perceptual responses to whole-body yaw-plane step rotations were: (1) Briefer and (2) uncorrelated (controls' reflex and perception were correlated). Voxel-based morphometry showed a selective gray matter (GM) reduction in dancers' vestibular cerebellum correlating with ballet experience. Dancers' vestibular cerebellar GM density reduction was related to shorter perceptual responses (i.e. positively correlated) but longer VOR duration (negatively correlated). Contrastingly, controls' vestibular cerebellar GM density negatively correlated with perception and VOR. Diffusion-tensor imaging showed that cerebral cortex white matter (WM) microstructure correlated with vestibular perception but only in controls. In summary, dancers display vestibular perceptuo-reflex dissociation with the neuronatomical correlate localized to the vestibular cerebellum. Controls' robust vestibular perception correlated with a cortical WM network conspicuously absent in dancers. Since primary vestibular afferents synapse in the vestibular cerebellum, we speculate that a cerebellar gating of perceptual signals to cortical regions mediates the training-related attenuation of vestibular perception and perceptuo-reflex uncoupling

Neurodevelopmental Disorders: Sensing Tourette's Tics Away

Though still shrouded in mystery, Gilles de la Tourette’s syndrome is widely regarded as an archetypal neurodevelopmental disorder of central, motor control. New evidence that its cardinal manifestation — prominent tics — may be ameliorated by a peripheral, sensory intervention compels us to revise not only our conception of the syndrome, but of the motor system itself

The dimensionalities of lesion-deficit mapping

Lesion-deficit mapping remains the most powerful method for localising function in the human brain. As the highest court of appeal where competing theories of cerebral function conflict, it ought to be held to the most stringent inferential standards. Though at first sight elegantly transferable, the mass-univariate statistical framework popularized by functional imaging is demonstrably ill-suited to the task, both theoretically and empirically. The critical difficulty lies with the handling of the data's intrinsically high dimensionality. Conceptual opacity and computational complexity lead lesion-deficit mappers to neglect two distinct sets of anatomical interactions: those between areas unified by function, and those between areas unified by the natural pattern of pathological damage. Though both are soluble through high-dimensional multivariate analysis, the consequences of ignoring them are radically different. The former will bleach and coarsen a picture of the functional anatomy that is nonetheless broadly faithful to reality; the latter may alter it beyond all recognition. That the field continues to cling to mass-univariate methods suggests the latter problem is misidentified with the former, and that their distinction is in need of elaboration. We further argue that the vicious effects of lesion-driven interactions are not limited to anatomical localisation but will inevitably degrade purely predictive models of function such as those conceived for clinical prognostic use. Finally, we suggest there is a great deal to be learnt about lesion-mapping by simulation-based modelling of lesion data, for the fundamental problems lie upstream of the experimental data themselves

The neural antecedents to voluntary action: A conceptual analysis.

The inferential standards for testing hypotheses are settled; those for constructing them rarely even discussed. If the fit to the data of a hypothesis matters, then so must its fundamental coherence. That is indeed prior to any other question. Here we make use of conceptual analysis in testing the coherence of hypotheses in cognitive neuroscience and apply it to the study of the antecedents to voluntary action. We show that many influential experiments in the literature are premised-often covertly-on erroneous conceptions that render their hypotheses incoherent. The inferences drawn from the data are therefore invalidated proximally to any objection empirical replication could counter. We further demonstrate the empirical consequences of these errors in generating artifactual observable effects that have no general significance and impede further progress. We conclude with a basic framework for constructing robust hypotheses in this difficult and important field

Neck atonia with a focal stimulation-induced seizure arising from the SMA: pathophysiological considerations.

A 28-year-old patient with pharmacoresistant non-lesional right frontal epilepsy underwent extra-operative intracranial EEG recordings and electrical cortical stimulation (ECS) to map eloquent cortex. Right supplementary motor area (SMA) ECS induced a brief seizure with habitual symptoms involving neck tingling followed by asymmetric tonic posturing. An additional feature was neck atonia. During atonia and sensory aura, discharges were seen in the mesial frontal electrodes and precentral gyrus. Besides motor signs, atonia, although rare and not described in the neck muscles, and sensations have been reported with SMA stimulation. The mechanisms underlying neck atonia in seizures arising from the SMA can be explained by supplementary negative motor area (SNMA) - though this was not mapped in electrodes overlying the ictal onset zone in our patient - or primary sensorimotor cortex activation through rapid propagation. Given the broad spectrum of signs elicited by SMA stimulation and rapid spread of seizures arising from the SMA, caution should be taken to not diagnose these as non-epileptic, as had previously occurred in this patient

The Frontal Control of Stopping

Stopping is a critical aspect of brain function. Like other voluntary actions, it is defined by its context as much as by its execution. Its neural substrate must therefore reflect both. Here, we distinguish those elements of the underlying brain circuit that preferentially reflect contextual aspects of stopping from those related to its execution. Contextual complexity of stopping was modulated using a novel "Stop/Change-signal" task, which also allowed us to parameterize the duration of the stopping process. Human magnetoencephalographic activity and behavioral responses were simultaneously recorded. Whereas theta/alpha frequency activity in the right inferior frontal gyrus was most closely associated with the duration of the stopping process, earlier gamma frequency activity in the pre-supplementary motor area was unique in showing contextual modulation. These results differentiate the roles of 2 key frontal regions involved in stopping, a crucial aspect of behavioral control

Reversed Procrastination by Focal Disruption of Medial Frontal Cortex.

An enduring puzzle in the neuroscience of voluntary action is the origin of the remarkably wide dispersion of the reaction time distribution, an interval far greater than is explained by synaptic or signal transductive noise [1, 2]. That we are able to change our planned actions-a key criterion of volition [3]-so close to the time of their onset implies decision-making must reach deep into the execution of action itself [4-6]. It has been influentially suggested the reaction time distribution therefore reflects deliberate neural procrastination [7], giving alternative response tendencies sufficient time for fair competition in pursuing a decision threshold that determines which one is behaviorally manifest: a race model, where action selection and execution are closely interrelated [8-11]. Although the medial frontal cortex exhibits a sensitivity to reaction time on functional imaging that is consistent with such a mechanism [12-14], direct evidence from disruptive studies has hitherto been lacking. If movement-generating and movement-delaying neural substrates are closely co-localized here, a large-scale lesion will inevitably mask any acceleration, for the movement itself could be disrupted. Circumventing this problem, here we observed focal intracranial electrical disruption of the medial frontal wall in the context of the pre-surgical evaluation of two patients with epilepsy temporarily reversing such hypothesized procrastination. Effector-specific behavioral acceleration, time-locked to the period of electrical disruption, occurred exclusively at a specific locus at the ventral border of the pre-supplementary motor area. A cardinal prediction of race models of voluntary action is thereby substantiated in the human brain