Nobuhiro Hagura

Consensus paper: roles of the cerebellum in motor control--the diversity of ideas on cerebellar involvement in movement.

Considerable progress has been made in developing models of cerebellar function in sensorimotor control, as well as in identifying key problems that are the focus of current investigation. In this consensus paper, we discuss the literature on the role of the cerebellar circuitry in motor control, bringing together a range of different viewpoints. The following topics are covered: oculomotor control, classical conditioning (evidence in animals and in humans), cerebellar control of motor speech, control of grip forces, control of voluntary limb movements, timing, sensorimotor synchronization, control of corticomotor excitability, control of movement-related sensory data acquisition, cerebro-cerebellar interaction in visuokinesthetic perception of hand movement, functional neuroimaging studies, and magnetoencephalographic mapping of cortico-cerebellar dynamics. While the field has yet to reach a consensus on the precise role played by the cerebellum in movement control, the literature has witnessed the emergence of broad proposals that address cerebellar function at multiple levels of analysis. This paper highlights the diversity of current opinion, providing a framework for debate and discussion on the role of this quintessential vertebrate structure.

Ready steady slow: action preparation slows the subjective passage of time

Professional ball game players report the feeling of the ball ‘slowing-down’ before hitting it. Because effective motor preparation is critical in achieving such expert motor performance, these anecdotal comments imply that the subjective passage of time may be influenced by preparation for action. Previous reports of temporal illusions associated with action generally emphasize compensation for suppressed sensory signals that accompany motor commands. Here, we show that the time is perceived slowed-down during preparation of a ballistic reaching movement before action, involving enhancement of sensory processing. Preparing for a reaching movement increased perceived duration of a visual stimulus. This effect was tightly linked to action preparation, because the amount of temporal dilation increased with the information about the upcoming movement. Furthermore, we showed a reduction of perceived frequency for flickering stimuli and an enhanced detection of rapidly presented letters during action preparation, suggesting increased temporal resolution of visual perception during action preparation. We propose that the temporal dilation during action preparation reflects the function of the brain to maximize the capacity of sensory information-acquisition prior to execution of a ballistic movement. This strategy might facilitate changing or inhibiting the planned action in response to last-minute changes in the external environment.

Perceptual decisions are biased by the cost to act

Perceptual decisions are classically thought to depend mainly on the stimulus characteristics, probability and associated reward. However, in many cases, the motor response is considered to be a neutral output channel that only reflects the upstream decision. Contrary to this view, we show that perceptual decisions can be recursively influenced by the physical resistance applied to the response. When participants reported the direction of the visual motion by left or right manual reaching movement with different resistances, their reports were biased towards the direction associated with less effortful option. Repeated exposure to such resistance on hand during perceptual judgements also biased subsequent judgements using voice, indicating that effector-dependent motor costs not only biases the report at the stage of motor response, but also changed how the sensory inputs are transformed into decisions. This demonstrates that the cost to act can influence our decisions beyond the context of the specific action. DOI: http://dx.doi.org/10.7554/eLife.18422.001

Food vibrations: Asian spice sets lips trembling.

Szechuan pepper, a widely used ingredient in the cuisine of many Asian countries, is known for the tingling sensation it induces on the tongue and lips. While the molecular mechanism by which Szechuan pepper activates tactile afferent fibres has been clarified, the tingling sensation itself has been less studied, and it remains unclear which fibres are responsible. We investigated the somatosensory perception of tingling in humans to identify the characteristic temporal frequency and compare this to the established selectivity of tactile afferents. Szechuan pepper was applied to the lower lip of participants. Participants judged the frequency of the tingling sensation on the lips by comparing this with the frequencies of mechanical vibrations applied to their right index finger. The perceived frequency of the tingling was consistently at around 50 Hz, corresponding to the range of tactile RA1 afferent fibres. Furthermore, adaptation of the RA1 channel by prolonged mechanical vibration reliably reduced the tingling frequency induced by Szechuan pepper, confirming that the frequency-specific tactile channel is shared between Szechuan pepper and mechanical vibration. Combining information about molecular reactions at peripheral receptors with quantitative psychophysical measurement may provide a unique method for characterizing unusual experiences by decomposing them into identifiable minimal units of sensation.

Constructing Visual Perception of Body Movement with the Motor Cortex

The human brain readily perceives fluent movement from static input. Using functional magnetic resonance imaging, we investigated brain mechanisms that mediate fluent apparent biological motion (ABM) perception from sequences of body postures. We presented body and nonbody stimuli varying in objective sequence duration and fluency of apparent movement. Three body postures were ordered to produce a fluent (ABC) or a nonfluent (ACB) apparent movement. This enabled us to identify brain areas involved in the perceptual reconstruction of body movement from identical lower-level static input. Participants judged the duration of a rectangle containing body/nonbody sequences, as an implicit measure of movement fluency. For body stimuli, fluent apparent motion sequences produced subjectively longer durations than nonfluent sequences of the same objective duration. This difference was reduced for nonbody stimuli. This body-specific bias in duration perception was associated with increased blood oxygen level-dependent responses in the primary (M1) and supplementary motor areas. Moreover, fluent ABM was associated with increased functional connectivity between M1/SMA and right fusiform body area. We show that perceptual reconstruction of fluent movement from static body postures does not merely enlist areas traditionally associated with visual body processing, but involves cooperative recruitment of motor areas, consistent with a “motor way of seeing”.

Decoding sequential finger movements from preparatory activity in higher-order motor regions: a functional magnetic resonance imaging multi-voxel pattern analysis

Performing a complex sequential finger movement requires the temporally well‐ordered organization of individual finger movements. Previous behavioural studies have suggested that the brain prepares a whole sequence of movements as a single set, rather than the movements of individual fingers. However, direct neuroimaging support for this hypothesis is lacking and, assuming it to be true, it remains unclear which brain regions represent the information of a prepared sequence. Here, we measured brain activity with functional magnetic resonance imaging while 14 right‐handed healthy participants performed two types of well‐learned sequential finger movements with their right hands. Using multi‐voxel pattern analysis, we examined whether the types of the forthcoming sequence could be predicted from the preparatory activities of nine regions of interest, which included the motor, somatosensory and posterior parietal regions in each hemisphere, bilateral visual cortices, cerebellum and basal ganglia. We found that, during preparation, the activity of the contralateral motor regions could predict which of the two sequences would be executed. Further detailed analysis revealed that the contralateral dorsal premotor cortex and supplementary motor area were the key areas that contributed to the prediction consistently across participants. These contrasted with results from execution‐related brain activity where a performed sequence was successfully predicted from the activities in the broad cortical sensory‐motor network, including the bilateral motor, parietal and ipsilateral somatosensory cortices. Our study supports the hypothesis that temporary well‐organized sequences of movements are represented as a set in the brain, and that preparatory activity in higher‐order motor regions represents information about upcoming motor actions.

Sanshool on The Fingertip Interferes with Vibration Detection in a Rapidly-Adapting (RA) Tactile Channel

An Asian spice, Szechuan pepper (sanshool), is well known for the tingling sensation it induces on the mouth and on the lips. Electrophysiological studies have revealed that its active ingredient can induce firing of mechanoreceptor fibres that typically respond to mechanical vibration. Moreover, a human behavioral study has reported that the perceived frequency of sanshool-induced tingling matches with the preferred frequency range of the tactile rapidly adapting (RA) channel, suggesting the contribution of sanshool-induced RA channel firing to its unique perceptual experience. However, since the RA channel may not be the only channel activated by sanshool, there could be a possibility that the sanshool tingling percept may be caused in whole or in part by other sensory channels. Here, by using a perceptual interference paradigm, we show that the sanshool-induced RA input indeed contributes to the human tactile processing. The absolute detection thresholds for vibrotactile input were measured with and without sanshool application on the fingertip. Sanshool significantly impaired detection of vibrations at 30 Hz (RA channel dominant frequency), but did not impair detection of higher frequency vibrations at 240 Hz (Pacinian-corpuscle (PC) channel dominant frequency) or lower frequency vibrations at 1 Hz (slowly adapting 1 (SA1) channel dominant frequency). These results show that the sanshool induces a peripheral RA channel activation that is relevant for tactile perception. This anomalous activation of RA channels may contribute to the unique tingling experience of sanshool.

Body Representation and Neuroprosthetics

Neuroprosthetics refer to prosthetic devices designed according to neuroscientific principles and interfacing directly with the nervous system. We propose a fundamental distinction between receptor prosthetics and somatic prosthetics. Receptor prosthetics involve substituting or augmenting the signals that the peripheral end-organ sends to the brain. In the ideal case, this substitution is perfectly transparent, so no novel learning or plastic change of neural processing is required. In contrast, somatic prosthetics will not just send new or substitute signals to the brain, but relies on plastic adjustments to the brain to use the novel signal in a functional way. The former does not involve any change in the representation of the body, but the latter may force the brain to change fundamental features of body representation. The continuum from receptor prosthetics to somatic prosthetics may provide a useful way of thinking about the hierarchy of the body representation extending from local receptor information processing (e.g. skin, muscle and joint) to the coherent representation of the body that apparently underlies the sense of ‘self’.

Effect of haptic feedback from self-touch on limb movement coordination

Touching ones own body provides haptic feedback about the spatial configuration and movement of body parts. However, the influence of self-touch on movement performance has not been investigated so far. The authors evaluated the contribution of self-touch by asking participants to perform cyclic movement sequences with their feet while touching them with their hands, or vice versa. Hands and feet were either crossed or uncrossed (parallel), manipulating anatomical congruency of haptic feedback. The effects of self-touch (vs. object-touch), active limb (feet vs. hands) and sequence complexity were assessed in three separate experiments. Task performance was strongly and specifically disrupted in one of the anatomically incongruent conditions (hands-parallel/feet-crossed). This disruption occurred only with self-touch (Experiment 1), with the feet active (Experiment 2), and was more pronounced for the more complex movement sequence (Experiment 3). Thus, incongruent self-touch can strongly interfere with motor performance, showing that haptic information is automatically integrated in the online control of movement. The observed asymmetry between hands and feet indicates limb-specific differences regarding the use of spatial frames of reference and/or regarding the weighting of sensory information. The results emphasize the intimate connection between programming of action sequences and the anticipation of somatic feedback from self-touch.

Specificity of action selection modulates the perceived temporal order of action and sensory events

The perceived temporal order of actions and changes in the environment is crucial for our inferences of causality. Sensory events presented shortly after an action are more likely considered as self-generated compared to the same events occurring before action execution. However, the estimation of when an action or a sensory change occurred is a challenge for the human brain. This estimation is formed from available sensory information combined with internal representations. Researchers suggested that internal signals associated with action preparation drive our awareness of initiating an action. This study aimed to directly investigate this hypothesis. Participants performed a speeded action (left or right key-press) in response to a go-signal (left or right arrow). A flash was presented at different time points around the time of the action, and participants judged whether it was simultaneous with the action or not. To investigate the role of action preparation in time perception, we compared trials where a cue indicated which action to perform in response to a later go signal presentation, and trials with a neutral cue where participants did not know until the time of the go signal which action to perform. We observed that a flash presented before the action was reported as simultaneous with the action more frequently when actions were cued than when they were uncued. This difference was not observed when the action was replaced by a tactile stimulation. These results indicate that precued actions are experienced earlier in time compared to unprepared actions. Further, this difference is not due to mere non-motor expectation of an event. The experience of initiating an action is driven by action preparation process: when we know what to do, actions are perceived ahead of time.