Sensory Reafference Research Articles

Predictive steering: integration of artificial motor signals in self-motion estimation.

The brain's computations for active and passive self-motion estimation can be unified with a single model that optimally combines vestibular and visual signals with sensory predictions based on efference copies. It is unknown whether this theoretical framework also applies to the integration of artificial motor signals, such as those that occur when driving a car, or whether self-motion estimation in this situation relies on sole feedback control. Here, we examined if training humans to control a self-motion platform leads to the construction of an accurate internal model of the mapping between the steering movement and the vestibular reafference. Participants (n = 15) sat on a linear motion platform and actively controlled the platform's velocity using a steering wheel to translate their body to a memorized visual target (motion condition). We compared their steering behavior to that of participants (n = 15) who remained stationary and instead aligned a nonvisible line with the target (stationary condition). To probe learning, the gain between the steering wheel angle and the platform or line velocity changed abruptly twice during the experiment. These gain changes were virtually undetectable in the displacement error in the motion condition, whereas clear deviations were observed in the stationary condition, showing that participants in the motion condition made within-trial changes to their steering behavior. We conclude that vestibular feedback allows not only the online control of steering but also a rapid adaptation to the gain changes to update the brain's internal model of the mapping between the steering movement and the vestibular reafference.NEW & NOTEWORTHY Perception of self-motion is known to depend on the integration of sensory signals and, when the motion is self-generated, the predicted sensory reafference based on motor efference copies. Here we show, using a closed-loop steering experiment with a direct coupling between the steering movement and the vestibular self-motion feedback, that humans are also able to integrate artificial motor signals, like the motor signals that occur when driving a car.

The Generic Inhibitory Function of Corollary Discharge in Motor Intention: Evidence from the Modulation Effects of Speech Preparation on the Late Components of Auditory Neural Responses.

The importance of action-perception loops necessitates efficient computations linking motor and sensory systems. Corollary discharge (CD), a concept in motor-to-sensory transformation, has been proposed to predict the sensory consequences of actions for efficient motor and cognitive control. The predictive computation has been assumed to realize via inhibiting sensory reafference when actions are executed. Continuous control throughout the course of action demands inhibitory function ubiquitously on all potential reafference when sensory consequences are not available before execution. However, the temporal and functional characteristics of CD are unclear. When does CD begin to operate? To what extent does CD inhibit sensory processes? How is the inhibitory function implemented in neural computation? Using a delayed articulation paradigm with three types of auditory probes (speech, nonspeech, and nonhuman sounds) in an electroencephalography experiment with 20 human participants (7 males), we found that preparing to speak without knowing what to say (general preparation) suppressed neural responses to each type of auditory probe, suggesting a generic inhibitory function of CD in motor intention. Moreover, power and phase coherence in low-frequency bands (1-8 Hz) were both suppressed, indicating that inhibition was mediated by dampening response amplitude and adding temporal variance to sensory processes. Furthermore, inhibition was stronger for sounds that humans can produce than nonhuman sounds, hinting that the generic inhibitory function of CD is regulated by the established motor-sensory associations. These results suggest a functional and temporal granularity of corollary discharge that mediates multifaceted computations in motor and cognitive control.

Effects of arousal and movement on secondary somatosensory and visual thalamus.

Neocortical sensory areas have associated primary and secondary thalamic nuclei. While primary nuclei transmit sensory information to cortex, secondary nuclei remain poorly understood. We recorded juxtasomally from secondary somatosensory (POm) and visual (LP) nuclei of awake mice while tracking whisking and pupil size. POm activity correlated with whisking, but not precise whisker kinematics. This coarse movement modulation persisted after facial paralysis and thus was not due to sensory reafference. This phenomenon also continued during optogenetic silencing of somatosensory and motor cortex and after lesion of superior colliculus, ruling out a motor efference copy mechanism. Whisking and pupil dilation were strongly correlated, possibly reflecting arousal. Indeed LP, which is not part of the whisker system, tracked whisking equally well, further indicating that POm activity does not encode whisker movement per se. The semblance of movement-related activity is likely instead a global effect of arousal on both nuclei. We conclude that secondary thalamus monitors behavioral state, rather than movement, and may exist to alter cortical activity accordingly.

Multiple behavior-specific cancellation signals contribute to suppressing predictable sensory reafference in a cerebellum-like structure.

Movement induces sensory stimulation of an animal's own sensory receptors, termed reafference. With a few exceptions, notably vestibular and proprioception, this reafference is unwanted sensory noise and must be selectively filtered in order to detect relevant external sensory signals. In the cerebellum-like electrosensory nucleus of elasmobranch fish, an adaptive filter preserves novel signals by generating cancellation signals that suppress predictable reafference. A parallel fiber network supplies the principal Purkinje-like neurons (called ascending efferent neurons, AENs) with behavior-associated internal reference signals, including motor corollary discharge and sensory feedback, from which predictive cancellation signals are formed. How distinct behavior-specific cancellation signals interact within AENs when multiple behaviors co-occur and produce complex, changing patterns of reafference is unknown. Here, we show that when multiple streams of internal reference signals are available, cancellation signals form that are specific to parallel fiber inputs temporally correlated with, and therefore predictive of, sensory reafference. A single AEN has the capacity to form more than one cancellation signal, and AENs form multiple cancellation signals simultaneously and modify them independently during co-occurring behaviors. Cancellation signals update incrementally during continuous behaviors, as well as episodic bouts of behavior that last minutes to hours. Finally, individual AENs, independently of their neighbors, form unique AEN-specific cancellation signals that depend on the particular sensory reafferent input it receives. Together, these results demonstrate the capacity of the adaptive filter to utilize multiple cancellation signals to suppress dynamic patterns of reafference arising from complex co-occurring and intermittently performed behaviors.

Illusion of control affects ERP amplitude reductions for auditory outcomes of self‐generated actions

The reduction of neural responses to self-generated stimuli compared to external stimuli is thought to result from the matching of motor-based sensory predictions and sensory reafferences and to serve the identification of changes in the environment as caused by oneself. The amplitude of the auditory event-related potential (ERP) component N1 seems to closely reflect this matching process, while the later positive component (P2/ P3a) has been associated with judgments of agency, which are also sensitive to contextual top-down information. In this study, we examined the effect of perceived control over sound production on the processing of self-generated and external stimuli, as reflected in these components. We used a new version of a classic two-button choice task to induce different degrees of the illusion of control (IoC) and recorded ERPs for the processing of self-generated and external sounds in a subsequent task. N1 amplitudes were reduced for self-generated compared to external sounds, but not significantly affected by IoC. P2/3a amplitudes were affected by IoC: We found reduced P2/3a amplitudes after a high compared to a low IoC induction training, but only for self-generated, not for external sounds. These findings suggest that prior contextual belief information induced by an IoC affects later processing as reflected in the P2/P3a, possibly for the formation of agency judgments, while early processing reflecting motor-based predictions is not affected.

Large Postural Sways Prevent Foot Tactile Information From Fading: Neurophysiological Evidence.

Cutaneous foot receptors are important for balance control, and their activation during quiet standing depends on the speed and the amplitude of postural oscillations. We hypothesized that the transmission of cutaneous input to the cortex is reduced during prolonged small postural sways due to receptor adaptation during continued skin compression. Central mechanisms would trigger large sways to reactivate the receptors. We compared the amplitude of positive and negative post-stimulation peaks (P50N90) somatosensory cortical potentials evoked by the electrical stimulation of the foot sole during small and large sways in 16 young adults standing still with their eyes closed. We observed greater P50N90 amplitudes during large sways compared with small sways consistent with increased cutaneous transmission during large sways. Postural oscillations computed 200 ms before large sways had smaller amplitudes than those before small sways, providing sustained compression within a small foot sole area. Cortical source analyses revealed that during this interval, the activity of the somatosensory areas decreased, whereas the activity of cortical areas engaged in motor planning (supplementary motor area, dorsolateral prefrontal cortex) increased. We concluded that large sways during quiet standing represent self-generated functional behavior aiming at releasing skin compression to reactivate mechanoreceptors. Such balance motor commands create sensory reafference that help control postural sway.

“Embodied” language processing: Mental motor imagery aptitude predicts word-definition skill for high but not for low imageable words in adolescents

Our study was designed to test a recent proposal by Cayol and Nazir (2020), according to which language processing takes advantage of motor system “emulators”. An emulator is a brain mechanism that learns the causal relationship between an action and its sensory consequences. Emulators predict the outcome of a motor command in terms of its sensory reafference and serve monitoring ongoing movements. For the purpose of motor planning/learning, emulators can “run offline”, decoupled from sensory input and motor output. Such offline simulations are equivalent to mental imagery (Grush, 2004). If language processing can profit from the associative-memory network of emulators, mental-imagery-aptitude should predict language skills. However, this should hold only for language content that is imageable. We tested this assumption in typically developing adolescents using two motor-imagery paradigms. One that measured participant’s error in estimating their motor ability, and another that measured the time to perform a mental simulation. When the time to perform a mental simulation is taken as measure, mental-imagery-aptitude does indeed selectively predict word-definition performance for high imageable words. These results provide an alternative position relative to the question of why language processes recruit modality-specific brain regions and support the often-hypothesized link between language and motor skills.

Tactile suppression in goal-directed movement.

Sharing numerous characteristics with suppression in the other senses, tactile suppression is a reliable phenomenon that accompanies movement. By investigating the simplest of movements (e.g., finger flexions), early research tried to explain the origins of the phenomenon in terms of motor command generation together with sensory reafference. Here, we review recent research that has delved into (naturalistic) goal-directed movements. In connection with goal-directed movement, tactile suppression is evident as a decrease in behavioural performance measured shortly prior to, and during, movement execution. It is also reflected in a consistent response bias highlighting the (perceptual) uncertainty of the movement. Goal-directed movement supports the forward model and establishes contextual influences as the defining influences on tactile suppression. Depending on the task at hand, people prioritize a certain percept during movement. Future research, we argue, should focus on studying naturalistic movements, or sequences of movements, that share a common meaning or goal.

Working memory facilitates the detection and correction of feedback errors in vocal pitch regulation

In speech processing, information related to the speech motor command and sensory re-afference can be stored in working memory (WM) within a feedback circuit and recalled when needed to adjust the motor activity. Whether WM facilitates the online monitoring of speech motor control, however, remains unclear. The present event-related potential study sought to examine the impact of WM on the auditory-motor processing of pitch feedback errors. Participants sustained a vowel phonation while hearing their voice pitch-shifted + 200 or + 500 cents five times. In the WM task, participants were asked to determine whether the sequence of 5 pitch shifts was different or not between two consecutive vocalizations. In the control task, they did nothing but maintaining their vocalizations steady when exposed to pitch-shifted auditory feedback. The behavioral results revealed a significant increase of vocal responses in the WM task as compared to the control task. At the cortical level, the WM task elicited significantly larger N1 responses and smaller P2 responses than the control task. Taken together, these findings demonstrate the influence of WM on the neurobehavioral responses to pitch-shifted voice auditory feedback, indicating that WM can facilitate the detection and correction of pitch feedback errors in vocal motor control.

Age-related changes in post-movement beta synchronization during a selective inhibition task.

Post-movement beta synchronization (PMBS) modulations have been related to sensory reafferences after movement initiation and inhibitory processes after movement interruption. Although these processes have been separately studied in young and old adults, little is known about the age-related changes in PMBS during selective inhibitory control (i.e. stop a part of an action). The present study examines the age-related modulations of PMBS associated with sensory reafferences and inhibitory processes in selective inhibitory control. Young (n=17) and old (n=13) participants performed a switching task first engaging bimanual finger tapping then requiring to stop the left while maintaining the right unimanual tapping (i.e. selective inhibition) at an imperative stimulus. Age groups were compared on behavioral (mean, variability and percentage of errors of inter-tap interval during and after the switching) and electrophysiological (time-frequency and source estimations in the 14-30Hz beta frequency range) data time-locked on the imperative stimulus. Behaviorally, old adults showed larger variability and percentage of errors during the switching but performed as well as young adults after the switching. Electrophysiologically, PMBS significantly increased after the switching in the old compared to the young group within bilateral frontal and parietal areas. Our results show that the effort to maintain selective inhibition involves increased brain activation in old compared to young adults. The larger PMBS within frontal and parietal regions in old adults may reflect an age-related brain compensation enabling to efficiently maintain post-switching inhibition.

What insects can tell us about the origins of consciousness.

How, why, and when consciousness evolved remain hotly debated topics. Addressing these issues requires considering the distribution of consciousness across the animal phylogenetic tree. Here we propose that at least one invertebrate clade, the insects, has a capacity for the most basic aspect of consciousness: subjective experience. In vertebrates the capacity for subjective experience is supported by integrated structures in the midbrain that create a neural simulation of the state of the mobile animal in space. This integrated and egocentric representation of the world from the animal's perspective is sufficient for subjective experience. Structures in the insect brain perform analogous functions. Therefore, we argue the insect brain also supports a capacity for subjective experience. In both vertebrates and insects this form of behavioral control system evolved as an efficient solution to basic problems of sensory reafference and true navigation. The brain structures that support subjective experience in vertebrates and insects are very different from each other, but in both cases they are basal to each clade. Hence we propose the origins of subjective experience can be traced to the Cambrian.

Plasticity of cerebellar Purkinje cells in behavioral training of body balance control.

Neural responses to sensory inputs caused by self-generated movements (reafference) and external passive stimulation (exafference) differ in various brain regions. The ability to differentiate such sensory information can lead to movement execution with better accuracy. However, how sensory responses are adjusted in regard to this distinguishability during motor learning is still poorly understood. The cerebellum has been hypothesized to analyze the functional significance of sensory information during motor learning, and is thought to be a key region of reafference computation in the vestibular system. In this study, we investigated Purkinje cell (PC) spike trains as cerebellar cortical output when rats learned to balance on a suspended dowel. Rats progressively reduced the amplitude of body swing and made fewer foot slips during a 5-min balancing task. Both PC simple (SSs; 17 of 26) and complex spikes (CSs; 7 of 12) were found to code initially on the angle of the heads with respect to a fixed reference. Using periods with comparable degrees of movement, we found that such SS coding of information in most PCs (10 of 17) decreased rapidly during balance learning. In response to unexpected perturbations and under anesthesia, SS coding capability of these PCs recovered. By plotting SS and CS firing frequencies over 15-s time windows in double-logarithmic plots, a negative correlation between SS and CS was found in awake, but not anesthetized, rats. PCs with prominent SS coding attenuation during motor learning showed weaker SS-CS correlation. Hence, we demonstrate that neural plasticity for filtering out sensory reafference from active motion occurs in the cerebellar cortex in rats during balance learning. SS-CS interaction may contribute to this rapid plasticity as a form of receptive field plasticity in the cerebellar cortex between two receptive maps of sensory inputs from the external world and of efference copies from the will center for volitional movements.

Distinct roles for alpha- and beta-band oscillations during mental simulation of goal-directed actions.

Rhythmic neural activity within the alpha (8-12 Hz) and beta (15-25 Hz) frequency bands is modulated during actual and imagined movements. Changes in these rhythms provide a mechanism to select relevant neuronal populations, although the relative contributions of these rhythms remain unclear. Here we use MEG to investigate changes in oscillatory power while healthy human participants imagined grasping a cylinder oriented at different angles. This paradigm allowed us to study the neural signals involved in the simulation of a movement in the absence of signals related to motor execution and sensory reafference. Movement selection demands were manipulated by exploiting the fact that some object orientations evoke consistent grasping movements, whereas others are compatible with both overhand and underhand grasping. By modulating task demands, we show a functional dissociation of the alpha- and beta-band rhythms. As movement selection demands increased, alpha-band oscillatory power increased in the sensorimotor cortex ipsilateral to the arm used for imagery, whereas beta-band power concurrently decreased in the contralateral sensorimotor cortex. The same pattern emerged when motor imagery trials were compared with a control condition, providing converging evidence for the functional dissociation of the two rhythms. These observations call for a re-evaluation of the role of sensorimotor rhythms. We propose that neural oscillations in the alpha-band mediate the allocation of computational resources by disengaging task-irrelevant cortical regions. In contrast, the reduction of neural oscillations in the beta-band is directly related to the disinhibition of neuronal populations involved in the computations of movement parameters.

Post-switching beta synchronization reveals concomitant sensory reafferences and active inhibition processes

It is known that post-movement beta synchronization (PMBS) is involved both in active inhibition and in sensory reafferences processes. The aim of this study was examine the temporal and spatial dynamics of the PMBS involved during multi-limb coordination task. We investigated post-switching beta synchronization (assigned PMBS) using time-frequency and source estimations analyzes. Participants (n=17) initiated an auditory-paced bimanual tapping. After a 1500ms preparatory period, an imperative stimulus required to either selectively stop the left while maintaining the right unimanual tapping (Switch condition: SWIT) or to continue the bimanual tapping (Continue condition: CONT). PMBS significantly increased in SWIT compared to CONT with maximal difference within right central region in broad-band 14–30Hz and within left central region in restricted-band 22–26Hz. Source estimations localized these effects within right pre-frontal cortex and left parietal cortex, respectively. A negative correlation showed that participants with a low percentage of errors in SWIT had a large PMBS amplitude within right parietal and frontal cortices. This study shows for the first time simultaneous PMBS with distinct functions in different brain regions and frequency ranges. The left parietal PMBS restricted to 22–26Hz could reflect the sensory reafferences of the right hand tapping disrupted by the switching. In contrast, the right pre-frontal PMBS in a broad-band 14–30Hz is likely reflecting the active inhibition of the left hand stopped. Finally, correlations between behavioral performance and the magnitude of the PMBS suggest that beta oscillations can be viewed as a marker of successful active inhibition.

P395: Switching from bimanual to unimanual tapping reveals two distinct post-switching beta synchronization processes

P395: Switching from bimanual to unimanual tapping reveals two distinct post-switching beta synchronization processes

Asymmetries of bilateral isometric force matching with movement intention and unilateral fatigue

During bilateral coordination, some level of inter-hemispheric remapping (i.e., the congruency between afferent and efferent force signals from both hemispheres) is required. In this case, sensory-motor information is exchanged between the two hemispheres, but it remains unclear whether this information exchange is always equivalent or not, especially in a bilateral isometric force-matching task. We used unilateral fatigue applied to one arm in order to determine whether inter-hemispheric remapping can vary asymmetrically during a bilateral isometric matching task. Because fatigue is considered to bias the sensory-motor system, we hypothesized that if bimanual coordination is modulated solely in function of the state of the sensory-motor system (motor efferences, inter-hemispheric inhibitions, and sensory reafferences), we should not observe any asymmetric effect of fatigue with movement intention (leading vs. matching arm). However, if any other process could participate in the modulation of inter-hemispheric remapping, we should observe an interaction between movement intentions and fatigue on the force produced. We found that, when the leading arm was the non-fatigued arm, participants succeeded in reproducing the force level with their fatigued arm. By contrast, when the leading arm was fatigued, subjects over-estimated the force level produced with their non-fatigued arm. Hence, lateralized fatigue exacerbates an asymmetric behavior that seems modulated by movement intention (leading vs. matching). In other words, when unilateral fatigue is introduced in a bilateral isometric force-matching task, inter-hemispheric remapping is asymmetrical. Intensity levels of motor commands sent to both arms (directly or modulated through inter-hemispheric inhibitions) and sensory reafferences alone cannot explain these observations. Some attentional focus may be not balanced continuously between both arms but may be mainly directed toward the matching arm.

Age-related changes in the bimanual advantage and in brain oscillatory activity during tapping movements suggest a decline in processing sensory reafference

Deficits in the processing of sensory reafferences have been suggested as accounting for age-related decline in motor coordination. Whether sensory reafferences are accurately processed can be assessed based on the bimanual advantage in tapping: because of tapping with an additional hand increases kinesthetic reafferences, bimanual tapping is characterized by a reduced inter-tap interval variability than unimanual tapping. A suppression of the bimanual advantage would thus indicate a deficit in sensory reafference. We tested whether elderly indeed show a reduced bimanual advantage by measuring unimanual (UM) and bimanual (BM) self-paced tapping performance in groups of young (n = 29) and old (n = 27) healthy adults. Electroencephalogram was recorded to assess the underlying patterns of oscillatory activity, a neurophysiological mechanism advanced to support the integration of sensory reafferences. Behaviorally, there was a significant interaction between the factors tapping condition and age group at the level of the inter-tap interval variability, driven by a lower variability in BM than UM tapping in the young, but not in the elderly group. This result indicates that in self-paced tapping, the bimanual advantage is absent in elderly. Electrophysiological results revealed an interaction between tapping condition and age group on low beta band (14-20 Hz) activity. Beta activity varied depending on the tapping condition in the elderly but not in the young group. Source estimations localized this effect within left superior parietal and left occipital areas. We interpret our results in terms of engagement of different mechanisms in the elderly depending on the tapping mode: a 'kinesthetic' mechanism for UM and a 'visual imagery' mechanism for BM tapping movement.

The Primate Cerebellum Selectively Encodes Unexpected Self-Motion

The ability to distinguish sensory signals that register unexpected events (exafference) from those generated by voluntary actions (reafference) during self-motion is essential for accurate perception and behavior. The cerebellum is most commonly considered in relation to its contributions to the fine tuning of motor commands and sensorimotor calibration required for motor learning. During unexpected motion, however, the sensory prediction errors that drive motor learning potentially provide a neural basis for the computation underlying the distinction between reafference and exafference. Recording from monkeys during voluntary and applied self-motion, we demonstrate that individual cerebellar output neurons encode an explicit and selective representation of unexpected self-motion by means of an elegant computation that cancels the reafferent sensory effects of self-generated movements. During voluntary self-motion, the sensory responses of neurons that robustly encode unexpected movement are canceled. Neurons with vestibular and proprioceptive responses to applied head and body movements are unresponsive when the same motion is self-generated. When sensory reafference and exafference are experienced simultaneously, individual neurons provide a precise estimate of the detailed time course of exafference. These results provide an explicit solution to the longstanding problem of understanding mechanisms by which the brain anticipates the sensory consequences of our voluntary actions. Specifically, by revealing a striking computation of a sensory prediction error signal that effectively distinguishes between the sensory consequences of self-generated and externally produced actions, our findings overturn the conventional thinking that the sensory errors coded by the cerebellum principally contribute to the fine tuning of motor activity required for motor learning.

Continuous theta-burst stimulation to primary motor cortex reveals asymmetric compensation for sensory attenuation in bimanual repetitive force production

Studies of fingertip force production have shown that self-produced forces are perceived as weaker than externally generated forces. This is due to mechanisms of sensory reafference where the comparison between predicted and actual sensory feedback results in attenuated perceptions of self-generated forces. Without an external reference to calibrate attenuated performance judgments, a compensatory overproduction of force is exhibited. It remains unclear whether the force overproduction seen in the absence of visual reference stimuli differs when forces are produced bimanually. We studied performance of two versions of a bimanual sequential force production task compared with each hand performing the task unimanually. When the task goal was shared, force series produced by each hand in bimanual conditions were found to be uncorrelated. When the bimanual task required each hand to reach a target force level, we found asymmetries in the degree of force overproduction between the hands following visual feedback removal. Unilateral continuous theta-burst stimulation of the left primary motor cortex yielded a selective reduction of force overproduction in the hand contralateral to stimulation by disrupting sensory reafference processes. While variability was lower in bimanual trials when the task goal was shared, this influence of hand condition disappeared when the target force level was to be reached by each hand simultaneously. Our findings strengthen the notion that force control in bimanual action is less tightly coupled than other mechanisms of bimanual motor control and show that this effector specificity may be extended to the processing and compensation for mechanisms of sensory reafference.

MEG studies of motor cortex gamma oscillations: evidence for a gamma “fingerprint” in the brain?

The human motor cortex exhibits transient bursts of high frequency gamma oscillations in the 60–90 Hz range during movement. It has been proposed that gamma oscillations generally reflect local intracortical activity. However, movement-evoked gamma is observed simultaneously in both cortical and subcortical (basal ganglia) structures and thus appears to reflect long-range cortical-subcortical interactions. Recent evidence suggests that gamma oscillations do not simply reflect sensory reafference, but have a facilitative role in movement initiation. Here we summarize contributions of MEG to our understanding of movement-evoked gamma oscillations, including evidence that transient gamma bursts during the performance of specific movements constitutes a stereotyped spectral and temporal pattern within individuals—a gamma “fingerprint”—that is highly stable over time. Although their functional significance remains to be fully understood, movement-evoked gamma oscillations may represent frequency specific tuning within cortical-subcortical networks that can be monitored non-invasively using MEG during a variety of motor tasks, and may provide important information regarding cortical dynamics of ongoing motor control.