Self-generated Movements Research Articles

Perceiving the self-generated motion on the retina caused by smooth pursuit

Perceiving the self-generated motion on the retina caused by smooth pursuit

Amplify Gait to Improve Locomotor Engagement in Spinal Cord Injury (AGILE SCI) trial: study protocol for an assessor blinded randomized controlled trial

BackgroundAmong ambulatory people with incomplete spinal cord injury (iSCI), balance deficits are a primary factor limiting participation in walking activities. There is broad recognition that effective interventions are needed to enhance walking balance following iSCI. Interventions that amplify self-generated movements (e.g., error augmentation) can accelerate motor learning by intensifying sensorimotor feedback and facilitating exploration of motor control strategies. These features may be beneficial for retraining walking balance after iSCI. We have developed a cable-driven robot that creates a movement amplification environment during treadmill walking. The robot applies a continuous, laterally-directed, force to the pelvis that is proportional in magnitude to real-time lateral velocity. Our purpose is to investigate the effects of locomotor training in this movement amplification environment on walking balance. We hypothesize that for ambulatory people with iSCI, locomotor training in a movement amplification environment will be more effective for improving walking balance and participation in walking activities than locomotor training in a natural environment (no applied external forces).MethodsWe are conducting a two-arm parallel-assignment intervention. We will enroll 36 ambulatory participants with chronic iSCI. Participants will be randomized into either a control or experimental group. Each group will receive 20 locomotor training sessions. Training will be performed in either a traditional treadmill environment (control) or in a movement amplification environment (experimental). We will assess changes using measures that span the International Classification of Functioning, Disability and Health (ICF) framework including 1) clinical outcome measures of gait, balance, and quality of life, 2) biomechanical assessments of walking balance, and 3) participation in walking activities quantified by number of steps taken per day.DiscussionTraining walking balance in people with iSCI by amplifying the individual’s own movement during walking is a radical departure from current practice and may result in new strategies for addressing balance impairments. Knowledge gained from this study will expand our understanding of how people with iSCI improve walking balance and how an intervention targeting walking balance affects participation in walking activities. Successful outcomes could motivate development of clinically feasible tools to replicate the movement amplification environment within clinical settings.Trial registrationNCT04340063.

Sensorimotor prediction is used to direct gaze toward task-relevant locations in a goal-directed throwing task.

Previous research has shown that action effects of self-generated movements are internally predicted before outcome feedback becomes available. To test whether these sensorimotor predictions are used to facilitate visual information uptake for feedback processing, we measured eye movements during the execution of a goal-directed throwing task. Participants could fully observe the effects of their throwing actions (ball trajectory and either hitting or missing a target) in most of the trials. In a portion of the trials, the ball trajectory was not visible, and participants only received static information about the outcome. We observed a large proportion of predictive saccades, shifting gaze toward the goal region before the ball arrived and outcome feedback became available. Fixation locations after predictive saccades systematically covaried with future ball positions in trials with continuous ball flight information, but notably also in trials with static outcome feedback and only efferent and proprioceptive information about the movement that could be used for predictions. Fixation durations at the chosen positions after feedback onset were modulated by action outcome (longer durations for misses than for hits) and outcome uncertainty (longer durations for narrow vs. clear outcomes). Combining both effects, durations were longest for narrow errors and shortest for clear hits, indicating that the chosen locations offer informational value for feedback processing. Thus, humans are able to use sensorimotor predictions to direct their gaze toward task-relevant feedback locations. Outcome-dependent saccade latency differences (miss vs. hit) indicate that also predictive valuation processes are involved in planning predictive saccades.NEW & NOTEWORTHY We elucidate the potential benefits of sensorimotor predictions, focusing on how the system actually uses this information to optimize feedback processing in goal-directed actions. Sensorimotor information is used to predict spatial parameters of movement outcomes, guiding predictive saccades toward future action effects. Saccade latencies and fixation durations are modulated by outcome quality, indicating that predictive valuation processes are considered and that the locations chosen are of high informational value for feedback processing.

Collective behavior from surprise minimization

Collective motion is ubiquitous in nature; groups of animals, such as fish, birds, and ungulates appear to move as a whole, exhibiting a rich behavioral repertoire that ranges from directed movement to milling to disordered swarming. Typically, such macroscopic patterns arise from decentralized, local interactions among constituent components (e.g., individual fish in a school). Preeminent models of this process describe individuals as self-propelled particles, subject to self-generated motion and "social forces" such as short-range repulsion and long-range attraction or alignment. However, organisms are not particles; they are probabilistic decision-makers. Here, we introduce an approach to modeling collective behavior based on active inference. This cognitive framework casts behavior as the consequence of a single imperative: to minimize surprise. We demonstrate that many empirically observed collective phenomena, including cohesion, milling, and directed motion, emerge naturally when considering behavior as driven by active Bayesian inference-without explicitly building behavioral rules or goals into individual agents. Furthermore, we show that active inference can recover and generalize the classical notion of social forces as agents attempt to suppress prediction errors that conflict with their expectations. By exploring the parameter space of the belief-based model, we reveal nontrivial relationships between the individual beliefs and group properties like polarization and the tendency to visit different collective states. We also explore how individual beliefs about uncertainty determine collective decision-making accuracy. Finally, we show how agents can update their generative model over time, resulting in groups that are collectively more sensitive to external fluctuations and encode information more robustly.

Developmentally Unique Cerebellar Processing Prioritizes Self- over Other-Generated Movements.

Animals must distinguish the sensory consequences of self-generated movements (reafference) from those of other-generated movements (exafference). Only self-generated movements entail the production of motor copies (i.e., corollary discharges), which are compared with reafference in the cerebellum to compute predictive or internal models of movement. Internal models emerge gradually over the first three postnatal weeks in rats through a process that is not yet fully understood. Previously, we demonstrated in postnatal day (P) 8 and P12 rats that precerebellar nuclei convey corollary discharge and reafference to the cerebellum during active (REM) sleep when pups produce limb twitches. Here, recording from a deep cerebellar nucleus (interpositus, IP) in P12 rats of both sexes, we compared reafferent and exafferent responses with twitches and limb stimulations, respectively. As expected, most IP units showed robust responses to twitches. However, in contrast with other sensory structures throughout the brain, relatively few IP units showed exafferent responses. Upon finding that exafferent responses occurred in pups under urethane anesthesia, we hypothesized that urethane inhibits cerebellar cortical cells, thereby disinhibiting exafferent responses in IP. In support of this hypothesis, ablating cortical tissue dorsal to IP mimicked the effects of urethane on exafference. Finally, the results suggest that twitch-related corollary discharge and reafference are conveyed simultaneously and in parallel to cerebellar cortex and IP. Based on these results, we propose that twitches provide opportunities for the nascent cerebellum to integrate somatotopically organized corollary discharge and reafference, thereby enabling the development of closed-loop circuits and, subsequently, internal models.

Effects of Therapeutic Dosing through Enriched Environment on Gross Motor Function in Spastic Quadriplegic Cerebral Palsy

Background: Cerebral palsy differs in every child in terms of impairments, activity limitations and participation restrictions, so intervention should be designed in a way which is specific to every child and is constantly adjusted according to the needs of the child. Level appropriate selection of dosage (frequency, type, time, intensity) of treatment plays a vital role in treatment efficacy. Objective: To investigate the effects of therapeutic dosing through age-appropriate enriched environment on gross motor function in spastic quadriplegic cerebral palsy. Methods: In this RCT, 82 spastic cerebral palsy children were randomly allocated to two groups. Group A received level appropriate enriched environmental inputs consisting of motor and sensory enriched play environment with therapeutic dosing (20-25 minutes intermittently, 5 hours per day, 5 days a week for 24 weeks) along with Neurodevelopmental Technique. The goal was to promote participant’s self-generated movements, exploration of the environment and successful task completion. Group B received clinical based regular physical therapy consisting of NDT. Guidance was given to parents on how to carry out a home program. Data was collected at the end of 5 months on GMFM scale to check improvement in gross motor function. Results: The data was analyzed using Mann Whitney U test. There was statistically significant difference between the two groups. Group A showed improvement in gross motor function (p value<0.05) whereas improvement in group B was not as significant (p-value>0.05). Conclusion: This study concluded that optimal dosage of an intervention along with parent/caregiver education started at an early age resulted in significant functional improvements in spastic quadriplegic cerebral palsy children. These improvements were observed not only in body functions but also in active involvement and participation of the child.

Weakly electric fish use self-generated motion to discriminate object shape

Weakly electric fish use self-generated motion to discriminate object shape

Cortical facilitation of tactile afferents during the preparation of a body weight transfer when standing on a biomimetic surface.

Self-generated movement shapes tactile perception, but few studies have investigated the brain mechanisms involved in the processing of the mechanical signals related to the static and transient skin deformations generated by forces and pressures exerted between the foot skin and the standing surface. We recently found that standing on a biomimetic surface (i.e., inspired by the characteristics of mechanoreceptors and skin dermatoglyphics), that magnified skin-surface interaction, increased the sensory flow to the somatosensory cortex and improved balance control compared to standing on control (e.g., smooth) surfaces. In this study, we tested whether the well-known sensory suppression that occurs during movements is alleviated when the tactile afferent signal becomes relevant with the use of a biomimetic surface. Eyes-closed participants (n = 25) self-stimulated their foot cutaneous receptors by shifting their body weight toward one of their legs while standing on either a biomimetic or a control (smooth) surface. In a control task, similar forces were exerted on the surfaces (i.e., similar skin-surface interaction) by passive translations of the surfaces. Sensory gating was assessed by measuring the amplitude of the somatosensory-evoked potential over the vertex (SEP, recorded by EEG). Significantly larger and shorter SEPs were found when participants stood on the biomimetic surface. This was observed whether the forces exerted on the surface were self-generated or passively generated. Contrary to our prediction, we found that the sensory attenuation related to the self-generated movement did not significantly differ between the biomimetic and control surfaces. However, we observed an increase in gamma activity (30-50 Hz) over centroparietal regions during the preparation phase of the weight shift only when participants stood on the biomimetic surface. This result might suggest that gamma-band oscillations play an important functional role in processing behaviorally relevant stimuli during the early stages of body weight transfer.

A dedicate sensorimotor circuit enables fine texture discrimination by active touch.

Active touch facilitates environments exploration by voluntary, self-generated movements. However, the neural mechanisms underlying sensorimotor control for active touch are poorly understood. During foraging and feeding, Drosophila gather information on the properties of food (texture, hardness, taste) by constant probing with their proboscis. Here we identify a group of neurons (sd-L neurons) on the fly labellum that are mechanosensitive to labellum displacement and synapse onto the sugar-sensing neurons via axo-axonal synapses to induce preference to harder food. These neurons also feed onto the motor circuits that control proboscis extension and labellum spreading to provide on-line sensory feedback critical for controlling the probing processes, thus facilitating ingestion of less liquified food. Intriguingly, this preference was eliminated in mated female flies, reflecting an elevated need for softer food. Our results propose a sensorimotor circuit composed of mechanosensory, gustatory and motor neurons that enables the flies to select ripe yet not over-rotten food by active touch.

Distinguishing externally from saccade-induced motion in visual cortex

Distinguishing sensory stimuli caused by changes in the environment from those caused by an animal’s own actions is a hallmark of sensory processing1. Saccades are rapid eye movements that shift the image on the retina. How visual systems differentiate motion of the image induced by saccades from actual motion in the environment is not fully understood2. Here we discovered that in mouse primary visual cortex (V1) the two types of motion evoke distinct activity patterns. This is because, during saccades, V1 combines the visual input with a strong non-visual input arriving from the thalamic pulvinar nucleus. The non-visual input triggers responses that are specific to the direction of the saccade and the visual input triggers responses that are specific to the direction of the shift of the stimulus on the retina, yet the preferred directions of these two responses are uncorrelated. Thus, the pulvinar input ensures differential V1 responses to external and self-generated motion. Integration of external sensory information with information about body movement may be a general mechanism for sensory cortices to distinguish between self-generated and external stimuli.

Unperceived motor actions of the balance system interfere with the causal attribution of self-motion.

The instability of human bipedalism demands that the brain accurately senses balancing self-motion and determines whether movements originate from self-generated actions or external disturbances. Here, we challenge the longstanding notion that this process relies on a single representation of the body and world to accurately perceive postural orientation and organize motor responses to control balance self-motion. Instead, we find that the conscious sense of balance can be distorted by the corrective control of upright standing. Using psychophysics, we quantified thresholds to imposed perturbations and balance responses evoking cues of self-motion that are (in)distinguishable from corrective balance actions. When standing immobile, participants clearly perceived imposed perturbations. Conversely, when freely balancing, participants often misattributed their own corrective responses as imposed motion because their balance system had detected, integrated, and responded to the perturbation in the absence of conscious perception. Importantly, this only occurred for perturbations encoded ambiguously with balance-correcting responses and that remained below the natural variability of ongoing balancing oscillations. These findings reveal that our balance system operates on its own sensorimotor principles that can interfere with causal attribution of our actions, and that our conscious sense of balance depends critically on the source and statistics of induced and self-generated motion cues.

The rapid developmental rise of somatic inhibition disengages hippocampal dynamics from self-motion.

Early electrophysiological brain oscillations recorded in preterm babies and newborn rodents are initially mostly driven by bottom-up sensorimotor activity and only later can detach from external inputs. This is a hallmark of most developing brain areas, including the hippocampus, which, in the adult brain, functions in integrating external inputs onto internal dynamics. Such developmental disengagement from external inputs is likely a fundamental step for the proper development of cognitive internal models. Despite its importance, the developmental timeline and circuit basis for this disengagement remain unknown. To address this issue, we have investigated the daily evolution of CA1 dynamics and underlying circuits during the first two postnatal weeks of mouse development using two-photon calcium imaging in non-anesthetized pups. We show that the first postnatal week ends with an abrupt shift in the representation of self-motion in CA1. Indeed, most CA1 pyramidal cells switch from activated to inhibited by self-generated movements at the end of the first postnatal week, whereas the majority of GABAergic neurons remain positively modulated throughout this period. This rapid switch occurs within 2 days and follows the rapid anatomical and functional surge of local somatic GABAergic innervation. The observed change in dynamics is consistent with a two-population model undergoing a strengthening of inhibition. We propose that this abrupt developmental transition inaugurates the emergence of internal hippocampal dynamics.

Brain-Inspired Spiking Neural Network Controller for a Neurorobotic Whisker System.

It is common for animals to use self-generated movements to actively sense the surrounding environment. For instance, rodents rhythmically move their whiskers to explore the space close to their body. The mouse whisker system has become a standard model for studying active sensing and sensorimotor integration through feedback loops. In this work, we developed a bioinspired spiking neural network model of the sensorimotor peripheral whisker system, modeling trigeminal ganglion, trigeminal nuclei, facial nuclei, and central pattern generator neuronal populations. This network was embedded in a virtual mouse robot, exploiting the Human Brain Project's Neurorobotics Platform, a simulation platform offering a virtual environment to develop and test robots driven by brain-inspired controllers. Eventually, the peripheral whisker system was adequately connected to an adaptive cerebellar network controller. The whole system was able to drive active whisking with learning capability, matching neural correlates of behavior experimentally recorded in mice.

0131 Theta oscillations during REM sleep synchronize behavior and neural activity in the developing motor system

Abstract Introduction Myoclonic twitches are abundantly produced during REM sleep in skeletal muscles across the body. In infant rats, movements are produced by the red nucleus (RN), with the RN both sending motor commands and receiving sensory feedback from twitches. The RN’s role in producing twitches contrasts with that of primary motor cortex (M1), which does not generate motor commands at early postnatal ages. Instead, M1 functions as a sensory structure, processing sensory feedback from self-generated movements, including twitches. By postnatal day (P) 12, the RN (but not M1) also begins to exhibit a continuous theta rhythm (~6 Hz) during REM sleep that promotes sensorimotor integration with other brain areas. Given that the RN and M1 collaborate to control movement in adult rats, we hypothesized that theta emerges in M1 after P12, at which time theta synchronizes M1 and RN activity. Methods To determine if and when theta synchronizes activity in the RN and M1, we recorded local field potentials and unit activity in the RN and the forelimb region of M1 in unanesthetized preweanling rats at P12 and P20. Rats were head-fixed but were able to locomote and cycle freely between sleep and wake. Results Neurons in the RN and M1 continued to respond to twitches through P20. Further, as predicted, we observed the developmental emergence of REM-associated theta oscillations in M1 by P20 that were coherent with theta in the RN. Additionally, neural activity was phase-locked to theta; surprisingly, twitches were also phase-locked to theta, with twitches being more likely during the troughs of the oscillation. Finally, the temporal relationship between twitch-related activity in the two structures depended on the phase of theta, with twitch-related activity in M1 lagging behind twitch-related activity in the RN in the rising phase of theta. However, in the falling phase of theta, twitch-related activity in the RN and M1 showed similar time courses. Conclusion These results show how theta during REM sleep promotes the developmental integration of behavior with neural activity in the RN and M1. Because synchronous activity strengthens synaptic connectivity, and theta synchronized twitch-related activity in the RN and M1, these results also implicate twitches and twitch-related activity in the development of somatotopically precise functional connectivity between the RN and M1. Support (If Any) R37-HD081168 to M.S.B. and SRSF Career Development Award to J.C.D.

Mislocalization in saccadic suppression of displacement

Visual stability across saccades requires us to discriminate self-generated motion by eye movements from motion occurring in the external world. In the laboratory visual stability is often studied by asking observers to discriminate the direction of trans-saccadic target displacements. It is a well established finding that in this paradigm performance is usually very poor. If observers are insensitive to the intra-saccadic motion and see the pre- and the post-saccadic target in one location, one of both targets should be reported as shifted when observers would localize them. Here, I asked participants to perform a saccade to a target. During saccade execution the target was displaced either in backward or forward direction. After finishing the saccade, subjects had to report the position of either the pre-or the post-saccadic target. I found that subjects mislocalized the pre-saccadic target to the physical position of the post-saccadic target. This mislocalization occurred only after backward but not after forward displacements.

Human psychophysical discrimination of spatially dependant Pancharatnam\u2013Berry phases in optical spin-orbit states

We tested the ability of human observers to discriminate distinct profiles of spatially dependant geometric phases when directly viewing stationary structured light beams. Participants viewed polarization coupled orbital angular momentum (OAM) states, or “spin-orbit” states, in which the OAM was induced through Pancharatnam–Berry phases. The coupling between polarization and OAM in these beams manifests as spatially dependant polarization. Regions of uniform polarization are perceived as specifically oriented Haidinger’s brushes, and study participants discriminated between two spin-orbit states based on the rotational symmetry in the spatial orientations of these brushes. Participants used self-generated eye movements to prevent adaptation to the visual stimuli. After initial training, the participants were able to correctly discriminate between two spin-orbit states, differentiated by OAM =pm 1, with an average success probability of 69% (S.D. = 22%, p = 0.01). These results support our previous observation that human observers can directly perceive spin-orbit states, and extend this finding to non-rotating beams, OAM modes induced via Pancharatnam–Berry phases, and the discrimination of states that are differentiated by OAM.

Imagery adds stimulus-specific sensory evidence to perceptual detection.

Internally generated imagery and externally triggered perception rely on overlapping sensory processes. This overlap poses a challenge for perceptual reality monitoring: determining whether sensory signals reflect reality or imagination. In this study, we used psychophysics to investigate how imagery and perception interact to determine visual experience. Participants were instructed to detect oriented gratings that gradually appeared in noise while simultaneously either imagining the same grating, a grating perpendicular to the to-be-detected grating, or nothing. We found that, compared to both incongruent imagery and no imagery, congruent imagery caused a leftward shift of the psychometric function relating stimulus contrast to perceptual threshold. We discuss how this effect can best be explained by a model in which imagery adds sensory signal to the perceptual input, thereby increasing the visibility of perceived stimuli. These results suggest that, in contrast to changes in sensory signals caused by self-generated movement, the brain does not discount the influence of self-generated sensory signals on perception.

Infants' Attributions of Insides and Animacy in Causal Interactions.

Past work has found that infants show more interest when an object that has at least two properties of animate beings, such as engaging in self-generated motion and having fur, is shown to be hollow than when an object with none or one of these properties is revealed to be hollow. When an object is grabbed by a hand and moved to a new place, by 7 months of age, infants explain the motion of the object as due to the hand, and thus do not interpret this object as capable of self-generated motion. This constant application of force is called an "entraining" event. Other work has found that 6-month-old infants are sensitive to the reversals of causal roles in "launching" events (billiard-ball-like collisions), but not entraining events. Here, we examine whether 10-month-old infants explain the motion of the patient in a launching event as being due to the contact with the launching agent. Experiment 1 replicates past work, showing that infants look longer when a self-propelled object with animate features (fur or feathers) is shown to be hollow, compared to a similar object undergoing spatiotemporally identical motion entrained by a human agent. Experiment 2 finds that infants look equally at the agent and patient, both covered by fur or feathers, of a launching event when each is revealed to be hollow. Experiment 3 shows that infants look longer when a fur-covered causal patient is shown to be hollow compared to a plain-box causal agent, indicating that 10-month-old infants do not explain the motion of the causal patient of a launching event as due to the agent, even though they do so for an entraining event. This dissociation suggests the existence of multiple independent causal representations in the first year of life.

An electrically coupled pioneer circuit enables motor development via proprioceptive feedback in Drosophila embryos

Precocious movements are widely seen in embryos of various animal species. Whether such movements via proprioceptive feedback play instructive roles in motor development or are a mere reflection of activities in immature motor circuits is a long-standing question. Here we image the emerging motor activities in Drosophila embryos that lack proprioceptive feedback and show that proprioceptive experience is essential for the development of locomotor central pattern generators (CPGs). Downstream of proprioceptive inputs, we identify a pioneer premotor circuit composed of two pairs of segmental interneurons, whose gap-junctional transmission requires proprioceptive experience and plays a crucial role in CPG formation. The circuit autonomously generates rhythmic plateau potentials via IP3-mediated Ca2+ release from internal stores, which contribute to muscle contractions and hence produce proprioceptive feedback. Our findings demonstrate the importance of self-generated movements in instructing motor development and identify the cells, circuit, and physiology at the core of this proprioceptive feedback.

Where in the Brain is “the Other’s” Hand? Mapping Dysfunctional Neural Networks in Somatoparaphrenia

Somatoparaphrenia refers to the delusional belief, typically observed in right brain-damaged patients, that the contralesional limbs belong to someone else. Here, we aimed to uncover the neural activity associated with this productive, i.e. confabulatory, component in a patient, S.P.P., with a large right-sided lesion of both cortical and subcortical gray and white matter. He claimed that his left paralyzed hand belonged to his mother. In a block-design functional magnetic resonance (fMRI) experiment, S.P.P. imagined that the mother would move her (i.e. his left) hand (condition “mother”). Subtraction of the activity elicited by control conditions (imagery of self-generated movement of either left or right hand) from that in the “mother” condition resulted in the focal activation of the pars opercularis of the right inferior frontal gyrus (rIFG). In a separate, resting-state fMRI experiment with S.P.P. and 21 healthy controls, we examined the functional connectivity of the rIFG and the affected hand somatosensory network to the rest of the brain. We found a negative correlation between the activity in the rIFG and that of Broca area and the temporo-parietal junction in the left hemisphere. Furthermore, the affected hand somatosensory network was disconnected from the left secondary somatosensory cortex. Our results link the productive component of somatoparaphrenia to the activity of crucial hubs for integrating the multimodal signals of the affected hand. Furthermore, they provide the first direct evidence supporting the “left narrator model”, proposed by Halligan et al. (1995), according to which the confabulations of somatoparaphrenia are due to a disconnection of left hemisphere language areas from right hemisphere parieto-temporal cortex.