Neural populations within macaque early vestibular pathways are adapted to encode natural self-motion.

How the activities of large neural populations are integrated in the brain to ensure accurate perception and behavior remains a central problem in systems neuroscience. Here, we investigated population coding of naturalistic self-motion by neurons within early vestibular pathways in rhesus macaques (Macacca mulatta). While vestibular neurons displayed similar dynamic tuning to self-motion, inspection of their spike trains revealed significant heterogeneity. Further analysis revealed that, during natural but not artificial stimulation, heterogeneity resulted primarily from variability across neurons as opposed to trial-to-trial variability. Interestingly, vestibular neurons displayed different correlation structures during naturalistic and artificial self-motion. Specifically, while correlations due to the stimulus (i.e., signal correlations) did not differ, correlations between the trial-to-trial variabilities of neural responses (i.e., noise correlations) were instead significantly positive during naturalistic but not artificial stimulation. Using computational modeling, we show that positive noise correlations during naturalistic stimulation benefits information transmission by heterogeneous vestibular neural populations. Taken together, our results provide evidence that neurons within early vestibular pathways are adapted to the statistics of natural self-motion stimuli at the population level. We suggest that similar adaptations will be found in other systems and species.

Sensory adaptation mediates efficient and unambiguous encoding of natural stimuli by vestibular thalamocortical pathways.

Sensory systems must continuously adapt to optimally encode stimuli encountered within the natural environment. The prevailing view is that such optimal coding comes at the cost of increased ambiguity, yet to date, prior studies have focused on artificial stimuli. Accordingly, here we investigated whether such a trade-off between optimality and ambiguity exists in the encoding of natural stimuli in the vestibular system. We recorded vestibular nuclei and their target vestibular thalamocortical neurons during naturalistic and artificial self-motion stimulation. Surprisingly, we found no trade-off between optimality and ambiguity. Using computational methods, we demonstrate that thalamocortical neural adaptation in the form of contrast gain control actually reduces coding ambiguity without compromising the optimality of coding under naturalistic but not artificial stimulation. Thus, taken together, our results challenge the common wisdom that adaptation leads to ambiguity and instead suggest an essential role in underlying unambiguous optimized encoding of natural stimuli.

Context-independent encoding of passive and active self-motion in vestibular afferent fibers during locomotion in primates.

The vestibular system detects head motion to coordinate vital reflexes and provide our sense of balance and spatial orientation. A long-standing hypothesis has been that projections from the central vestibular system back to the vestibular sensory organs (i.e., the efferent vestibular system) mediate adaptive sensory coding during voluntary locomotion. However, direct proof for this idea has been lacking. Here we recorded from individual semicircular canal and otolith afferents during walking and running in monkeys. Using a combination of mathematical modeling and nonlinear analysis, we show that afferent encoding is actually identical across passive and active conditions, irrespective of context. Thus, taken together our results are instead consistent with the view that the vestibular periphery relays robust information to the brain during primate locomotion, suggesting that context-dependent modulation instead occurs centrally to ensure that coding is consistent with behavioral goals during locomotion.

Challenges to the Vestibular System in Space: How the Brain Responds and Adapts to Microgravity.

In the next century, flying civilians to space or humans to Mars will no longer be a subject of science fiction. The altered gravitational environment experienced during space flight, as well as that experienced following landing, results in impaired perceptual and motor performance-particularly in the first days of the new environmental challenge. Notably, the absence of gravity unloads the vestibular otolith organs such that they are no longer stimulated as they would be on earth. Understanding how the brain responds initially and then adapts to altered sensory input has important implications for understanding the inherent abilities as well as limitations of human performance. Space-based experiments have shown that altered gravity causes structural and functional changes at multiple stages of vestibular processing, spanning from the hair cells of its sensory organs to the Purkinje cells of the vestibular cerebellum. Furthermore, ground-based experiments have established the adaptive capacity of vestibular pathways and neural mechanism that likely underlie this adaptation. We review these studies and suggest that the brain likely uses two key strategies to adapt to changes in gravity: (i) the updating of a cerebellum-based internal model of the sensory consequences of gravity; and (ii) the re-weighting of extra-vestibular information as the vestibular system becomes less (i.e., entering microgravity) and then again more reliable (i.e., return to earth).

Neural variability determines coding strategies for natural self-motion in macaque monkeys.

We have previously reported that central neurons mediating vestibulo-spinal reflexes and self-motion perception optimally encode natural self-motion (Mitchell et al., 2018). Importantly however, the vestibular nuclei also comprise other neuronal classes that mediate essential functions such as the vestibulo-ocular reflex (VOR) and its adaptation. Here we show that heterogeneities in resting discharge variability mediate a trade-off between faithful encoding and optimal coding via temporal whitening. Specifically, neurons displaying lower variability did not whiten naturalistic self-motion but instead faithfully represented the stimulus' detailed time course, while neurons displaying higher variability displayed temporal whitening. Using a well-established model of VOR pathways, we demonstrate that faithful stimulus encoding is necessary to generate the compensatory eye movements found experimentally during naturalistic self-motion. Our findings suggest a novel functional role for variability toward establishing different coding strategies: (1) faithful stimulus encoding for generating the VOR; (2) optimized coding via temporal whitening for other vestibular functions.

Learning to use vestibular sense for spatial updating is context dependent.

As we move, perceptual stability is crucial to successfully interact with our environment. Notably, the brain must update the locations of objects in space using extra-retinal signals. The vestibular system is a strong candidate as a source of information for spatial updating as it senses head motion. The ability to use this cue is not innate but must be learned. To date, the mechanisms of vestibular spatial updating generalization are unknown or at least controversial. In this paper we examine generalization patterns within and between different conditions of vestibular spatial updating. Participants were asked to update the position of a remembered target following (offline) or during (online) passive body rotation. After being trained on a single spatial target position within a given task, we tested generalization of performance for different spatial targets and an unpracticed spatial updating task. The results demonstrated different patterns of generalization across the workspace depending on the task. Further, no transfer was observed from the practiced to the unpracticed task. We found that the type of mechanism involved during learning governs generalization. These findings provide new knowledge about how the brain uses vestibular information to preserve its spatial updating ability.

Cerebellar Prediction of the Dynamic Sensory Consequences of Gravity.

As we go about our everyday activities, our brain computes accurate estimates of both our motion relative to the world and our orientation relative to gravity. However, how the brain then accounts for gravity as we actively move and interact with our environment is not yet known. Here, we provide evidence that, although during passive movements, individual cerebellar output neurons encode representations of head motion and orientation relative to gravity, these gravity-driven responses are cancelled when head movement is a consequence of voluntary generated movement. In contrast, the gravity-driven responses of primary otolith and semicircular canal afferents remain intact during both active and passive self-motion, indicating the attenuated responses of central neurons are not inherited from afferent inputs. Taken together, our results are consistent with the view that the cerebellum builds a dynamic prediction (e.g., internal model) of the sensory consequences of gravity during active self-motion, which in turn enables the preferential encoding of unexpected motion to ensure postural and perceptual stability.

Visual Online Control of Goal-Directed Aiming Movements in Children.

The present study investigated whether the initial impulse of goal-directed movements was visually monitored by 5- to 12-years-old children (n = 36) in a manner similar to adults (n = 12). The participants moved a cursor toward a fixed target. In some trials, the cursor was unpredictably translated by 20 mm following movement initiation. The results showed that even the youngest children visually monitor the initial impulse of goal-directed movements. This monitoring and the error correction process that it triggers seem automatic because it occurs even when the cursor jump is not consciously detected. Finally, it appears that this process does not fully mature before late childhood, which suggests that a putative dedicated channel for processing visual hand information develops during childhood.

Childhood obesity affects postural control and aiming performance during an upper limb movement.

Obesity reduces the efficiency of postural and movement control mechanisms. However, the effects of obesity on a functional motor task and postural control in standing and seated position have not been closely quantified among children. The aim of this study is to examine the effects of obesity on the execution of aiming tasks performed in standing and seated conditions in children. Twelve healthy weight children and eleven obese children aged between 8 and 11 years pointed to a target in standing and seated position. The difficulty of the aiming task was varied by using 2 target sizes (1.0 cm and 5.0 cm width; pointing to the smaller target size needs a more precise movement and constitutes a more difficult task). Hand movement time (MT) and its phases were measured to quantify the aiming task. Mean speed of the center of pressure displacement (COP speed) was calculated to assess postural stability during the movement. Obese children had significantly higher MTs compared to healthy-weight children in seated and standing conditions explained by greater durations of deceleration phase when aiming. Concerning the COP speed during the movement, obese children showed significantly higher values when standing compared to healthy-weight children. This was also observed in the seated position. In conclusion, obesity adds a postural constraint during an aiming task in both seated and standing conditions and requires obese children to take more time to correct their movements due to a greater postural instability of the body when pointing to a target with the upper-limb.

Is visual-based, online control of manual-aiming movements disturbed when adapting to new movement dynamics?

Previous research has shown that for goal-directed movements, online visual feedback is not necessary for the adaptation of movement planning to novel movement dynamics. In the present study, we wanted to put this proposition to a stringent test and determine whether the usually dominant role of online visual feedback in movement control is diminished when goal-directed movements are performed in a condition that modifies limb dynamics. Participants performed a video-aiming task while the center of mass of their forearm was experimentally displaced by a 1.5-kg mass attached laterally to its longitudinal axis. A cursor representing the position of the participant's hand was either visible or not visible during the acquisition phase. Then, in a transfer test, the participants performed the task without online visual feedback and either with or without the lateral mass. During the acquisition phase, the participants adapted to the new movement dynamics imposed by the added mass regardless of whether online visual feedback was available. An important new finding of the present study was the observation that the role usually played by online visual feedback in refining movement planning and ensuring control of the initial portion of goal-directed movements was suppressed during adaptation to novel movement dynamics. This resulted in an increase in the role played by visual feedback late in the movement to ensure endpoint accuracy.

Developmental aspects of pluriarticular movement control.

Precise pluriarticular movement control is required to perform straight and smooth out-and-back movements. Our goal was to determine whether children perform out-and-back movements as accurately as adults do in the presence and absence of visual feedback. To reach our goal, 36 children aged between 6 and 12 years, and 12 young adults, performed an out-and-back movement in a normal-vision condition and in a target-only condition. Reversal angle and overlapping error were taken to represent the ability of children to control pluriarticular movement. The results showed that adults exhibited sharper movement reversal than the three children groups did, but only for eccentric targets relative to their midline. This suggests that pluriarticular movement control improved across the course of development for eccentric regions of the workspace. Visual feedback did not result in sharper movement reversal even when relatively large errors were noted (eccentric targets in children). This underlines the relatively minor role of visual feedback for interjoint coordination when proprioception is intact. Finally, we observed that directional variability was smaller at the 100-ms mark for the back than for the out portion of the movement, suggesting that movement-planning processes appear less variable when based on dynamic rather than static afferent information.

Specificity of practice results from differences in movement planning strategies.

Withdrawing visual feedback after practice of a manual aiming task results in a severe decrease in aiming accuracy. This decrease in accuracy is such that participants are often less accurate than controls who are beginning practice of the task without visual feedback. These results have been interpreted as evidence that motor learning is specific to the sources of afferent information optimizing performance, because it could be processed at the exclusion of other sources of afferent information. The goal of the present study was to test this hypothesis. To reach our goal we evaluated whether online visual feedback prevented kinesthetic information to be used for: (1) eliminating movement anisotropy resulting from difference in limb inertia when aiming in different directions and (2) creating an internal model of limb mechanics. Participants practiced a manual aiming task with or without visual feedback and with knowledge of results. After this acquisition phase, participants performed two transfer tests. The first transfer test was performed without visual feedback and/or knowledge of results. The second transfer test was similar to the first one but participants initiated their movements from a different starting base. The results showed strong specificity effects in that withdrawing visual feedback resulted in large pointing bias and variability. However, the results of the two transfer tests showed that the processing of visual feedback did not prevent the processing of kinesthetic information used to eliminate movement anisotropy or to create an internal model of limb mechanics. Rather, specificity of practice effects resulted from participants using the same motor plan in transfer as they did in acquisition even though they had no longer access to visual feedback to modulate their movement online. These results indicate that during acquisition participants adopted different movement planning strategies depending on the source of afferent information available.