Do we use a priori knowledge of gravity when making elbow rotations?

In this study, we aim to investigate whether motor commands, emanating from movement planning, are customized to movement orientation relative to gravity from the first trial on. Participants made fast point-to-point elbow flexions and extensions in the transverse plane. We compared movements that had been practiced in reclined orientation either against or with gravity with the same movement relative to the body axis made in the upright orientation (neutral compared to gravity). For each movement type, five rotations from reclined to upright orientation were made. For each rotation, we analyzed the first trial in upright orientation and the directly preceding trial in reclined orientation. Additionally, we analyzed the last five trials of a 30-trial block in upright position and compared these trials with the first trials in upright orientation. Although participants moved fast, gravitational torques were substantial. The change in body orientation affected movement planning: we found a decrease in peak angular velocity and a decrease in amplitude for the first trials made in the upright orientation, regardless of whether the previous movements in reclined orientation were made against or with gravity. We found that these decreases disappeared after participants familiarized themselves with moving in upright position in a 30-trial block. These results indicate that participants used a general strategy, corresponding to the strategy observed in situations with unreliable or limited information on external conditions. From this, we conclude that during movement planning, a priori knowledge of gravity was not used to specifically customize motor commands for the neutral gravity condition

Do Gravity-Related Sensory Information Enable the Enhancement of Cortical Proprioceptive Inputs When Planning a Step in Microgravity?

International audienceWe recently found that the cortical response to proprioceptive stimulation was greater when participants were planning a step than when they stood still, and that this sensory facilitation was suppressed in microgravity. The aim of the present study was to test whether the absence of gravity-related sensory afferents during movement planning in microgravity prevented the proprioceptive cortical processing to be enhanced. We reestablished a reference frame in microgravity by providing and translating a horizontal support on which the participants were standing and verified whether this procedure restored the proprioceptive facilitation. The slight translation of the base of support (lateral direction), which occurred prior to step initiation, stimulated at least cutaneous and vestibular receptors. The sensitivity to proprioceptive stimulation was assessed by measuring the amplitude of the cortical somatosensory-evoked potential (SEP, over the Cz electrode) following the vibration of the leg muscle. The vibration lasted 1 s and the participants were asked to either initiate a step at the vibration offset or to remain still. We found that the early SEP (90–160 ms) was smaller when the platform was translated than when it remained stationary, revealing the existence of an interference phenomenon (i.e., when proprioceptive stimulation is preceded by the stimulation of different sensory modalities evoked by the platform translation). By contrast, the late SEP (550 ms post proprioceptive stimulation onset) was greater when the translation preceded the vibration compared to a condition without pre-stimulation (i.e., no translation). This suggests that restoring a body reference system which is impaired in microgravity allowed a greater proprioceptive cortical processing. Importantly, however, the late SEP was similarly increased when participants either produced a step or remained still. We propose that the absence of step-induced facilitation of proprioceptive cortical processing results from a decreased weight of proprioception in the absence of balance constraints in microgravity

Vertical frames of reference and control of body orientation.

International audienceThe present paper aims at critically reviewing the most outstanding and recent studies regarding the control of body orientation in the vertical space. A first part defines the general concepts used throughout this manuscript. The second part investigates the vertical perception and the main factors which affect it, while trying to overcome the five areas of theoretical and experimental controversies we have identified in the literature. The third part of this review presents the different theoretical models of the vertical perception and body orientation in space. Finally, the last part focuses on the functional coupling between perception of the vertical and orientation of the body in space. It considers more particularly how these two dimensions interact for explaining the observed behaviors

Influence of multisensory graviceptive information on the apparent zenith

We studied the contribution of vestibular and somatosensory/proprioceptive stimulation to the perception of the apparent zenith (AZ). Experiment 1 involved rotation on a centrifuge and settings of the AZ. Subjects were supine on the centrifuge, and their body position was varied in relation to the rotation axis so that the gravitoinertial resultant force at the otoliths was 1 or 1.2 g with the otolith organs positioned 50 or 100 cm from the axis of rotation. Their legs were also positioned in different configurations, elevated or extended, to create different distributions of blood and lymph. Experiment 2 involved (a) settings of the AZ for subjects positioned supine with legs fully extended or legs elevated to create a torso-ward shift of blood and (b) settings of the subjective visual vertical for subjects horizontally positioned on their sides with legs extended or bent. Experiment 3 had subjects in the same body configurations as in Experiment 2 indicate when they were horizontal as they were rotated in pitch or roll about an inter-aural or naso-occipital axis. The experimental results for all three experiments demonstrated that both visual localization and apparent body horizontal are jointly determined by multimodal combinations of otolithic and somatosensory/proprioceptive stimulation. No evidence was found for non-overlapping or exclusive mechanisms determining one or the other. The subjective postural horizontal and AZ were affected in similar ways by comparable manipulations

Statistics of the vestibular input experienced during natural self-motion: implications for neural processing

It is widely believed that sensory systems are optimized for processing stimuli occurring in the natural environment. However, it remains unknown whether this principle applies to the vestibular system, which contributes to essential brain functions ranging from the most automatic reflexes to spatial perception and motor coordination. Here we quantified, for the first time, the statistics of natural vestibular inputs experienced by freely moving human subjects during typical everyday activities. Although previous studies have found that the power spectra of natural signals across sensory modalities decay as a power law (i.e., as 1/f(α)), we found that this did not apply to natural vestibular stimuli. Instead, power decreased slowly at lower and more rapidly at higher frequencies for all motion dimensions. We further establish that this unique stimulus structure is the result of active motion as well as passive biomechanical filtering occurring before any neural processing. Notably, the transition frequency (i.e., frequency at which power starts to decrease rapidly) was lower when subjects passively experienced sensory stimulation than when they actively controlled stimulation through their own movement. [...

Strong correlations between sensitivity and variability give rise to constant discrimination thresholds across the otolith afferent population

The vestibular system is vital for our sense of linear self-motion. At the earliest processing stages, the otolith afferents of the vestibularnerve encode linear motion. Their resting discharge regularity has long been known to span a wide range, suggesting an important role insensory coding, yet to date, the question of how this regularity alters the coding of translational motion is not fully understood. Here, werecorded from single otolith afferents in macaque monkeys during linear motion along the preferred directional axis of each afferent overa wide range of frequencies (0.5–16 Hz) corresponding to physiologically relevant stimulation. We used signal-detection theory todirectly measure neuronal thresholds and found that values for single afferents were substantially higher than those observed for humanperception evenwhena Kaiser filter was used to provide an estimate of firing rate. Surprisingly,wefurther found that neuronal thresholdswere independent of both stimulus frequency and resting discharge regularity. This was because increases in trial-to-trial variability werematched by increases in sensitivity such that their ratio remains constant: a coding strategy that markedly differs from that used bysemicircular canal vestibular afferents to encode rotations. Finally, using Fisher information, we show that pooling the activities ofmultiple otolith afferents gives rise to neural thresholds comparable with those measured for perception. Together, our results stronglysuggest that higher-order structures integrate inputs across afferent populations to provide our sense of linear motion and provideunexpected insight into the influence of variability on sensory encoding

Envelope statistics of self-motion signals experienced by human subjects during everyday activities: Implications for vestibular processing

There is accumulating evidence that the brain's neural coding strategies are constrained bynatural stimulus statistics. Here we investigated the statistics of the time varying envelope(i.e. a second-order stimulus attribute that is related to variance) of rotational and translationalself-motion signals experienced by human subjects during everyday activities. Wefound that envelopes can reach large values across all six motion dimensions (~450 deg/sfor rotations and ~4 G for translations). Unlike results obtained in other sensory modalities,the spectral power of envelope signals decreased slowly for low (< 2 Hz) and more sharplyfor high (>2 Hz) temporal frequencies and thus was not well-fit by a power law. We nextcompared the spectral properties of envelope signals resulting from active and passive selfmotion,as well as those resulting from signals obtained when the subject is absent (i.e.external stimuli). Our data suggest that different mechanisms underlie deviation from scaleinvariance in rotational and translational self-motion envelopes. Specifically, active selfmotionand filtering by the human body cause deviation from scale invariance primarily fortranslational and rotational envelope signals, respectively. Finally, we used well-establishedmodels in order to predict the responses of peripheral vestibular afferents to natural envelopestimuli. [...

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

Signal correlations are similar during artificial and naturalistic stimulation.

(A) Left: Schematic showing a hypothetical scenario in which the activities of 2 neurons are modulated by a common signal, which gives rise to signal correlations as well as by independent noise sources. In this case, because the noises are independent, there are no noise correlations. Right: Schematic showing a hypothetical scenario similar to the one described for panel A except that a source of shared noise has been added, which will give rise to noise correlations. Such shared noise could in principle originate from lateral connections as well as shared afferent input. (B) Methodology used to calculate signal correlation between the response of pair of VO neurons. The unit activity of cell 1 and cell 2 from Fig 2B is shown. Top: For each cell, the number of spikes is counted for a given timescale (e.g., 250 ms) and spike count sequences are generated. Bottom: The spike count sequence for the second neuron is shuffled to exclude the effect noise correlations due to simultaneous common input. The signal correlation for the timescale is calculated by computing Pearson’s correlation coefficient between the latter spike count sequences. (C) Signal correlations as a function of timescale during naturalistic stimulus (N = 820 pairs). The solid and dashed lines represent the correlations for the same-type and opposite-type pairs, respectively. The thick solid and dashed lines are the average values of the correlations for the same-type and opposite-type pairs, respectively. (D) Same as in C except it was calculated for an artificial stimulus (f = 4 Hz; N = 780 pairs). (E) Boxplots showing the signal correlation values during artificial (all frequencies) and naturalistic stimuli. Signal correlations during artificial and naturalistic stimuli are not significantly different (two-sample t test, N = 861 pairs, p = 0.83). For artificial stimuli, the timescale was chosen to be a quarter to a half-period of the sinewave period, where the signal correlations were maximum in magnitude on average. For naturalistic stimulus, the signal correlations were calculated for a 100 ms timescale that was consistent with the time scale of the stimulus and where signal correlations were highest in magnitude. In panels C and D, while the average values were calculated using all the pairs, only 75 traces of same and opposite-type pairs were shown for visualization purposes. Note that data were computed over different pairings during naturalistic and artificial stimulation, this is because not all pairs were held during both protocols. The data for this panel are available from the Borealis database (https://doi.org/10.5683/SP3/FXFZ2J) (see files “Fig 4E.mat,” “Fig 4E.m,” and associated “readme.txt”).</p