Jérome Carriot

A prevailing view is that Weber’s law constitutes a fundamental principle of perception. This widely accepted psychophysical law states that the minimal change in a given stimulus that can be perceived increases proportionally with amplitude and has been observed across systems and species in hundreds of studies. Importantly, however, Weber’s law is actually an oversimplification. Notably, there exist violations of Weber’s law that have been consistently observed across sensory modalities. Specifically, perceptual performance is better than that predicted from Weber’s law for the higher stimulus amplitudes commonly found in natural sensory stimuli. To date, the neural mechanisms mediating such violations of Weber’s law in the form of improved perceptual performance remain unknown. Here, we recorded from vestibular thalamocortical neurons in rhesus monkeys during self-motion stimulation. Strikingly, we found that neural discrimination thresholds initially increased but saturated for higher stimulus amplitudes, thereby causing the improved neural discrimination performance required to explain perception. Theory predicts that stimulus-dependent neural variability and/or response nonlinearities will determine discrimination threshold values. Using computational methods, we thus investigated the mechanisms mediating this improved performance. We found that the structure of neural variability, which initially increased but saturated for higher amplitudes, caused improved discrimination performance rather than response nonlinearities. Taken together, our results reveal the neural basis for violations of Weber’s law and further provide insight as to how variability contributes to the adaptive encoding of natural stimuli with continually varying statistics.

It is commonly assumed that the brain’s neural coding strategies are adapted to the statistics of natural stimuli. Specifically, to maximize information transmission, a sensory neuron’s tuning function should effectively oppose the decaying stimulus spectral power, such that the neural response is temporally decorrelated (i.e. ‘whitened’). However, theory predicts that the structure of neuronal variability also plays an essential role in determining how coding is optimized. Here, we provide experimental evidence supporting this view by recording from neurons in early vestibular pathways during naturalistic self-motion. We found that central vestibular neurons displayed temporally whitened responses that could not be explained by their tuning alone. Rather, computational modeling and analysis revealed that neuronal variability and tuning were matched to effectively complement natural stimulus statistics, thereby achieving temporal decorrelation and optimizing information transmission...

Ce travail doctoral s'interesse aux similitudes et differences comportementales qu'engendrent une mclinaison reelle et simulee par acceleration lineaire (centrifugation, illusions somatogravique et oculogravique). En desaccord avec l'ambiguite inclinaison/translation du systeme otolithique, les trois premieres experiences mettent en evidence qu'une meme orientation par rapport a la gravite (G) pour l'inclinaison reelle ou aux forces gravito-inertielles (GiF) en centrifugeuse n'induit pas la meme perception de l'horizon. Les ajustements visuels et proprio-kinesthesiques realises en centrifugeuse sont toujours au-dessus de ceux observes en environnement gravitaire. Cet abaissement de l'horizon gravitaire en centrifugeuse s'expliquerait en partie par un decalage illusoire de la reference egocentree, probablement lie aux contraintes mecaniques engendrees au niveau des effecteurs par l'augmentation de l'intensite de la force. Une deuxieme serie d'experiences suggere que l'intensite de l'illusion oculogravique peut etre modifiee par l'experience des variations inertielles. La derniere experience met en exergue le role important des signaux somesthesiques dans l'illusion oculogravique. D'une part, pour une distance donnee fixe entre le systeme vestibulaire et l'axe de rotation (force centrifuge semblable sur les otolithes), le simple fait d'allonger les jambes (variation de la distance entre les differentes parties du corps et l'axe de rotation) module l'amplitude de l'illusion oculogravique. D'autre part, lorsque les otolithes ne sont pas affectes par la force de centrifugation, et que les gravicepteurs somesthesiques sont soumis a un changement en direction et en amplitude de la gravite, on observe un deplacement de la localisation de l'horizon dans la direction de GiF appliquee au niveau du centre de masse. L'ensemble des resultats permet d'aborder l'illusion oculogravique sous l'angle d'un modele interne de la gravite. La remanence de la perception d'inclinaison en centrifugation serait liee a la difficulte pour l'individu d'associer la stimulation somesthesique engendree par l'acceleration lineaire, a un alignement de son propre corps sur ce modele interne (conflit cognitif).

<p><b>A:</b> Schematic showing the MEMS module (gold box) located on the subject’s head and placed on the seat during passive self-motion. <b>B,C,D,E, F, G:</b> Trial-averaged power spectra of signals in the external environment (green) during passive self-motion for inter aural (<b>B</b>), Fore-Aft (<b>C</b>), Vertical (<b>D</b>), LARP (<b>E</b>), RALP (<b>F</b>), and YAW (<b>G</b>). The power spectra were in general well fit by a single power law over the entire frequency range (blue lines).</p

<p><b>A:</b> Subject-averaged best-fit power law exponents over the low (gray) and high (black) frequency ranges for all six motion dimensions for active self-motion. Also shown for comparison are the subject-averaged best-fit power law exponents for a single power law over the entire frequency range (blue). <b>B:</b> Subject-averaged best-fit power law exponents over the low (gray) and high (black) frequency ranges for all six motion dimensions for passive self-motion. Also shown for comparison are the subject-averaged best-fit power law exponents for a single power law over the entire frequency range (blue). “*” indicates statistical significance at the p = 0.01 level using a one-way ANOVA.</p

<p><b>A:</b> Schematic showing the vestibular end organs as well as regular and irregular vestibular afferents projecting to the vestibular nuclei. <b>B:</b> Sensitivity to the carrier for the regular (dashed black) and irregular (solid red) model afferents. <b>C:</b> Time series showing a segment of the envelope stimulus (solid black) and the responses of the model regular (dashed black) and irregular (solid red) afferents. <b>D:</b> Gain to the envelope as a function of frequency for the regular (dashed black) and irregular (solid red) model afferents. In both cases the gain is relatively independent of frequency but is about twice higher for the irregular model afferent.</p

<p><b>A:</b> Schematic showing a subject engaged in active self-motion (left) and in passive self-motion (right). <b>B,C,D,E, F, G:</b> Subject-averaged envelope power spectra for active (left panels) and passive (right panels) activities for inter aural (<b>B</b>), Fore-Aft (<b>C</b>), Vertical (<b>D</b>), LARP (<b>E</b>), RALP (<b>F</b>), and YAW (<b>G</b>). In each case, the power spectra were fitted using two power laws over the low and high frequency ranges (black lines) as well as by a single power law over the entire frequency range (blue lines). Also shown are the best-fit power law exponents with confidence interval as well as the transition frequency.</p

<p><b>A:</b> Subject-averaged power spectra (red lines) with best-fit power laws over the low and high frequency ranges (black lines) as well as best-fit single power law over the entire frequency range (blue lines). Also shown are the best-fit power law exponents with confidence interval as well as the transition frequency. The dashed gray lines show the “noise floor”, which is the spectrum of the noise in the measurement obtained when the sensor was not moving (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0178664#sec002" target="_blank">Methods</a>). Gray bands show 1 STD. <b>B:</b> Subject-averaged best-fit power law exponents over the low (gray) and high (black) frequency ranges for all six motion dimensions. Also shown for comparison are the subject-averaged best-fit power law exponents for a single power law over the entire frequency range (blue). “*” indicates statistical significance at the p = 0.01 level using a one-way ANOVA. <b>C:</b> Subject-averaged frequency at which the power spectrum starts decreasing more sharply for all six motion dimensions.</p

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 va...

The detection of gravito-inertial forces by the otolith system is essential for our sense of balance and accurate perception. To date, however, how this system encodes the self-motion stimuli that are experienced during everyday activities remains unknown. Here, we addressed this fundamental question directly by recording from single otolith afferents in monkeys during naturalistic translational self-motion and changes in static head orientation. Otolith afferents with higher intrinsic variability transmitted more information overall about translational self-motion than their regular counterparts, owing to stronger nonlinearities that enabled precise spike timing including phase locking. By contrast, more regular afferents better discriminated between different static head orientations relative to gravity. Using computational methods, we further demonstrated that coupled increases in intrinsic variability and sensitivity accounted for the observed functional differences between affe...

There is accumulating evidence that the brain's neural coding strategies are constrained by natural 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 translational self-motion signals experienced by human subjects during everyday activities. We found that envelopes can reach large values across all six motion dimensions (~450 deg/s for 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 sharply for high (>2 Hz) temporal frequencies and thus was not well-fit by a power law. We next compared the spectral properties of envelope signals resulting from active and passive self-motion, as well as those resulting from signals obtained when the subject is absent (i.e. external stimuli). Our data suggest that different mechanisms underlie devi...

Understanding how the brain processes sensory information is often complicated by the fact that neurons exhibit trial-to-trial variability in their responses to stimuli. Indeed, the role of variability in sensory coding is still highly debated. Here, we examined how variability influences neural responses to naturalistic stimuli consisting of a fast time-varying waveform (i.e., carrier or first order) whose amplitude (i.e., envelope or second order) varies more slowly. Recordings were made from fish electrosensory and monkey vestibular sensory neurons. In both systems, we show that correlated but not single-neuron activity can provide detailed information about second-order stimulus features. Using a simple mathematical model, we made the strong prediction that such correlation-based coding of envelopes requires neural variability. Strikingly, the performance of correlated activity at predicting the envelope was similarly optimally tuned to a nonzero level of variability in both sys...

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 go...

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 adap...

Human activities often involve sensing body orientation using cues from gravity. Astronauts in microgravity are deprived of those cues and may have difficulty with certain tasks. We theorized that experience in microgravity combined with mechanically induced pressure under the feet(footpressure)wouldimprovetheaccuracyofasubject’sperception of the body’s z-axis as indicated by pointing to the subjective horizon (SH). Method: Experiments were conducted during parabolic flights using five experienced subjects and five novices. Subjects were required to raise their arm to point to their SH with eyes closed. Measurements were made on Earth and in microgravity, with or without foot pressure. Both pointing accuracy and the kinetics of the movement were analyzed. Results: Performance by experts was stable under all conditions. However, novices in microgravity pointed to a significantly lower SH (16.5°] below the 1-G SH) and slowed their movements (mean angular velocity of movement: 16.8°
s
1 less than in 1 G). Foot pressure improved the performance of the novices so that it was closer to that observed at 1 G (8.9° below the 1-G SH). Discussion: These results suggest that pressure cues under the feet activated the internal model of gravity in the novices, and thus improved the accuracy of their perception of their z-axis. Subjects with prior experience in microgravity correctly perceived their z-axis without the supplementary input.

There is considerable evidence that the cerebellum has a vital role in motor learning by constructing an estimate of the sensory consequences of movement. Theory suggests that this estimate is compared with the actual feedback to compute the sensory prediction error. However, direct proof for the existence of this comparison is lacking. We carried out a trial-by-trial analysis of cerebellar neurons during the execution and adaptation of voluntary head movements and found that neuronal sensitivities dynamically tracked the comparison of predictive and feedback signals. When the relationship between the motor command and resultant movement was altered, neurons robustly responded to sensory input as if the movement was externally generated. Neuronal sensitivities then declined with the same time course as the concurrent behavioral learning. These findings demonstrate the output of an elegant computation in which rapid updating of an internal model enables the motor system to learn to expect unexpected sensory inputs.

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, flexed and 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 flexed and elevated to create a torsoward 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 whe...

Human activities often involve sensing body orientation using cues from gravity. Astronauts in microgravity are deprived of those cues and may have difficulty with certain tasks. We theorized that experience in microgravity combined with mechanically induced pressure under the feet (foot pressure) would improve the accuracy of a subject's perception of the body's z-axis as indicated by pointing to the subjective horizon (SH). Experiments were conducted during parabolic flights using five experienced subjects and five novices. Subjects were required to raise their arm to point to their SH with eyes closed. Measurements were made on Earth and in microgravity, with or without foot pressure. Both pointing accuracy and the kinetics of the movement were analyzed. Performance by experts was stable under all conditions. However, novices in microgravity pointed to a significantly lower SH (16.5 degrees below the 1-G SH) and slowed their movements (mean angular velocity of movement: 1...