scholarly journals Decision letter: Neural variability determines coding strategies for natural self-motion in macaque monkeys

2020 ◽  
2020 ◽  
Author(s):  
Isabelle Mackrous ◽  
Jérome Carriot ◽  
Kathleen E Cullen ◽  
Maurice J Chacron

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Isabelle Mackrous ◽  
Jérome Carriot ◽  
Kathleen E Cullen ◽  
Maurice J Chacron

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.


2021 ◽  
Vol 118 (36) ◽  
pp. e2025061118
Author(s):  
Jerome Carriot ◽  
Kathleen E. Cullen ◽  
Maurice J. Chacron

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.


eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Diana E Mitchell ◽  
Annie Kwan ◽  
Jerome Carriot ◽  
Maurice J Chacron ◽  
Kathleen E Cullen

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. Taken together, our findings reveal a novel strategy by which neural variability contributes to optimized processing of naturalistic stimuli.


eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
Mohsen Jamali ◽  
Jerome Carriot ◽  
Maurice J Chacron ◽  
Kathleen E Cullen

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 afferent classes. Together, our results indicate that irregular and regular otolith afferents use different strategies to encode naturalistic self-motion and static head orientation relative to gravity.


2020 ◽  
Author(s):  
V De Castro ◽  
A T Smith ◽  
A L Beer ◽  
C Leguen ◽  
N Vayssière ◽  
...  

Abstract In humans, the posterior cingulate cortex contains an area sensitive to visual cues to self-motion. This cingulate sulcus visual area (CSv) is structurally and functionally connected with several (multi)sensory and (pre)motor areas recruited during locomotion. In nonhuman primates, electrophysiology has shown that the cingulate cortex is also related to spatial navigation. Recently, functional MRI in macaque monkeys identified a cingulate area with similar visual properties to human CSv. In order to bridge the gap between human and nonhuman primate research, we examined the structural and functional connectivity of putative CSv in three macaque monkeys adopting the same approach as in humans based on diffusion MRI and resting-state functional MRI. The results showed that putative monkey CSv connects with several visuo-vestibular areas (e.g., VIP/FEFsem/VPS/MSTd) as well as somatosensory cortex (e.g., dorsal aspects of areas 3/1/2), all known to process sensory signals that can be triggered by self-motion. Additionally, strong connections are observed with (pre)motor areas located in the dorsal prefrontal cortex (e.g., F3/F2/F1) and within the anterior cingulate cortex (e.g., area 24). This connectivity pattern is strikingly reminiscent of that described for human CSv, suggesting that the sensorimotor control of locomotion relies on similar organizational principles in human and nonhuman primates.


Author(s):  
Jan Churan ◽  
Andre Kaminiarz ◽  
Jakob Christian Benjamin Schwenk ◽  
Frank Bremmer

Successful interaction with the environment requires the dissociation of self-induced from externally induced sensory stimulation. Temporal proximity of action and effect is hereby often used as an indicator of whether an observed event should be interpreted as a result of own actions or not. We tested how the delay between an action (press of a touch bar) and an effect (onset of simulated self-motion) influences the processing of visually simulated self-motion in the ventral intraparietal area (VIP) of macaque monkeys. We found that a delay between the action and the start of the self-motion stimulus led to a rise of activity above the baseline activity before motion onset in a subpopulation of 21% of the investigated neurons. In the responses to the stimulus, we found a significantly lower sustained activity when the press of a touch bar and the motion onset were contiguous compared to the condition when the motion onset was delayed. We speculate that this weak inhibitory effect might be part of a mechanism that sharpens the tuning of VIP neurons during self-induced motion and thus has the potential to increase the precision of heading information that is required to adjust the orientation of self-motion in everyday navigational tasks.


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