scholarly journals Neuronal variability and tuning are balanced to optimize naturalistic self-motion coding in primate vestibular pathways

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Diana E Mitchell ◽  
Annie Kwan ◽  
Jerome Carriot ◽  
Maurice J Chacron ◽  
Kathleen E Cullen
Keyword(s):  
Information Transmission ◽  
Neural Coding ◽  
Spectral Power ◽  
Natural Stimulus ◽  
Modeling And Analysis ◽  
Motion Coding ◽  
Novel Strategy ◽  
Self Motion ◽  
Neural Variability ◽  
Vestibular Pathways

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.

scholarly journals Author response: Neuronal variability and tuning are balanced to optimize naturalistic self-motion coding in primate vestibular pathways

2018 ◽  
Author(s):  
Diana E Mitchell ◽  
Annie Kwan ◽  
Jerome Carriot ◽  
Maurice J Chacron ◽  
Kathleen E Cullen
Keyword(s):  
Author Response ◽  
Motion Coding ◽  
Self Motion ◽  
Vestibular Pathways

Multisensory Integration and the Perception of Self-Motion

2018 ◽  
Author(s):  
Kathleen E. Cullen
Keyword(s):  
Rotational Velocity ◽  
Sensory Information ◽  
Proprioceptive Information ◽  
Everyday Activities ◽  
Perceptual Stability ◽  
The World ◽  
Perception Of Self ◽  
Self Motion ◽  
The Brain ◽  
Vestibular Pathways

As we go about our everyday activities, our brain computes accurate estimates of both our motion relative to the world, and of our orientation relative to gravity. Essential to this computation is the information provided by the vestibular system; it detects the rotational velocity and linear acceleration of our heads relative to space, making a fundamental contribution to our perception of self-motion and spatial orientation. Additionally, in everyday life, our perception of self-motion depends on the integration of both vestibular and nonvestibular cues, including visual and proprioceptive information. Furthermore, the integration of motor-related information is also required for perceptual stability, so that the brain can distinguish whether the experienced sensory inflow was a result of active self-motion through the world or if instead self-motion that was externally generated. To date, understanding how the brain encodes and integrates sensory cues with motor signals for the perception of self-motion during natural behaviors remains a major goal in neuroscience. Recent experiments have (i) provided new insights into the neural code used to represent sensory information in vestibular pathways, (ii) established that vestibular pathways are inherently multimodal at the earliest stages of processing, and (iii) revealed that self-motion information processing is adjusted to meet the needs of specific tasks. Our current level of understanding of how the brain integrates sensory information and motor-related signals to encode self-motion and ensure perceptual stability during everyday activities is reviewed.

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

2020 ◽  
Author(s):  
Isabelle Mackrous ◽  
Jérome Carriot ◽  
Kathleen E Cullen ◽  
Maurice J Chacron
Keyword(s):  
Author Response ◽  
Macaque Monkeys ◽  
Coding Strategies ◽  
Self Motion ◽  
Neural Variability

Attention modulates event-related spectral power in multisensory self-motion perception

NeuroImage ◽  
2019 ◽  
Vol 191 ◽  
pp. 68-80 ◽  
Author(s):  
Ben Townsend ◽  
Joey K. Legere ◽  
Shannon O'Malley ◽  
Martin v. Mohrenschildt ◽  
Judith M. Shedden
Keyword(s):  
Motion Perception ◽  
Spectral Power ◽  
Self Motion

The neural basis for violations of Weber’s law in self-motion perception

2021 ◽  
Vol 118 (36) ◽  
pp. e2025061118
Author(s):  
Jerome Carriot ◽  
Kathleen E. Cullen ◽  
Maurice J. Chacron
Keyword(s):  
Discrimination Performance ◽  
Fundamental Principle ◽  
Weber’S Law ◽  
Neural Basis ◽  
Sensory Stimuli ◽  
Weber's Law ◽  
Perceptual Performance ◽  
Improved Performance ◽  
Self Motion ◽  
Neural Variability

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.

scholarly journals Boosts in brain signal variability track liberal shifts in decision bias

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Niels A Kloosterman ◽  
Julian Q Kosciessa ◽  
Ulman Lindenberger ◽  
Johannes Jacobus Fahrenfort ◽  
Douglas D Garrett
Keyword(s):  
Spectral Power ◽  
Event Related Potentials ◽  
Response Strategy ◽  
False Alarms ◽  
Time Frequency ◽  
Decision Bias ◽  
Related Potentials ◽  
Neural Variability ◽  
Environmental Demands ◽  
Liberal Bias

Adopting particular decision biases allows organisms to tailor their choices to environmental demands. For example, a liberal response strategy pays off when target detection is crucial, whereas a conservative strategy is optimal for avoiding false alarms. Using conventional time-frequency analysis of human electroencephalographic (EEG) activity, we previously showed that bias setting entails adjustment of evidence accumulation in sensory regions (Kloosterman et al., 2019), but the presumed prefrontal signature of a conservative-to-liberal bias shift has remained elusive. Here, we show that a liberal bias shift is reflected in a more unconstrained neural regime (boosted entropy) in frontal regions that is suited to the detection of unpredictable events. Overall EEG variation, spectral power and event-related potentials could not explain this relationship, highlighting that moment-to-moment neural variability uniquely tracks bias shifts. Neural variability modulation through prefrontal cortex appears instrumental for permitting an organism to adapt its biases to environmental demands.

Cognitive, Systems, and Computational Neurosciences of the Self in Motion

2021 ◽  
Vol 73 (1) ◽  
Author(s):  
Jean-Paul Noel ◽  
Dora E. Angelaki
Keyword(s):  
Annual Review ◽  
Publication Date ◽  
Time Varying ◽  
Systems Neuroscience ◽  
Theoretical Approaches ◽  
Self Motion ◽  
The Brain ◽  
Position Estimate ◽  
Acceleration Signals ◽  
Vestibular Pathways

Navigating by path integration requires continuously estimating one's self-motion. This estimate may be derived from visual velocity and/or vestibular acceleration signals. Importantly, these senses in isolation are ill-equipped to provide accurate estimates, and thus visuo-vestibular integration is an imperative. After a summary of the visual and vestibular pathways involved, the crux of this review focuses on the human and theoretical approaches that have outlined a normative account of cue combination in behavior and neurons, as well as on the systems neuroscience efforts that are searching for its neural implementation. We then highlight a contemporary frontier in our state of knowledge: understanding how velocity cues with time-varying reliabilities are integrated into an evolving position estimate over prolonged time periods. Further, we discuss how the brain builds internal models inferring when cues ought to be integrated versus segregated—a process of causal inference. Lastly, we suggest that the study of spatial navigation has not yet addressed its initial condition: self-location. Expected final online publication date for the Annual Review of Psychology, Volume 73 is January 2022. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

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