Choice-related activity and correlated noise in subcortical vestibular neurons

Functional links between neuronal activity and perception are studied by examining trial-by-trial correlations (choice probabilities) between neural responses and perceptual decisions. We addressed fundamental issues regarding the nature and origin of choice probabilities by recording from subcortical (brainstem and cerebellar) neurons in rhesus monkeys during a vestibular heading discrimination task. Subcortical neurons showed robust choice probabilities that exceeded those seen in cortex (area MSTd) under identical conditions. The greater choice probabilities of subcortical neurons could be predicted by a stronger dependence of correlated noise on tuning similarity, as revealed by population decoding. Significant choice probabilities were observed almost exclusively for neurons that responded selectively to translation, whereas neurons that represented net gravito-inertial acceleration did not show choice probabilities. These findings suggest that the emergence of choice probabilities in the vestibular system depends on a critical signal transformation that occurs in subcortical pathways to distinguish translation from orientation relative to gravity.

[1]  B. Cumming,et al.  Psychophysically measured task strategy for disparity discrimination is reflected in V2 neurons , 2007, Nature Neuroscience.

[2]  P. May,et al.  Vestibular Signals in Primate Thalamus: Properties and Origins , 2007, The Journal of Neuroscience.

[3]  D. Angelaki,et al.  Sensory vestibular contributions to constructing internal models of self-motion , 2005, Journal of neural engineering.

[4]  Ehud Zohary,et al.  Correlated neuronal discharge rate and its implications for psychophysical performance , 1994, Nature.

[5]  G. DeAngelis,et al.  A functional link between area MSTd and heading perception based on vestibular signals , 2007, Nature Neuroscience.

[6]  Corinna Cortes,et al.  Support-Vector Networks , 1995, Machine Learning.

[7]  G. DeAngelis,et al.  Contribution of Area MT to Stereoscopic Depth Perception Choice-Related Response Modulations Reflect Task Strategy , 2004, Neuron.

[8]  R. Romo,et al.  Neuronal correlates of subjective sensory experience , 2005, Nature Neuroscience.

[9]  B. Cumming,et al.  Decision-related activity in sensory neurons reflects more than a neuron’s causal effect , 2009, Nature.

[10]  J. Movshon,et al.  A computational analysis of the relationship between neuronal and behavioral responses to visual motion , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  A. Parker,et al.  Perceptually Bistable Three-Dimensional Figures Evoke High Choice Probabilities in Cortical Area MT , 2001, The Journal of Neuroscience.

[12]  G. DeAngelis,et al.  Representation of Vestibular and Visual Cues to Self-Motion in Ventral Intraparietal Cortex , 2011, The Journal of Neuroscience.

[13]  K. H. Britten,et al.  A relationship between behavioral choice and the visual responses of neurons in macaque MT , 1996, Visual Neuroscience.

[14]  J. Maunsell,et al.  Attention improves performance primarily by reducing interneuronal correlations , 2009, Nature Neuroscience.

[15]  A. Parker,et al.  The Precision of Single Neuron Responses in Cortical Area V1 during Stereoscopic Depth Judgments , 2000, The Journal of Neuroscience.

[16]  Dora E Angelaki,et al.  Responses of ventral posterior thalamus neurons to three-dimensional vestibular and optic flow stimulation. , 2010, Journal of neurophysiology.

[17]  K. Krug.  A common neuronal code for perceptual processes in visual cortex? Comparing choice and attentional correlates in V5/MT. , 2004, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[18]  D. Bradley,et al.  Neural population code for fine perceptual decisions in area MT , 2005, Nature Neuroscience.

[19]  W. Newsome,et al.  Context-Dependent Changes in Functional Circuitry in Visual Area MT , 2008, Neuron.

[20]  Bruce Cumming,et al.  Correlations between the activity of sensory neurons and behavior: how much do they tell us about a neuron's causality? , 2010, Current Opinion in Neurobiology.

[21]  Gregory C. DeAngelis,et al.  A Comparison of Vestibular Spatiotemporal Tuning in Macaque Parietoinsular Vestibular Cortex, Ventral Intraparietal Area, and Medial Superior Temporal Area , 2011, The Journal of Neuroscience.

[22]  W. Newsome,et al.  Estimates of the Contribution of Single Neurons to Perception Depend on Timescale and Noise Correlation , 2009, The Journal of Neuroscience.

[23]  Dora E. Angelaki,et al.  Vestibular Signals in Macaque Extrastriate Visual Cortex Are Functionally Appropriate for Heading Perception , 2009, The Journal of Neuroscience.

[24]  A. Perachio,et al.  Central projections of the vestibular nerve: a review and single fiber study in the Mongolian gerbil , 2003, Brain Research Bulletin.

[25]  Dora E Angelaki,et al.  Properties of cerebellar fastigial neurons during translation, rotation, and eye movements. , 2005, Journal of neurophysiology.

[26]  T. Sanger,et al.  Probability density estimation for the interpretation of neural population codes. , 1996, Journal of neurophysiology.

[27]  Yong Gu,et al.  Perceptual Learning Reduces Interneuronal Correlations in Macaque Visual Cortex , 2011, Neuron.

[28]  A. Parker,et al.  Neurons in Dorsal Visual Area V5/MT Signal Relative Disparity , 2011, The Journal of Neuroscience.

[29]  Arnulf B. A. Graf,et al.  Decoding the activity of neuronal populations in macaque primary visual cortex , 2011, Nature Neuroscience.

[30]  M. A. Smith,et al.  Stimulus Dependence of Neuronal Correlation in Primary Visual Cortex of the Macaque , 2005, The Journal of Neuroscience.

[31]  Ichiro Fujita,et al.  Neural Correlates of Fine Depth Discrimination in Monkey Inferior Temporal Cortex , 2005, The Journal of Neuroscience.

[32]  Dora E. Angelaki,et al.  Neurons compute internal models of the physical laws of motion , 2004, Nature.

[33]  J. Simpson,et al.  Projections of individual purkinje cells of identified zones in the flocculus to the vestibular and cerebellar nuclei in the rabbit , 1994, The Journal of comparative neurology.

[34]  Dora E Angelaki,et al.  Visual and Nonvisual Contributions to Three-Dimensional Heading Selectivity in the Medial Superior Temporal Area , 2006, The Journal of Neuroscience.

[35]  D. Angelaki,et al.  Vestibular system: the many facets of a multimodal sense. , 2008, Annual review of neuroscience.

[36]  B. Cumming,et al.  Macaque V2 Neurons, But Not V1 Neurons, Show Choice-Related Activity , 2006, The Journal of Neuroscience.

[37]  Xin Huang,et al.  Noise correlations in cortical area MT and their potential impact on trial-by-trial variation in the direction and speed of smooth-pursuit eye movements. , 2009, Journal of neurophysiology.

[38]  Dora E Angelaki,et al.  Spatial Reference Frames of Visual, Vestibular, and Multimodal Heading Signals in the Dorsal Subdivision of the Medial Superior Temporal Area , 2007, The Journal of Neuroscience.

[39]  G. DeAngelis,et al.  Neural correlates of multisensory cue integration in macaque MSTd , 2008, Nature Neuroscience.

[40]  Dora E Angelaki,et al.  Pursuit--vestibular interactions in brain stem neurons during rotation and translation. , 2005, Journal of neurophysiology.

[41]  W. Newsome,et al.  Correlation between Speed Perception and Neural Activity in the Middle Temporal Visual Area , 2005, The Journal of Neuroscience.

[42]  D. Angelaki,et al.  Purkinje Cells in Posterior Cerebellar Vermis Encode Motion in an Inertial Reference Frame , 2007, Neuron.

[43]  G. DeAngelis,et al.  Linking Neural Representation to Function in Stereoscopic Depth Perception: Roles of the Middle Temporal Area in Coarse versus Fine Disparity Discrimination , 2006, The Journal of Neuroscience.

[44]  Vladimir Vapnik,et al.  The Nature of Statistical Learning , 1995 .

[45]  Alexander S. Ecker,et al.  Decorrelated Neuronal Firing in Cortical Microcircuits , 2010, Science.

[46]  Yong Gu,et al.  Decoding of MSTd Population Activity Accounts for Variations in the Precision of Heading Perception , 2010, Neuron.

[47]  Ron Kohavi,et al.  A Study of Cross-Validation and Bootstrap for Accuracy Estimation and Model Selection , 1995, IJCAI.

[48]  Anthony J. Movshon,et al.  Optimal representation of sensory information by neural populations , 2006, Nature Neuroscience.

[49]  M. Cohen,et al.  Measuring and interpreting neuronal correlations , 2011, Nature Neuroscience.

[50]  J. Movshon,et al.  The analysis of visual motion: a comparison of neuronal and psychophysical performance , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[51]  R. Romo,et al.  Neural correlate of subjective sensory experience gradually builds up across cortical areas , 2006, Proceedings of the National Academy of Sciences.

[52]  W. Newsome,et al.  Neuronal and psychophysical sensitivity to motion signals in extrastriate area MST of the macaque monkey , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[53]  G. Leichnetz,et al.  Afferents of the caudal fastigial nucleus in a New World monkey (Cebus apella) , 2004, Experimental Brain Research.

[54]  A. Pouget,et al.  Neural correlations, population coding and computation , 2006, Nature Reviews Neuroscience.

[55]  M. A. Smith,et al.  Spatial and Temporal Scales of Neuronal Correlation in Primary Visual Cortex , 2008, The Journal of Neuroscience.

[56]  G. DeAngelis,et al.  Direction Discrimination Thresholds of Vestibular and Cerebellar Nuclei Neurons , 2010, Journal of Neuroscience.