Causal Links between Dorsal Medial Superior Temporal Area Neurons and Multisensory Heading Perception

The dorsal medial superior temporal area (MSTd) in the extrastriate visual cortex is thought to play an important role in heading perception because neurons in this area are tuned to both optic flow and vestibular signals. MSTd neurons also show significant correlations with perceptual judgments during a fine heading direction discrimination task. To test for a causal link with heading perception, we used microstimulation and reversible inactivation techniques to artificially perturb MSTd activity while monitoring behavioral performance. Electrical microstimulation significantly biased monkeys' heading percepts based on optic flow, but did not significantly impact vestibular heading judgments. The latter result may be due to the fact that vestibular heading preferences in MSTd are more weakly clustered than visual preferences and multiunit tuning for vestibular stimuli is weak. Reversible chemical inactivation, however, increased behavioral thresholds when heading judgments were based on either optic flow or vestibular cues, although the magnitude of the effects was substantially stronger for optic flow. Behavioral deficits in a combined visual/vestibular stimulus condition were intermediate between the single-cue effects. Despite deficits in discrimination thresholds, animals were able to combine visual and vestibular cues near optimally, even after large bilateral muscimol injections into MSTd. Simulations show that the overall pattern of results following inactivation is consistent with a mixture of contributions from MSTd and other areas with vestibular-dominant tuning for heading. Our results support a causal link between MSTd neurons and multisensory heading perception but suggest that other multisensory brain areas also contribute.

[1]  W. Newsome,et al.  Microstimulation in visual area MT: effects on direction discrimination performance , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[2]  W. Warren,et al.  Perception of translational heading from optical flow. , 1988, Journal of experimental psychology. Human perception and performance.

[3]  Wei Ji Ma,et al.  Bayesian inference with probabilistic population codes , 2006, Nature Neuroscience.

[4]  K. H. Britten,et al.  Clustering of response selectivity in the medial superior temporal area of extrastriate cortex in the macaque monkey , 1998, Visual Neuroscience.

[5]  S Celebrini,et al.  Microstimulation of extrastriate area MST influences performance on a direction discrimination task. , 1995, Journal of neurophysiology.

[6]  Christopher R Fetsch,et al.  Neural correlates of reliability-based cue weighting during multisensory integration , 2011, Nature Neuroscience.

[7]  Kenneth H Britten,et al.  Area MST and heading perception in macaque monkeys. , 2002, Cerebral cortex.

[8]  Dora E Angelaki,et al.  Macaque Parieto-Insular Vestibular Cortex: Responses to Self-Motion and Optic Flow , 2010, Journal of Neuroscience.

[9]  W. Newsome,et al.  Microstimulation in visual area MT: effects of varying pulse amplitude and frequency , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  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.

[11]  Jean-Marc Edeline,et al.  Muscimol Diffusion after Intracerebral Microinjections: A Reevaluation Based on Electrophysiological and Autoradiographic Quantifications , 2002, Neurobiology of Learning and Memory.

[12]  C. Duffy,et al.  Heading representation in MST: sensory interactions and population encoding. , 2003, Journal of neurophysiology.

[13]  William T. Newsome,et al.  Cortical microstimulation influences perceptual judgements of motion direction , 1990, Nature.

[14]  田中 啓治 Analysis of Local and Wide-Field Movements in the Superior Temporal Visual Areas of the Macaque Monkey , 1987 .

[15]  T. Woolsey,et al.  A method to measure the effective spread of focally injected muscimol into the central nervous system with electrophysiology and light microscopy , 2002, Journal of Neuroscience Methods.

[16]  A. V. D. Berg,et al.  Robustness of perception of heading from optic flow , 1992, Vision Research.

[17]  Jennifer L. Campos,et al.  Bayesian integration of visual and vestibular signals for heading. , 2009, Journal of vision.

[18]  Christopher R Fetsch,et al.  Visual–vestibular cue integration for heading perception: applications of optimal cue integration theory , 2010, The European journal of neuroscience.

[19]  François Klam,et al.  ã Federation of European Neuroscience Societies Visual±vestibular interactive responses in the macaque ventral intraparietal area (VIP) , 2022 .

[20]  Michael R Ibbotson,et al.  Vestibular Stimulation Affects Optic-Flow Sensitivity , 2010, Perception.

[21]  K. Tanaka,et al.  Underlying mechanisms of the response specificity of expansion/contraction and rotation cells in the dorsal part of the medial superior temporal area of the macaque monkey. , 1989, Journal of neurophysiology.

[22]  R. Wurtz,et al.  Sensitivity of MST neurons to optic flow stimuli. I. A continuum of response selectivity to large-field stimuli. , 1991, Journal of neurophysiology.

[23]  G. DeAngelis,et al.  Multimodal Coding of Three-Dimensional Rotation and Translation in Area MSTd: Comparison of Visual and Vestibular Selectivity , 2007, The Journal of Neuroscience.

[24]  M. Banks,et al.  Perceiving heading with different retinal regions and types of optic flow , 1993, Perception & psychophysics.

[25]  Christopher R Fetsch,et al.  Dynamic Reweighting of Visual and Vestibular Cues during Self-Motion Perception , 2009, The Journal of Neuroscience.

[26]  Dora E Angelaki,et al.  Does the Middle Temporal Area Carry Vestibular Signals Related to Self-Motion? , 2009, The Journal of Neuroscience.

[27]  Frank Bremmer,et al.  ã Federation of European Neuroscience Societies Heading encoding in the macaque ventral intraparietal area (VIP) , 2022 .

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

[29]  R. Wurtz,et al.  Response of monkey MST neurons to optic flow stimuli with shifted centers of motion , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  M. Goldberg,et al.  Ventral intraparietal area of the macaque: anatomic location and visual response properties. , 1993, Journal of neurophysiology.

[31]  S. Sterbing-D’Angelo,et al.  Behavioral/systems/cognitive Multisensory Space Representations in the Macaque Ventral Intraparietal Area , 2022 .

[32]  James A. Crowell,et al.  The perception of heading during eye movements , 1992, Nature.

[33]  A. V. van den Berg,et al.  Judgements of Heading , 1996, Vision Research.

[34]  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.

[35]  J. Weesie,et al.  Integration of visual and inertial cues in perceived heading of self-motion. , 2010, Journal of vision.

[36]  William T Newsome,et al.  Middle Temporal Visual Area Microstimulation Influences Veridical Judgments of Motion Direction , 2002, The Journal of Neuroscience.

[37]  M. Ernst,et al.  Humans integrate visual and haptic information in a statistically optimal fashion , 2002, Nature.

[38]  D. Sparks,et al.  A simple method for constructing microinjectrodes for reversible inactivation in behaving monkeys , 2001, Journal of Neuroscience Methods.

[39]  Dora E Angelaki,et al.  Convergence of Vestibular and Visual Self-Motion Signals in an Area of the Posterior Sylvian Fissure , 2011, The Journal of Neuroscience.

[40]  R. Kiani,et al.  Microstimulation of inferotemporal cortex influences face categorization , 2006, Nature.

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

[42]  G. DeAngelis,et al.  Multisensory integration: psychophysics, neurophysiology, and computation , 2009, Current Opinion in Neurobiology.

[43]  C. Duffy MST neurons respond to optic flow and translational movement. , 1998, Journal of neurophysiology.

[44]  Thomas H. Brown,et al.  Imaging the spread of reversible brain inactivations using fluorescent muscimol , 2008, Journal of Neuroscience Methods.

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

[46]  K. Hoffmann,et al.  Linear Vestibular Self‐Motion Signals in Monkey Medial Superior Temporal Area , 1999, Annals of the New York Academy of Sciences.

[47]  Yong Gu,et al.  Clustering of self-motion selectivity and visual response properties in macaque area MSTd. , 2008, Journal of neurophysiology.

[48]  Kenneth H. Britten,et al.  Mechanisms of self-motion perception. , 2008, Annual review of neuroscience.

[49]  Frank Bremmer,et al.  Interaction of linear vestibular and visual stimulation in the macaque ventral intraparietal area (VIP) , 2002, The European journal of neuroscience.

[50]  Yq Liu,et al.  Intention and Attention: Different functional roles for LIPd and LIPv , 2010, Nature Neuroscience.

[51]  B J Geesaman,et al.  Maps of complex motion selectivity in the superior temporal cortex of the alert macaque monkey: a double-label 2-deoxyglucose study. , 1997, Cerebral cortex.

[52]  W. Newsome,et al.  What electrical microstimulation has revealed about the neural basis of cognition , 2004, Current Opinion in Neurobiology.

[53]  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.

[54]  G. DeAngelis,et al.  Fine Discrimination Training Alters the Causal Contribution of Macaque Area MT to Depth Perception , 2008, Neuron.