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Visual and Nonvisual Contributions to Three-Dimensional Heading Selectivity in the Medial Superior Temporal Area
Open accessAbstract
Robust perception of self-motion requires integration of visual motion signals with nonvisual cues. Neurons in the dorsal subdivision of the medial superior temporal area (MSTd) may be involved in this sensory integration, because they respond selectively to global patterns of optic flow, as well as translational motion in darkness. Using a virtual-reality system, we have characterized the three-dimensional (3D) tuning of MSTd neurons to heading directions defined by optic flow alone, inertial motion alone, and congruent combinations of the two cues. Among 255 MSTd neurons, 98% exhibited significant 3D heading tuning in response to optic flow, whereas 64% were selective for heading defined by inertial motion. Heading preferences for visual and inertial motion could be aligned but were just as frequently opposite. Moreover, heading selectivity in response to congruent visual/vestibular stimulation was typically weaker than that obtained using optic flow alone, and heading preferences under congruent stimulation were dominated by the visual input. Thus, MSTd neurons generally did not integrate visual and nonvisual cues to achieve better heading selectivity. A simple two-layer neural network, which received eye-centered visual inputs and head-centered vestibular inputs, reproduced the major features of the MSTd data. The network was trained to compute heading in a head-centered reference frame under all stimulus conditions, such that it performed a selective reference-frame transformation of visual, but not vestibular, signals. The similarity between network hidden units and MSTd neurons suggests that MSTd may be an early stage of sensory convergence involved in transforming optic flow information into a (head-centered) reference frame that facilitates integration with vestibular signals.
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“Consistent with previous work (6), only units which were considered to have strong tuning (fitted amplitude [α] parameter > median across all units) were included in the histogram showing the number of units as a function of the difference between preferred visual and vestibular direction (xpref).”
From How multisensory neurons solve causal inference. (2021) · cites this paper as [6]
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“Studies of vestibular–visual integration have identified two types of multisensory neurons with similar prevalence in MSTd and VIP; those that are tuned to vestibular and visual motion in the same direction (congruent neurons) and those that prefer opposite directions (opposite neurons) (6, 8, 11).”
From How multisensory neurons solve causal inference. (2021) · cites this paper as [6]
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“Studies of vestibular–visual integration have identified two types of multisensory neurons with similar prevalence in MSTd and VIP; those that are tuned to vestibular and visual motion in the same direction (congruent neurons) and those that prefer opposite directions (opposite neurons) (6, 8, 11).”
From How multisensory neurons solve causal inference. (2021) · cites this paper as [6]
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“The former is consistent with previous neurophysiological work (6), whereas the latter provides an explanation for the existence of opposite neurons.”
From How multisensory neurons solve causal inference. (2021) · cites this paper as [6]
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“We found that this was made possible by asymmetries in sensitivity to different cues, which are also common among macaque MSTd neurons (6, 8, 10, 11).”
From How multisensory neurons solve causal inference. (2021) · cites this paper as [6]
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“Neurophysiological work in macaque monkeys indicates that vestibular and visual signals are combined on the dorsal subdivision of the medial superior temporal area (MSTd) (6–11) and in the ventral intraparietal area (VIP) (12, 13).”
From How multisensory neurons solve causal inference. (2021) · cites this paper as [6]
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“Moreover, the distribution of differences between the network’s MSTd units’ visual–vestibular preferred direction was similar to that found in macaque MSTd (Fig. 3G) (6) (i.e., bimodal with peaks at 0° and 180°).”
From How multisensory neurons solve causal inference. (2021) · cites this paper as [6]
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BackgroundResultActivity of Pursuit-Related Neurons in Medial Superior Temporal Area (MST) during Static Roll-Tilt
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Self-citationThe Neural Mechanisms of Visual and Vestibular Interaction in Self-Motion Perception
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“Neurons that respond to global optic flow patterns and exhibit heading tuning have been found in various regions of the primate visual system, including MSTd (Duffy and Wurtz, 1991; Gu et al., 2006) and VIP (Britten, 2008; Chen et al., 2011).”
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Path perturbation detection tasks reduce MSTd neuronal self-movement heading responses
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“Available neural data appears to support a weak-to-moderate peripheral bias consistent with the best performing model: the largest number of MSTd neurons possess tuning to eccentric headings but not to those in the far periphery (Duffy andWurtz, 1995; Gu et al., 2006).”
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“A well-studied example of visual and vestibular motion interaction is the study of optic flow and heading perception (e.g. Gu et al. 2006, reviewed in DeAngelis and Angelaki 2012).”
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Self-citationNeuronal Encoding of Multisensory Motion Features in the Rat Associative Parietal Cortex
Caron‐Guyon, J., Corbo, J., Zennou‐Azogui, Y., Xerri, C., Kavounoudias, A., & Catz, N. (2020) · Cerebral Cortex · doi:10.1093/cercor/bhaa118 · Cited by 3
“Several studies demonstrated that dorsal MST is not only involved in the processing of visual cues but also of vestibular information for self-motion perception (Fetsch et al., 2012; Gu, 2006; Gu et al., 2008).”
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Self-citationHierarchical and distinct biological motion processing in macaque visual cortical areas MT and MST
Feng, T., Zhang, Y., Han, W., Luo, X., Han, Y., Wei, W., Qu, H., Kuang, S., Zhang, T., & Zhang, Y. (2025) · Communications Biology · doi:10.1038/s42003-025-07861-y · Cited by 2
“MST neurons receive vestibular input and have been shown to integrate visual and vestibular information 43,44 .”
Decentralized Neural Circuits of Multisensory Information Integration in the Brain
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Self-citationSequential sparse autoencoder for dynamic heading representation in ventral intraparietal area
Gao, W., Shen, J., Lin, Y., Wang, K., Lin, Z., Tang, H., & Chen, X. (2023) · Computers in Biology and Medicine · doi:10.1016/j.compbiomed.2023.107114 · Cited by 1
Cross-Modal Plasticity during Self-Motion Perception
Lin, R., Zeng, F., Wang, Q., & Chen, A. (2023) · Brain Sciences · doi:10.3390/brainsci13111504 · Cited by 1
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Locomotion selectively enhances visual speed encoding in mouse medial higher visual areas
Horrocks, E. A. B., & Saleem, A. B. (2025) · iScience · doi:10.1016/j.isci.2025.114395 · Cited by 1
“Locomotion non-selectively enhanced drifting gratings direction tuning across all cortical areas.”
Neural Population Dynamics in Primate Multisensory Cortical Areas during Heading Discrimination
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How a neuron perceives visual motion during self-motion
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The neural mechanism of eye movements compensation during self-motion
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Li Zhaoping, A. (2024) · Vision Research · doi:10.1016/j.visres.2024.108489 · Cited by 1
“In MST and MT cells, some neurons are neither congruent nor opposite so that their preferred heading direction or preferred depths for the two input sources are neither identical nor opposite to each other (Gu et al., 2006; Nadler et al., 2013).”
InfluentialIntracellular processing of motion information in a network of blowfly visual interneurons
Elyada, Y. M. (2009) · doi:10.5282/edoc.10325 · Cited by 1
Chaplin, T. A., Allitt, B. J., Hagan, M. A., Rosa, M. G. P., Rajan, R., & Lui, L. L. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/204529 · Cited by 1
Emergence of opposite neurons in a decentralized firing-rate model of multisensory integrationPreprint
Niu, X., Chau, H. Y., Lee, T. S., & Zhang, W. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/845743 · Cited by 1
“ks is a scaling constant, while R ∈ [0, 1] is the reliability of the input.”
BackgroundSteinmetz, S., Layton, O. W., Powell, N. V., & Fajen, B. R. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.06.17.448823 · Cited by 1
“Neurons that respond to global optic flow patterns and exhibit heading tuning have been found in various regions of the primate visual system, including MSTd (Duffy & Wurtz, 1991; Gu et al., 2006) and VIP (Britten, 2008; Chen et al., 2011).”
BackgroundFeature Topography and Sound Intensity Level Encoding in Primary Auditory Cortex
Watkins, P. V. (2009) · Open Scholarship Institutional Repository (Washington University in St. Louis) · doi:10.7936/k7kp8047
Self-citationNeural Correlates of Reach Planning and Execution
Pearce, T. M. (2014) · Open Scholarship Institutional Repository (Washington University in St. Louis) · doi:10.7936/k7cc0xq1
Sunkara, A. (2014) · Open Scholarship Institutional Repository (Washington University in St. Louis) · doi:10.7936/k7n014p4
“While a lot of MST cells show preferences towards leftward or rightward translations, this is ideal for making fine discriminations of forward heading (Gu et al., 2006).”
BackgroundConvergenceofVestibularandVisualSelf-MotionSignalsin anAreaofthePosteriorSylvianFissure
DeAngelis, G. C. (2011)
Self-citationMacaque Rostral Vestibular and Fastigial Nuclei Optokinetic and Vestibular Responsiveness in the
Angelaki, D. E., Shinder, M. E., Taube, J. S., Chen, A., DeAngelis, G. C., Yakusheva, T. A., & Blázquez, P. M. (2015)
Self-citationPsychophysical and Psychological Factors Affecting Recovery from Acute Balance Disorders
Cousins, S. (2012) · Spiral (Imperial College London) · doi:10.25560/10122
“…recordings and spatial psychophysics in monkeys have only been carried out in intact animals (Chowdhury et al., 2009; Purushothaman and Bradley, 2005) and those with bilateral labyrinthectomy (Gu et al., 2007) so our human findings may prompt further experimental animal neuronal recordings.”
BackgroundEmergence of opposite neurons in a firing-rate model of multisensory integrationPreprint
Chau, H. Y., Zhang, W., & Lee, T. S. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/814483
“ks is a scaling constant, while R ∈ [0, 1] is the reliability of the input.”
BackgroundInfluentialMultisensory Integration: Mathematical Solution of Inherent Sensory Ambiguities
Yakusheva, T. A. (2019) · Contemporary clinical neuroscience · doi:10.1007/978-3-030-31407-1_2
空間知覚：物体の運動知覚に関与する視覚- 前庭情報統合の神経基盤
亮, 佐. (2017) · Journal of the Society of Biomechanisms · doi:10.3951/sobim.41.4_183
A spiking neural circuit model for learning multi-sensory integrationPreprint
Song, D., Niu, X., Zhang, W., & Lee, T. S. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.11.27.401216
“[3] [4] [5] [6] [7] Previously, a firing-rate model has been proposed to achieve visual and vestibular sensory integration.”
BackgroundHeteromodal Motion Coding in the Associative Parietal Cortex in RatsPreprint
Caron‐Guyon, J., Corbo, J., Zennou‐Azogui, Y., Xerri, C., Kavounoudias, A., & Catz, N. (2019) · SSRN Electronic Journal · doi:10.2139/ssrn.3377643
Decoding Estimates of Curvilinear Self-Motion from Neural Signals in a Model of Primate MSTdPreprint
Layton, O. W., Powell, N. V., Steinmetz, S., & Fajen, B. R. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.09.29.462288
“…heading from MSTd cells tuned to different FoE positions following strong connections forged over decades of physiological (Duffy & Wurtz, 1995) (Gu et al., 2012) (Gu et al., 2006) (Britten & van Wezel, 2002) and computational (Warren & Saunders, 1995) (Royden, 2002) (Layton et al., 2012) studies.”
BackgroundCasagrande, V. A. (2007) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.1090173.543389
Receptive Field Characterization in MSTd Neurons
Maamoun, A. (2018) · doi:10.53846/goediss-7200
Cullen, K. E. (2008) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.1103665.560827
Zhang, J., Huang, M., Gu, Y., Chen, A., & Yu, Y. (2022) · Brain Sciences · doi:10.3390/brainsci12101387
“Due to the prevalence of visual signals in MST-d [25], the integration is mostly based on the visual frame.”
BackgroundMethodResultInfluentialSelf-citationNeural activity during monkey vehicular wayfinding
Page, W. K., Sulon, D., & Duffy, C. J. (2023) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2023.120593
(2024) · The MIT Press eBooks · doi:10.7551/mitpress/9621.003.0004
Gao, Y., Cai, Y., Liu, D., Yu, J., Wang, J., Li, M., Xu, B., Wang, T., Chen, G., Northoff, G., et al. (2024) · eLife · doi:10.7554/elife.97545.2.sa0
Gao, Y., Cai, Y., Liu, D., Yu, J., Wang, J., Li, M., Xu, B., Wang, T., Chen, G., Northoff, G., et al. (2024) · eLife · doi:10.7554/elife.97545.2
Metadata
- Authors
- Gu, Y., Watkins, P. V., Angelaki, D. E., & DeAngelis, G. C.
- Affiliations
- Washington University in St. Louis (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2006-01-04
- Volume
- 26
- Issue
- 1
- Pages
- 73-85
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- OpenAlex
- W2041650980
- Cited by
- 316
- References
- 76
- Citations by year
- 2026: 6 · 2025: 13 · 2024: 23 · 2023: 11 · 2022: 15 · 2021: 22 · 2020: 15 · 2019: 12 · 2018: 17 · 2017: 20 · 2016: 13 · 2015: 17 · 2014: 21 · 2013: 20 · 2012: 12
- FWCI
- 18.84
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Eye Institute (R01EY012814, EY-12814, EY-016178, R01EY016178)
- National Institute on Deafness and Other Communication Disorders (DC04260., R01DC004260)
- Topics
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Multisensory perception and integration
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Life Sciences › Neuroscience › Neurology › Vestibular and auditory disorders
- Keywords
- medial superior temporal area, optical flow, inertial motion, vestibular cues, multisensory integration, self-motion perception, reference frame transformation, neural network model, virtual reality
- MeSH terms
- Action Potentials, Animals, Eye Movements, Macaca mulatta, Male, Motion Perception, Neurons, Photic Stimulation, Temporal Lobe, Head Movements, Imaging, Three-Dimensional
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