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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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Citations
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Cited by
Sorted by citations
Items 301–315 of 315
Kong, L., Zeng, F., Zhang, Y., Li, L., & Chen, A. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e36913
“…primate brain regions have been reported to be in charge of heading perception from optic flow, e.g., the dorsal medial superior temporal area (MSTd, [11 – 13]), the ventral intraparietal area (VIP, [14 – 16]), superior temporal polysensory area (STP, [17,18]), area V6 [19 – 21] and 7a [22], and.”
BackgroundZENG, Z., Zhang, C., Xu, Y., He, H., & Gu, Y. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.09.03.610907
Self-citationGao, 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.97545.3
Integration of audiovisual motion in dorsolateral prefrontal cortical neurons
Karimi, A., Mozumder, R., Schoenhaut, A. M., Rausis, O., Wallace, M. T., Ramachandran, R., & Constantinidis, C. (2025) · Journal of Neurophysiology · doi:10.1152/jn.00289.2025
Encoding and combining naturalistic motion cues in the ferret higher visual cortexPreprint
Schaffhauser, T., Mamassian, P., & Boubenec, Y. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.09.23.678183
“…agrees with mechanisms at earlier stages of the visual system (Busse et al., 2009), supports feature pooling over Fourier space in motion processing (Masson & Castet, 2002), and echoes mechanisms highlighted in multisensory contexts (Deneve & Pouget, 2004; Gu et al., 2006; Fetsch et al., 2012).”
Marchand, S., Castro, V. D., Excoffier, E., Laurent, M.-A., Rosito, M., Vayssière, N., Cottereau, B. R., Cauquil, A. S., & Durand, J. (2025) · Imaging Neuroscience · doi:10.1162/imag.a.1093
Multisensorialité et kinesthésie : règles et substrats cérébraux de l'intégration multimodale
Blanchard, C. C. V. (2013) · theses.fr (ABES) · doi:10.70675/31d024acz0316z4dc7za32czeff4f77803dd
Spatial and temporal integration of binocular disparity in the primate brain
Héjja‐Brichard, Y. (2020) · theses.fr (ABES) · doi:10.70675/5cc70f79z5093z4528zaac7zd9647c35a925
A hemispheric decoding principle for vestibular heading perception in the posterior sylvian area
Xu, Y., & Gu, Y. (2026) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2533498123
Self-citationWei, Y., Wang, Y., Liu, S., Zhang, N. L., Yan, L., & Sheng, J. (2026) · International Journal of Human-Computer Interaction · doi:10.1080/10447318.2026.2663071
Sun, H., Tan, Z., Zeng, F., & Chen, A. (2026) · Frontiers in Neural Circuits · doi:10.3389/fncir.2026.1876597
“…(Felleman and Van Essen, 1991; Lopez and Blanke, 2011), including the dorsal medial superior temporal area (MSTd; Duffy, 1998; Page and Duffy, 2003; Gu et al., 2006, 2007), the ventral intraparietal area (VIP; Bremmer et al., 2002a,b; Schlack Sun et al. 10.3389/fncir.2026.1876597 et al., 2002;…”
InfluentialConflict-Dependent Gain Control in Area VIP during Visual-Vestibular Self-Motion Processing
Sun, H., Wang, R., Zeng, F., & Chen, A. (2026) · Journal of Neuroscience · doi:10.1523/jneurosci.0975-26.2026
Decoding self-motion: insights into visual-vestibular causal inference
Sun, H., Chen, A., & Zeng, F. (2026) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2026.1879282
“…for optic-flow patterns associated with translational and rotational self-motion and also receives vestibular heading signals, allowing the area to represent heading from either modality or their combination (Lappe et al., 1996; Duffy, 1998; Bremmer et al., 1999; Gu et al., 2006; Gu et al., 2008).”
Influential
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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