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The Journal of Neuroscience, September 5, 2007, 27(36):9742-9756; doi:10.1523/JNEUROSCI.0817-07.2007

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Behavioral/Systems/Cognitive
Multimodal Coding of Three-Dimensional Rotation and Translation in Area MSTd: Comparison of Visual and Vestibular Selectivity

Katsumasa Takahashi,¹ Yong Gu,¹ Paul J. May,² Shawn D. Newlands,³ Gregory C. DeAngelis,^1 * and Dora E. Angelaki^1 *

¹Department of Anatomy and Neurobiology, Washington University School of Medicine, St. Louis, Missouri 63110, ²Departments of Anatomy, Ophthalmology, and Neurology, University of Mississippi Medical Center, Jackson, Mississippi 39216, and ³Department of Otolaryngology, University of Texas Medical Branch, Galveston, Texas 77550

Correspondence should be addressed to Dr. Dora E. Angelaki, Department of Anatomy and Neurobiology, Box 8108, Washington University School of Medicine, 660 South Euclid Avenue, St. Louis, MO 63110. Email: angelaki{at}pcg.wustl.edu

Recent studies have shown that most neurons in the dorsal medial superior temporal area (MSTd) signal the direction of self-translation (i.e., heading) in response to both optic flow and inertial motion. Much less is currently known about the response properties of MSTd neurons during self-rotation. We have characterized the three-dimensional tuning of MSTd neurons while monkeys passively fixated a central, head-fixed target. Rotational stimuli were either presented using a motion platform or simulated visually using optic flow. Nearly all MSTd cells were significantly tuned for the direction of rotation in the absence of optic flow, with more neurons preferring roll than pitch or yaw rotations. The preferred rotation axis in response to optic flow was generally the opposite of that during physical rotation. This result differs sharply from our findings for translational motion, where approximately half of MSTd neurons have congruent visual and vestibular preferences. By testing a subset of neurons with combined visual and vestibular stimulation, we also show that the contributions of visual and vestibular cues to MSTd responses depend on the relative reliabilities of the two stimulus modalities. Previous studies of MSTd responses to motion in darkness have assumed a vestibular origin for the activity observed. We have directly verified this assumption by recording from MSTd neurons after bilateral labyrinthectomy. Selectivity for physical rotation and translation stimuli was eliminated after labyrinthectomy, whereas selectivity to optic flow was unaffected. Overall, the lack of MSTd neurons with congruent rotation tuning for visual and vestibular stimuli suggests that MSTd does not integrate these signals to produce a robust perception of self-rotation. Vestibular rotation signals in MSTd may instead be used to compensate for the confounding effects of rotatory head movements on optic flow.

Key words: monkey; MST; optic flow; vestibular; visual motion; rotation

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Received Feb. 22, 2007; revised June 27, 2007; accepted July 26, 2007.

Correspondence should be addressed to Dr. Dora E. Angelaki, Department of Anatomy and Neurobiology, Box 8108, Washington University School of Medicine, 660 South Euclid Avenue, St. Louis, MO 63110. Email: angelaki{at}pcg.wustl.edu

This article has been cited by other articles:

				S. A. Chowdhury, K. Takahashi, G. C. DeAngelis, and D. E. Angelaki Does the Middle Temporal Area Carry Vestibular Signals Related to Self-Motion? J. Neurosci., September 23, 2009; 29(38): 12020 - 12030. [Abstract] [Full Text] [PDF]

				S. Liu and D. E. Angelaki Vestibular Signals in Macaque Extrastriate Visual Cortex Are Functionally Appropriate for Heading Perception J. Neurosci., July 15, 2009; 29(28): 8936 - 8945. [Abstract] [Full Text] [PDF]

				A. Chen, Y. Gu, K. Takahashi, D. E. Angelaki, and G. C. DeAngelis Clustering of Self-Motion Selectivity and Visual Response Properties in Macaque Area MSTd J Neurophysiol, November 1, 2008; 100(5): 2669 - 2683. [Abstract] [Full Text] [PDF]

				H. Meng, P. J. May, J. D. Dickman, and D. E. Angelaki Vestibular Signals in Primate Thalamus: Properties and Origins J. Neurosci., December 12, 2007; 27(50): 13590 - 13602. [Abstract] [Full Text] [PDF]

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