Multimodal coding of three-dimensional rotation and translation in area MSTd: Comparison of visual and vestibular selectivity

Katsumasa Takahashi, Yong Gu, Paul J. May, Shawn D. Newlands, Gregory C. DeAngelis, Dora Angelaki

Research output: Contribution to journalArticle

Abstract

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.

Original languageEnglish (US)
Pages (from-to)9742-9756
Number of pages15
JournalJournal of Neuroscience
Volume27
Issue number36
DOIs
StatePublished - Sep 5 2007

Fingerprint

Optic Flow
Neurons
Yaws
Head Movements
Photic Stimulation
Darkness
Haplorhini
Cues
Head

Keywords

  • Monkey
  • MST
  • Optic flow
  • Rotation
  • Vestibular
  • Visual motion

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Multimodal coding of three-dimensional rotation and translation in area MSTd : Comparison of visual and vestibular selectivity. / Takahashi, Katsumasa; Gu, Yong; May, Paul J.; Newlands, Shawn D.; DeAngelis, Gregory C.; Angelaki, Dora.

In: Journal of Neuroscience, Vol. 27, No. 36, 05.09.2007, p. 9742-9756.

Research output: Contribution to journalArticle

Takahashi, Katsumasa ; Gu, Yong ; May, Paul J. ; Newlands, Shawn D. ; DeAngelis, Gregory C. ; Angelaki, Dora. / Multimodal coding of three-dimensional rotation and translation in area MSTd : Comparison of visual and vestibular selectivity. In: Journal of Neuroscience. 2007 ; Vol. 27, No. 36. pp. 9742-9756.
@article{3237de23219d4bf198809f466ff094ea,
title = "Multimodal coding of three-dimensional rotation and translation in area MSTd: Comparison of visual and vestibular selectivity",
abstract = "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.",
keywords = "Monkey, MST, Optic flow, Rotation, Vestibular, Visual motion",
author = "Katsumasa Takahashi and Yong Gu and May, {Paul J.} and Newlands, {Shawn D.} and DeAngelis, {Gregory C.} and Dora Angelaki",
year = "2007",
month = "9",
day = "5",
doi = "10.1523/JNEUROSCI.0817-07.2007",
language = "English (US)",
volume = "27",
pages = "9742--9756",
journal = "Journal of Neuroscience",
issn = "0270-6474",
publisher = "Society for Neuroscience",
number = "36",

}

TY - JOUR

T1 - Multimodal coding of three-dimensional rotation and translation in area MSTd

T2 - Comparison of visual and vestibular selectivity

AU - Takahashi, Katsumasa

AU - Gu, Yong

AU - May, Paul J.

AU - Newlands, Shawn D.

AU - DeAngelis, Gregory C.

AU - Angelaki, Dora

PY - 2007/9/5

Y1 - 2007/9/5

N2 - 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.

AB - 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.

KW - Monkey

KW - MST

KW - Optic flow

KW - Rotation

KW - Vestibular

KW - Visual motion

UR - http://www.scopus.com/inward/record.url?scp=34848867818&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=34848867818&partnerID=8YFLogxK

U2 - 10.1523/JNEUROSCI.0817-07.2007

DO - 10.1523/JNEUROSCI.0817-07.2007

M3 - Article

VL - 27

SP - 9742

EP - 9756

JO - Journal of Neuroscience

JF - Journal of Neuroscience

SN - 0270-6474

IS - 36

ER -