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The Journal of Neuroscience, December 12, 2007, 27(50):13590-13602; doi:10.1523/JNEUROSCI.3931-07.2007

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Behavioral/Systems/Cognitive
Vestibular Signals in Primate Thalamus: Properties and Origins

Hui Meng,¹ Paul J. May,² J. David Dickman,¹ and Dora E. Angelaki¹

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

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

Vestibular activation is found in diverse cortical areas. To characterize the pathways and types of signals supplied to cortex, we recorded responses to rotational and/or translational stimuli in the macaque thalamus. Few cells responded to rotation alone, with most showing convergence between semicircular canal and otolith signals. During sinusoidal rotation, thalamic responses lead head velocity by 30° on average at frequencies between 0.01–4 Hz. During translation, neurons encoded combinations of linear acceleration and velocity. In general, thalamic responses were similar to those recorded in the vestibular and cerebellar nuclei using identical testing paradigms, but differed from those of vestibular afferents. Thalamic responses represented a biased continuum: most cells more strongly encoded translation and fewer cells modulated primarily in response to net gravitoinertial acceleration. Responsive neurons were scattered within a large area that included regions of the ventral posterior and ventral lateral nuclei, and so were not restricted to the known vestibular nuclei projection zones. To determine the origins of these responses, a retrograde tracer was injected into a dorsolateral thalamic site where rotation/translation-sensitive cells were encountered. This injection labeled neurons in the rostral contralateral anterior interposed and fastigial nuclei, but did not label cells within the vestibular nuclei. Examination of thalamic terminations after tracer injections into the cerebellar and vestibular nuclei indicated that most vestibular responsive units fall within the thalamic terminal zones of these nuclei. Thus, vestibular signals, which are supplied to the thalamus from both vestibular and cerebellar nuclei, are positioned for distribution to widespread cortical areas.

Key words: sensorimotor; thalamocortical; cerebellar nuclei; vestibular nuclei; translation; semicircular canals; motion; otolith organs

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Received Aug. 28, 2007; revised Oct. 3, 2007; accepted Oct. 22, 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

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