Canal and Otolith Contributions to Compensatory Tilt Responses in Pigeons

Abstract

McArthur KL, Dickman JD. Canal and otolith contributions to compensatory tilt responses in pigeons. J Neurophysiol 100: 1488 -1497, 2008. First published July 16, 2008 doi:10.1152/jn.90257.2008. Gazestabilizing eye and head responses compensate more effectively for low-frequency rotational motion when such motion stimulates the otolith organs, as during earth-horizontal axis rotations. However, the nature of the otolith signal responsible for this improvement in performance has not been previously determined. In this study, we used combinations of earth-horizontal axis rotational and translational motion to manipulate the magnitude of net linear acceleration experienced by pigeons, under both head-fixed and head-free conditions. We show that phase enhancement of eye and head responses to low-frequency rotational motion was causally related to the magnitude of dynamic net linear acceleration and not the gravitational acceleration component. We also show that canal-driven and otolithdriven eye responses were both spatially and temporally appropriate to combine linearly, and that a simple linear model combining canaland otolith-driven components predicted eye responses to complex motion that were consistent with our experimental observations. However, the same model did not predict the observed head responses, which were spatially but not temporally appropriate to combine according to the same linear scheme. These results suggest that distinct vestibular processing substrates exist for eye and head responses in pigeons and that these are likely different from the vestibular processing substrates observed in primates.

Spatial and temporal characteristics of vestibular convergence

“…In a previous study, we demonstrated that pigeons integrate canal and otolith signals to generate compensatory responses to EHA rotation (McArthur and Dickman 2008). Thus, we transformed the maximum sensitivity vectors for canal (α CANAL ) and otolith (α OTO ) response components, to predict each component’s maximum sensitivity vector for EHA rotation (see Methods for details).…”

“…For pigeons and other lateral-eyed animals, both canal and otolith stimulation contribute to compensatory eye and head responses that stabilize gaze during rotation relative to gravity (i.e. EHA rotation; pigeon: Dickman and Angelaki 1999; Dickman, Beyer and Hess 2000; McArthur and Dickman 2008; mouse: Harrod and Baker 2003; rat: Brettler et al 2000; rabbit: Barmack 1981). Specifically in pigeons, we have demonstrated that a dynamic net head-horizontal linear acceleration signal improves the phase of both eye and head responses to EHA tilt (McArthur and Dickman 2008).…”

“…EHA rotation; pigeon: Dickman and Angelaki 1999; Dickman, Beyer and Hess 2000; McArthur and Dickman 2008; mouse: Harrod and Baker 2003; rat: Brettler et al 2000; rabbit: Barmack 1981). Specifically in pigeons, we have demonstrated that a dynamic net head-horizontal linear acceleration signal improves the phase of both eye and head responses to EHA tilt (McArthur and Dickman 2008). Indeed, the canal- and otolith-driven components of these responses are spatially aligned with one another when examined separately (Dickman and Angelaki 1999; McArthur and Dickman 2008).…”

“…In pigeons, the head response provides the primary means for active gaze stabilization, with magnitudes that far exceed that of the eye-in-head response when the head is free to move (Gioanni 1988; Haque and Dickman 2005). In a previous study, we used discrete combinations of canal and otolith stimulation to demonstrate that pigeons integrate these signals when generating eye and head responses to rotation (McArthur and Dickman 2008). Results were consistent with a linear combination of canal- and otolith-generated response components during rotational VOR.…”

Behavioral State Modulates the Activity of Brainstem Sensorimotor Neurons

“…For rotational stimuli, neural gains were expressed as the peak change in IFR (spk/s) relative to peak angular velocity (°/s), and phase values were expressed relative to peak positive angular velocity. Responses to translational stimuli were expressed relative to the apparent tilt-that is, the earth-horizontal axis rotation that would produce the equivalent linear acceleration stimulus in the head (McArthur and Dickman, 2008). For example, an x-axis (fore-aft) translation (0.5 Hz, 0.1G) would correspond to an apparent y-axis (pitch) tilt (0.5 Hz, Ϯ6°, ϳ20°/s), allowing us to directly compare neural responses to these two stimuli where the linear acceleration stimulus to the animal was matched.…”