Vestibular Convergence Patterns in Vestibular Nuclei Neurons of Alert Primates

Abstract

Sensory signal convergence is a fundamental and important aspect of brain function. Such convergence may often involve complex multidimensional interactions as those proposed for the processing of otolith and semicircular canal (SCC) information for the detection of translational head movements and the effective discrimination from physically congruent gravity signals. In the present study, we have examined the responses of primate rostral vestibular nuclei (VN) neurons that do not exhibit any eye movement-related activity using 0.5-Hz translational and three-dimensional (3D) rotational motion. Three distinct neural populations were identified. Approximately one-fourth of the cells exclusively encoded rotational movements (canal-only neurons) and were unresponsive to translation. The canal-only central neurons encoded head rotation in SCC coordinates, exhibited little orthogonal canal convergence, and were characterized with significantly higher sensitivities to rotation as compared to primary SCC afferents. Another fourth of the neurons modulated their firing rates during translation (otolith-only cells). During rotations, these neurons only responded when the axis of rotation was earth-horizontal and the head was changing orientation relative to gravity. The remaining one-half of VN neurons were sensitive to both rotations and translations (otolith + canal neurons). Unlike primary otolith afferents, however, central neurons often exhibited significant spatiotemporal (noncosine) tuning properties and a wide variety of response dynamics to translation. To characterize the pattern of SCC inputs to otolith + canal neurons, their rotational maximum sensitivity vectors were computed using exclusively responses during earth-vertical axis rotations (EVA). Maximum sensitivity vectors were distributed throughout the 3D space, suggesting strong convergence from multiple SCCs. These neurons were also tested with earth-horizontal axis rotations (EHA), which would activate both vertical canals and otolith organs. However, the recorded responses could not be predicted from a linear combination of EVA rotational and translational responses. In contrast, one-third of the neurons responded similarly during EVA and EHA rotations, although a significant response modulation was present during translation. Thus this subpopulation of otolith + canal cells, which included neurons with either high- or low-pass dynamics to translation, appear to selectively ignore the component of otolith-selective activation that is due to changes in the orientation of the head relative to gravity. Thus contrary to primary otolith afferents and otolith-only central neurons that respond equivalently to tilts relative to gravity and translational movements, approximately one-third of the otolith + canal cells seem to encode a true estimate of the translational component of the imposed passive head and body movement.

Vestibular Signals in Primate Thalamus: Properties and Origins

“…The departure from cosine tuning is captured by the "tuning ratio," defined in the range between 0 and 1, as the ratio of the minimum over the maximum neural response gain. Figure 3A plots the distribution of tuning ratios during translation at 0.5 Hz, which was broad, and similar to that found in VN/CN neurons (Angelaki and Dickman, 2000;Dickman and Angelaki, 2002;Shaikh et al, 2005a). Thalamic neurons with tuning ratios close to zero were mostly cosine-tuned during translation along different directions in the horizontal plane.…”

“…There was a large cell-tocell variability in thalamic cell responses to translation, similar to that found in VN and CN neurons (Angelaki and Dickman, 2000;Dickman and Angelaki, 2002;Shaikh et al, 2005a). We have used a spatiotemporal analysis to describe each cell's tuning as a set of two orthogonal response vectors (Angelaki, 1991;Angelaki and Dickman, 2000).…”

“…Also superimposed in Figure 3D is the gain and phase dependence on frequency for neurons in the cerebellar nuclei (mostly rostral fastigial) (Shaikh et al, 2005a). Data from VN neurons are not shown because VN cell dynamics were more variable, ranging from gain increases to gain decreases, and phase lags to phase leads (Angelaki and Dickman, 2000;Dickman and Angelaki, 2002).…”

“…These studies, which were limited to yaw plane stimulation, reported that yaw response dynamics of thalamic neurons are similar to those in VN (Büttner et al, 1977). More recently, the response properties of VN and CN neurons have been characterized in detail using translations and rotations about multiple axes (Dickman and Angelaki, 2002;Angelaki et al, 2004;Shaikh et al, 2005a,b;Chen-Huang and Peterson, 2006;Yakushin et al, 2006). It remains to be determined whether the similarity between brainstem and thalamic response properties extends beyond yaw rotation.…”

Responses of caudal vestibular nucleus neurons of conscious cats to rotations in vertical planes, before and after a bilateral vestibular neurectomy

“…Although a variety of studies have considered the responses of vestibular nucleus neurons to rotations and translations of the head (e.g., Chubb et al 1984;Kasper et al 1988;Gdowski and McCrea 1999;Dickman and Angelaki 2002;Zhou et al 2006), virtually all of these experiments have focused on units in the rostral or middle portions of the nuclear complex. With the exception of a small GABAergic cell population that comprises the parasolitary nucleus (Barmack and Yakhnitsa 2000), the caudal vestibular nuclei (CVN) have not been extensively studied, particularly in conscious animals.…”