The coding of head orientations in neurons of bilateral vestibular nuclei of cats after unilateral labyrinthectomy: response to off-vertical axis rotation

Abstract

In decerebrate cats that had been acutely hemilabyrinthectomized (HL), the extracellular activities of vestibular nuclear neurons on the lesioned and labyrinth-intact sides were studied during constant-velocity off-vertical axis rotations (OVAR) in the clockwise (CW) and counterclockwise (CCW) directions (at 10 degrees tilt). Over the range of 1.75-15 degrees/s, two types of neuronal responses were identified on both sides. Some neurons showed symmetric and velocity-stable bidirectional response sensitivity (delta defined as the CW gain over the CCW gain) while other neurons exhibited asymmetric and velocity-variable delta. The mathematically derived gain tuning ratios of these two groups of neurons were within the range of one-dimensional and two-dimensional neurons respectively. The best response orientations in one-dimensional neurons and the orientations of the maximum response vector, S(max), in two-dimensional neurons were found to point in all directions on the horizontal plane. On the labyrinth-intact side, both the one-dimensional and two-dimensional neurons showed asymmetry in the neuron numbers and/or the response gains between the two roll quadrants as well as between the two pitch quadrants. In addition, both the neuron number and gain were significantly higher for neurons in the head-down/ipsilateral-side-down half-circle than those in the head-up/contralateral-side-down half-circle. None of the aforementioned asymmetries was observed on the lesioned side. That a comparable pattern of distribution was observed in the one-dimensional and two-dimensional neurons suggests that these neurons maintain a common spatial reference frame in encoding head orientational signals arising from the ipsilateral and contralateral otoliths. Furthermore, a predominance of two-dimensional neurons that exhibited a greater gain with CW rotations was observed on both sides of HL cats. Of the response dynamics observed amongst neurons on the two sides of HL cats, no difference was found with regard to the response gain and the pattern of response lead. However, a difference in response lag was observed between neurons on the two sides of HL cats. These suggest that there is a segregation of otolithic signals to reach the ipsilateral and contralateral vestibular nuclei. Taken together, the present study demonstrates that one-dimensional and two-dimensional neuronal responses could be elicited with inputs arising solely from the ipsilateral or contralateral otoliths. The observed orientational tuning and the CW-CCW asymmetry to bidirectional rotation may provide the essential directional coding of head orientations. Further, the imbalance of spatial/dynamic response patterns between the bilateral vestibular nuclei following the restriction of otolith inputs by HL implies that converging otolithic inputs from the bilateral labyrinths are essential for producing the neuronal responses in control animals. The results are also discussed in terms of the possible contribution of the various neural asymmetries between neuronal subp...

Development of the Vestibular System

“…Such a uniform spatial distribution was also observed in the cerebellar fastigial nucleus [82] and medial medullary reticular formation [86] of adult cats. However, an imbalance of spatial response patterns between the bilateral vestibular nuclei was observed following the restriction of otolith inputs by hemilabyrinthectomy [87,88]. This finding implies that in the normal state, where both labyrinths are intact, the crossed otolith signals serve to complement and supplement inputs arising from the ipsilateral otolith.…”

Developmental expression of NMDA and AMPA receptor subunits in vestibular nuclear neurons that encode gravity‐related horizontal orientations

“…First, Fos expression was triggered by defined sensory input (Dragunow and Faull, 1989) in nuclei of neurons but not glial cells (Mughaini et al, 1989). Second, constant-velocity OVAR has been the modus operandi for triggering otolithic neuronal activities (Reisine and Raphan, 1992;Manzoni et al, 1995;Chan, 1997;Chan et al, 1999;Lai and Chan, 2001) and otolithic reflexes (Cohen et al, 1983;Hess and Dieringer, 1990;Angelaki and Hess, 1996). This mode of scanning stimulus sequentially activates all utricular hair cells because of their multidirectional sensitivities close to the horizontal plane (cf.…”

Fos expression in otolith‐related brainstem neurons of postnatal rats following off‐vertical axis rotation

“…In the present study, constant-velocity OVAR was a suitable scanning stimulus that sequentially activates all the utricular hair cells by introducing a rotating gravity vector about the head (Cohen et al, 1983). Electrophysiological studies in canal-plugged animals also revealed that OVAR-evoked neuronal responses were due to selective stimulation of the utricle (Cohen et al, 1983;Chan, 1997;Fig. 6.…”

“…This mode of stimulation is also an established stimulus for the study of otolithic neuronal activities (Reisine and Raphan, 1992;Manzoni et al, 1995;Chan, 1997) and otolithic reflexes (Cohen et al, 1983;Hess and Dieringer, 1990;Angelaki and Hess, 1996). With the use of OVAR, central otolith neurons that have established functional connection(s) with hair cells on any sector of the utricular maculae should be excited and should express Fos.…”