Otolith and canal integration on single vestibular neurons in cats

Abstract

In this review, based primarily on work from our laboratory, but related to previous studies, we summarize what is known about the convergence of vestibular afferent inputs onto single vestibular neurons activated by selective stimulation of individual vestibular nerve branches. Horizontal semicircular canal (HC), anterior semicircular canal (AC), posterior semicircular canal (PC), utricular (UT), and saccular (SAC) nerves were selectively stimulated in decerebrate cats. All recorded neurons were classified as either projection neurons, which consisted of vestibulospinal (VS), vestibulo-oculospinal (VOS), vestibulo-ocular (VO) neurons, or non-projection neurons, which we simply term "vestibular'' (V) neurons. The first three types could be successfully activated antidromically from oculomotor/trochlear nuclei and/or spinal cord, and the last type could not be activated antidromically from either site. A total of 1228 neurons were activated by stimulation of various nerve pair combinations. Convergent neurons were located in the caudoventral part of the lateral, the rostral part of the descending, and the medial vestibular nuclei. Otolith-activated vestibular neurons in the superior vestibular nucleus were extremely rare. A high percentage of neurons received excitatory inputs from two nerve pairs, a small percentage received reciprocal convergent inputs and even fewer received inhibitory inputs from both nerves. More than 30% of vestibular neurons received convergent inputs from vertical semicircular canal/otolith nerve pairs. In contrast, only half as many received convergent inputs from HC/otolith-nerve pairs, implying that convergent input from vertical semicircular canal and otolith-nerve pairs may play a more important role than that played by inputs from horizontal semicircular canal and otolith-nerve pairs. Convergent VS neurons projected through the ipsilateral lateral vestibulospinal tract (i-LVST) and the medial vestibulospinal tract (MVST). Almost all the VOS neurons projected through the MVST. Convergent neurons projecting to the oculomotor/trochlear nuclei were much fewer in number than those projecting to the spinal cord. Some of the convergent neurons that receive both canal and otolith input may contribute to the short-latency pathway of the vestibulocollic reflex. The functional significance of these convergences is discussed.

Response of Vestibular Nerve Afferents Innervating Utricle and Saccule During Passive and Active Translations

“…Given that the majority of the neurons in the vestibular nuclei receive convergent inputs from multiple vestibular end organs (Curthoys and Markham 1971;Dickman and Angelaki 2002;Kaufman et al 2000;Markham and Curthoys 1972;McConville et al 1996;Straka et al 2002;Tomlinson et al 1996;Uchino et al 2005;Yakushin et al 2006;Zakir et al 2000;Zhang et al 2001), it seems logical that a comparable strategy is used for encoding both linear and rotation acceleration at the level of the vestibular periphery. As such, otolith-derived reafference can be suppressed at the level of vestibular nuclei in a manner comparable to canal-derived inputs (McCrea et al 1999;Cullen 2001, 2004).…”

Canal–Otolith Interactions and Detection Thresholds of Linear and Angular Components During Curved-Path Self-Motion

“…However, the two sets of signals converge onto single central vestibular neurons as early as the vestibular nuclei (Angelaki and Dickman 2003;Bush et al 1993;Dickman and Angelaki 2002;Jian et al 2002;Uchino et al 2005;Yakushin et al 2006;Zhang et al 2001Zhang et al , 2002. The functional significance of this convergence has been of interest for some time.…”

The Cervical Vestibular-Evoked Myogenic Potentials (cVEMPs) Recorded Along the Sternocleidomastoid Muscles During Head Rotation and Flexion in Normal Human Subjects

“…Based on the synaptic organizations of the VCR shown in Figure 6, the SCM motoneurons receive excitatory inputs from all the three contralateral canals and the utricle, which are comparable in strength to the inhibitory inputs from all the three ipsilateral canals and the two otoliths (for review, Uchino et al 2005). Based on this model, the contracVEMPs are expected to exhibit similar amplitudes to the ipsi-cVEMPs with reversed polarity.…”

“…However, this prediction is not validated by data of the present study and the study of Li et al (1999). It is worth noting that the VCR synaptic connectivity patterns shown in Figure 6 are derived from studies in cats (for review, Uchino et al 2005). Since it has been well documented that non-primate quadrupeds such as cats have very different neck-muscle organization than human bipeds (Graf et al 1994;Richmond et al 2001;Corneil et al 2001), it is possible that the VCR connectivity patterns in humans are different from that in cats.…”