The neurophysiological substrate for the cervico-ocular reflex in the squirrel monkey

Abstract

Passive rotation of the trunk with respect to the head evoked cervico-ocular reflex (COR) eye movements in squirrel monkeys. The amplitude of the reflex varied both within and between animals, but the eye movements were always in the same direction as trunk rotation. In the dark, the COR typically had a gain of 0.3-0.4. When animals fixated earth-stationary targets during low-frequency passive neck rotation or actively tracked moving visual targets with head movements, the COR was suppressed. The COR and vestibulo-ocular reflex (VOR) summed during passive head-on-trunk rotation producing compensatory eye movements whose gain was greater than 1.0. The firing behavior of VOR-related vestibular neurons and cerebellar flocculus Purkinje cells was studied during the COR. Passive neck rotation produced changes in firing rate related to neck position and/or neck velocity in both position-vestibular-pause neurons and eye-head-vestibular neurons, although the latter neurons were much more sensitive to the COR than the former. The neck rotation signals were reduced or reversed in direction when the COR was suppressed. Flocculus Purkinje cells were relatively insensitive to COR eye movements. However, when the COR was suppressed, their firing rate was modulated by neck rotation. These neck rotation signals summed with ocular pursuit signals when the head was used to pursue targets. We suggest that the neural substrate that produces the COR includes central VOR pathways, and that the flocculus plays an important role in suppressing the reflex when it would cause relative movement of a visual target on the retina.

Brain Stem Pursuit Pathways: Dissociating Visual, Vestibular, and Proprioceptive Inputs During Combined Eye-Head Gaze Tracking

“…Studies in squirrel monkey have suggested that EH neurons respond to changes in neck position or velocity during passive rotation of the monkey's body with its head-held stationary in space (Gdowski and McCrea 2000;Gdowski et al 2001). In contrast, when we tested neurons with a comparable paradigm in the present study, we found no influence of passive neck activation in rhesus monkeys (Fig.…”

“…Studies in alert squirrel monkey have suggested that most second-order neurons in the medial vestibular nuclei including EH neurons are influenced by passive activation of neck proprioceptors McCrea 1999, 2000;Gdowski et al 2001). In contrast, our recent studies in rhesus monkey have found no evidence that second-order neurons within the medial vestibular nuclei are influenced by neck proprioceptive inputs Cullen 2001, 2002).…”

“…1993;McCrea 1999, 2000;Gdowski et al 2001;McCrea et al 1996;McFarland and Fuchs 1992;Scudder and Fuchs 1992). Specifically, neurons were modulated in response to head velocity during pWBRc and to eye velocity in the same direction during smooth-pursuit eye movements (see following text).…”

“…11A). Gdowski and colleagues (Gdowski and McCrea 2000;Gdowski et al 2001) also tested neurons during a paradigm in which the monkey's head was passively rotated on its earth-stationary body and found that neuronal responses to head motion were different from during passive wholebody rotation. They argued that EH neurons could mediate, in part, the cervicoocular reflex (COR), which functions to produce compensatory eye movements in response to unexpected neck motion.…”

“…The responses of these brain stem neurons largely correspond with those of a distinct physiological subclass of cells, termed eye-head (EH) neurons, which have been well characterized during eye and head movements in the head-restrained monkey (Chen-Huang and McCrea 1999;Cullen at al. 1993;McCrea 1999, 2000;Gdowski et al 2001;McCrea et al 1996;McFarland and Fuchs 1992;Scudder and Fuchs 1992;Tomlinson and Robinson 1984). Accordingly, for the sake of simplicity, both FTN and EH neurons will be referred to from here on as EH neurons (although these 2 populations of neurons may not be strictly equivalent).…”