Visual and vestibular reflexes that stabilize gaze in the chameleon

Abstract

Spontaneous eye movements as well as visual, vestibular, and proprioceptive cervical reflexes which contribute to gaze stabilization were investigated in the chameleon using the magnetic search-coil technique. The oculomotor range of each eye was very large (180 deg horizontally x 80 deg vertically). Spontaneous ocular saccades were independent in the two eyes and could have very large amplitudes. The fast phases of nystagmus during the stabilization reflexes were also independent in the eyes. In the head-restrained condition, optokinetic nystagmus (OKN) had a low gain in both horizontal and vertical planes (0.35 at 5 deg/s) and showed little binocular interaction. The vestibulo-ocular reflex (VOR) exhibited a low gain (0.2-0.3 from 0.05-1 Hz) and a high-phase lead at low frequency (140 deg at 0.05 Hz). Rotation of the animal in the presence of a visible surround increased the overall gain of gaze stabilization to 0.4-0.5 (P < 0.01) and considerably reduced the phase lead (38 deg at 0.05 Hz). In the head-free condition, head and eye reflexes were active simultaneously during both optokinetic and vestibular stimulation, but nystagmic head movements appeared only occasionally with a rather loose eye-head coordination. During optokinetic stimulation, eye movements contributed more than head movements to gaze stabilization, whereas, during vestibular or visuo-vestibular stimulation, the relative contribution of eye and head responses varied with stimulus frequency. When the head was freed, overall gain for gaze stabilization increased from 0.35 to 0.45 (P < 0.05) for optokinetic stimulation at 5 deg/s and from 0.2-0.3 to 0.4-0.75 (P < 0.001) for vestibular stimulation at 0.05-1 Hz. Optimal gaze stabilization (gain of 0.8) was only obtained with combined visual and vestibular stimulation in the free-head condition. Cervical stimulation provoked a compensatory cervico-ocular reflex (COR) with a gain of 0.2-0.4 as well as ocular saccades, which were especially numerous in the presence of a visual surround. The direction of these saccades alternated between compensatory and anti-compensatory.

Eye movements of laterally eyed birds are not independent

“…In accordance with our results, Bloch and colleagues describe converging binocular saccades towards frontally presented stimuli in pigeons, but in contrast to our results in zebra finches, the pigeons reacted to lateral stimulation with only one attending eye, the other eye showing no coordinated movements (Bloch et al, 1986). The pigeon results are in accordance with observations in chameleons where left and right eyes are synchronized during prey tracking (Ott, 2001), and spontaneous eye movements can be independent in direction and amplitude (Gioanni et al, 1993). In contrast, zebra finches only use one eye to move towards a target after stimulation in both lateral visual fields.…”

Vestibular Gaze Stabilization: Different Behavioral Strategies for Arboreal and Terrestrial Avians

“…Dieringer et al (1983) examined eye and head contributions to gaze stability in frogs and turtles and determined that the head played a major role in stabilization (Ͼ80%), with the eyes only being used in a transient manner. In chameleons, which also happen to have a very large oculomotor range, undercompensatory gaze was observed during rotational motion, with the head once again contributing the major response component (Gioanni et al 1993). Collewijn (1977) noted similar results in rabbits to those observed in our study, with VCR gains during head-free conditions to reach near unity in the dark, with a small eye movement component.…”

“…Eye movements in response to head motion have been extensively studied in a variety of vertebrate species ranging from fish to primates (Escudero et al 1993). In lateral-eyed species, such as frogs (Dieringer and Precht 1982), lizards (Gioanni et al 1993), rabbits (Baarsma and Collewijn 1974), chinchillas (Merwin et al 1989), and guinea pigs (Escudero et al 1993), eye movements in response to motion when the head is fixed have largely been shown to be undercompensatory. For example, in pigeons, we recently found that the three-dimensional (3-D) vestibuloocular (VOR) responses to both rotational and linear motion were significantly undercompensatory in gain (Dickman and Angelaki 1999;Dickman et al 2000).…”

Visual resolution and contrast sensitivity in two benthic sharks

“…Our findings support the existence of a monocularly organised oculomotor system in sharks (Maxwell, 1920;Masseck and Hoffmann, 2008). Monocular organisation is more common in animals with laterally positioned eyes as described for some teleost fishes [sandlance, Lymnichthyes fasciatus, and pipefish, Corythoichthyes intestinalis (Fritsches and Marshall, 2002;Pettigrew et al, 1999)] and the chameleon, Chamaleo chamaleo (Gioanni et al, 1993;Pettigrew et al, 1999). The contralateral placement of the medial rectus motor neurons in the midbrain of sharks differs from most vertebrates, which may allow eye movements to be controlled independently (Graf and Brunken, 1984).…”