A frequency and time domain study of the horizontal and vertical vestibuloocular reflex in the pigeon

Abstract

1. The horizontal and vertical vestibuloocular reflex (HVOR and VVOR, respectively) was studied in four chronically instrumented pigeons. Eye movements were measured using the magnetic search-coil technique and were produced by rotation in the dark. During the rotation paradigms, the pigeons were either pharmacologically aroused (using amphetamine) or drug free (normal). The pigeon HVOR and VVOR were tested using step and sinusoidal rotational stimulation. The range of frequencies (0.03-6.0 Hz) and the magnitude of the sinusoidal stimuli were chosen to match those used in a previous study of the responses of semicircular canal primary afferents (SCPAs) in unanesthetized (i.e., normal) pigeons. 2. The gain of the HVOR and VVOR in both normal and aroused pigeons was independent of stimulus magnitude (6-30 degrees/s) over the frequency range tested. In aroused pigeons, the frequency independent gain (G) of the HVOR (G = 0.6) and VVOR (G = 0.9) was roughly twice that for normal pigeons. Pigeon VOR phase under all combinations of orientation and arousal level was independent of stimulus magnitude except at the lowest frequency tested (0.03 Hz). At this frequency, phase lead decreased as stimulus magnitude increased for the HVOR and VVOR in both normal and aroused pigeons. 3. The step and sinusoidal gains were greater for the VVOR than for the HVOR under the same level of arousal. Neither the gain nor the dominant time constant of the VOR (tau vor) differed for rotation direction (clockwise or counterclockwise) for the HVOR or VVOR in normal or aroused pigeons. 4. The mean value of tau vor was 4.0 +/- 0.5 (SE) s as estimated from frequency response data and 4.3 +/- 0.4 s as estimated from step response data for the HVOR and VVOR in both normal and aroused pigeons. In comparison, the mean value of the dominant or cupular time constant (tau c) of normal pigeon SCPAs was approximately 10 s as estimated from frequency response data. These results indicate that tau vor is shorter than tau c in the pigeon. 5. At higher frequencies, the pigeon HVOR and VVOR exhibit an increasing phase lag unaccompanied by a gain change--characteristics produced by a pure time delay. The value of this time delay was about 7 ms for both the HVOR and VVOR in both normal and aroused pigeons. The HVOR and VVOR in normal and aroused pigeons lacked the higher frequency lead characteristics present in the frequency responses of most pigeon SCPAs.

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

“…The 3-D VOR responses to rotational motion observed in this study with the animal's head fixed were comparable with those reported previously for lateral-eyed birds (Anastasio and Correia 1988;Dickman et al 2000). In complete darkness, both the pigeon and the quail VOR slow-phase eye velocity gains were severely undercompensatory for visual stabilization relative to head velocity, regardless of the plane of rotational motion.…”

“…Some vertical and torsional eye movement components were present; however, these secondary responses were typically an order of magnitude less than the primary component response. As previously reported for birds, saccades (and fast phases) were followed by a brief high-frequency eye oscillation (ϳ30 Hz) (Anastasio and Correia 1988;Dickman et al 2000;Nye 1969;Wallman and Pettigrew 1985). Figure 2B shows the responses from the same pigeon during EVA rotation with its head free to move.…”

“…Although previous studies have investigated the different components that contribute to bird gaze stabilization including eye movements (Anastasio and Correia 1988;Dickman and Angelaki 1999;Dickman et al 2000;Nye 1969), vestibulocollic responses (Gioanni 1988a;Gioanni and Sansonetti 1999), neck muscle activation (Hayman and Donaldson 1997;Hayman et al 1993), and behavior (Nalbach 1992;Troje and Frost 2000;Turke et al 1996;Wohlschlager et al 1993), in this study, we have shown for the first time differences in gaze control strategies between two different bird species. Specifically, we found that, unlike the undercompensatory head-fixed VOR for both pigeons and quails, gaze was completely compensatory during normal head motion.…”

“…In complete darkness, both the pigeon and the quail VOR slow-phase eye velocity gains were severely undercompensatory for visual stabilization relative to head velocity, regardless of the plane of rotational motion. Higher VOR gains have been reported for pigeons receiving amphetamines, although those values still remained undercompensatory (Anastasio and Correia 1988;Gioanni 1988a). Like all animals, pigeons and quails exhibit a VOR response in the dark that is dependent on stimulus frequency.…”

Membrane and firing properties of avian medial vestibular nucleus neurons in vitro

“…We suspect that the membrane properties of hatchling chicks have attained the adult state: we found no differences in properties of 1 and 12 day olds, and furthermore, the adaptive capabilities of the VOR, presumably mediated by a subset of our sample of neurons, are present in newborn chicks (Wallman et al 1982). The similarities between birds and mammals in the physiology, anatomy, and behavioral properties of the VOR (Anastasio and Correia 1988;Anastasio et al 1985;Cox and Peusner 1990b;Labandeira-Garcia et al 1989;du Lac and Lisberger 1992;Petersdottir 1990;Wold 1978), coupled with our findings, discussed below, that avian MVN neurons appear identical to those recorded in rodents, suggest that it is reasonable to relate the intrinsic properties of avian MVN neurons with the response properties of their mammalian counterparts.…”