Compensatory Head Movements Research Articles

Differences in the central organization of gaze stabilizing reflexes between frog and turtle

1. Compensatory eye and head movements, and responses of central vestibular neurons of frogs and turtles were investigated. 2. Eye movements (head restrained) evoked by optokinetic stimulation reach low peak slow phase velocities in both species: 1.5 °/s in frog and ca. 4 °/s in turtle. The optimal working range of the ocular optokinetic system is restricted to stimulus velocities <1 °/s. Optokinetic-afternystagmus (OKAN) of the eyes is absent in frog (n = 14) and can be present in turtle (one out of five animals). 3. Head movements evoked by optokinetic stimuli reach higher velocities in both species than the eyes and gaze is stabilized by head movements up to 80% of the stimulus velocity within the different working ranges (up to ca. 4 °/s in frog and up to ca. 25 °/s in turtle). Head OKAN is absent in frog (n = 23) and present in turtle (n = 10). OKAN head velocity in turtle decays linearly with apparent time constants between 6 and 12 s (for 20 °/s stimulus velocity). 4. Vestibular per/postrotatory nystagmus (PRN) of the head is short in frog (2–4 s in duration) compared to that in the turtle, where PRN head velocity decays linearly with apparent time constants between 7 and 11s (for 20 °/s velocity steps). Parametric similarities of OKAN and PRN and almost perfect cancellation of head PRN by head OKAN for velocity steps below 30 °/s in the turtle suggest a common neuronal storage for optokinetically and vestibularly evoked head velocity signals. 5. Eye-head coordination is very similar in both species. Fast phases resetting the position of eyes and head are coupled. The major contribution of the ocular motor system is restricted to brief transient periods (at the onset of compensatory movements; after each fast phase) during which the neck motor system more slowly accelerates the head. 6. Responses of central vestibular neurons to velocity steps have short time constants (1–4 s) in alert frogs and optokinetic stimuli modulate the activity of these neurons only exceptionally (2 out of 82). In the turtle, apparent time constants are longer (between 6 and 14 s, mean ca. 9 s) and resting activity of 10 out of 11 neurons was optokinetically modulated. 7. Like the behavioral data, vestibular unit data contain evidence for a functioning velocity storage network in turtles, but not in frogs. These differences in the properties of gaze stabilizing reflexes are discussed in relation with the differing demands that result from differences in the locomotory repertoires of the two species.

Compensatory head and eye movements in the frog and their contribution to stabilization of gaze

Compensatory head movements, recorded in unrestrained frogs, were compared to compensatory eye movements recorded from animals that had their head fixed. Movements were evoked by oscillating the animal in the dark (vestibular stimulation) or in the light in front of an earth-fixed, patterned visual background (combined stimulation) or by rotating vertical black and white bars (optokinetic stimulation) around the stationary animal. Oscillations occurred in the horizontal plane at frequencies between 0.025 and 0.5 Hz. Gain and phase values of head and eye movements, relative to stimulus movements were calculated. Evoked eye movements were limited in amplitude to +/- 3-6 degrees, increasing with the size of the animal. Head movements were limited to +/- 30-40 degrees. Resetting fast-phases of both head and eyes were very rarely observed during sinusoidal stimulation and no eye movements were recorded in the absence of intended head movements. Vestibularly evoked head movements exhibited a frequency-dependent threshold that was not observed for vestibulo-ocular responses. Above threshold, the gain of evoked head responses increased and reached a frequency-dependent plateau at which the system behaved approximately linearly. Within the linear range, gain of vestibularly evoked responses increased with frequency (from 0.04 at 0.025 Hz to 0.75 at 0.5 Hz) and phase lead decreased (from about 80 degrees to 0 degrees). Vestibularly evoked eye movements similarly increased in gain from 0.05 to 0.56 and decreased in phase lead from about 56 degrees to 10 degrees over the same frequency range. Optokinetically evoked head and eye movements had their highest gains (about 0.8 and 0.5) at low constant velocities (less than or equal to 1-4 degrees/S) or frequencies (less than or equal to 0.025 Hz). At higher constant velocities or frequencies the gain dropped. The phase lag increased from close to zero (at 0.025 Hz) to about 60 degrees for the head and to about 20 degrees for the eye movements (at 0.25 Hz). These phase lags are explained by reaction times of the evoked movements of about 600 ms (head) and 200 ms (eyes). Combined stimulation evoked compensatory head movements with gain and phase values that were frequency-independent in the linear range. Head movements compensated for about 80-90% of the imposed gaze shift with a small phase lag (0-10 degrees). Evoked eye movements were found to be large enough in amplitude and fast enough in time to enable a frog to stabilize its gaze exclusively with slow phase compensatory movements for a large variety of frequency and amplitude combinations. The two motor systems controlling movements of the head and the eye are matched in such a way that the non-linearities of the evoked eye movements can compensate for the non-linearities of the evoked head movements.

Gravity reception in the walking fly, Calliphora erythrocephala: Tonic and modulatory influences of leg afferents on the head position

The proprioceptive gravity receptor system of the fly, Calliphora erythrocephala, is functionally organized in a manner similar to the statocyst system in vertebrates, molluscs and crustaceans. It includes one system in which excitation is modulated by the gravitational stimulus, and another which exerts a tonic excitation on the neurones of the reflex arc between the leg receptors and the neck muscles. While the modulating system for the compensatory head movement of the walking flies is located only in the forelegs and the middle legs, the tonic excitation is mediated by receptors of all legs.

Involvement of the pontine reticular formation in head movements and labyrinthine righting in the rat

Compensatory head movements as responses to passive angular acceleration are obvious in lower vertebrates, but they are usually small and difficult to observe in mammals. The may simply be cut short very early by an inhibitory mechanism linked to the initiation of anticompensatory head movements (quick phases of head nystagmus). After electrolytic lesions of the pontine reticular formation (PRF), rats made no spontaneous lateral head movements, but exhibited large compensatory lateral head movements and abnormal postrotatory circus movements, both of which can be regarded as consequences of a loss of the quick phase of head nystagmus. The quick phase of ocular nystagmus was also lost, corroborating earlier findings of others in primates, cats, and rabbits, and supporting the view that saccadic movements of the head and eyes are generated by closely related neural substrates. Rats with bilateral PRF lesions were unable to right themselves in the air. Together with additional observations, this indicates involvement of the PRF in some functions of the otolith organ.

Angular acceleration, compensatory head movements and the halteres of flies (Lucilia serricata)

Tethered flies were subjected to accelerations about their vertical axes while flying or walking. These accelerations were applied either suddenly to stationary animals or continuously by oscillating the animal from side to side. Head and wing movements resulting from the imposed angular accelerations were photographed with a camera and a stroboscopic flash.

The role of integrators in maintaining actively assumed abnormal postures

1. Geckos adapt their head-position to the spatial orientation of substrates they are actively moving on. Furthermore an adaptation of head-position is carried out in response to structures in the animal's vicinity. We found a tendency to keep the ventral side of the head orientated towards such objects. Thus, in geckos, visual guidance overrides vestibular mechanisms inducing compensatory head-movements during abnormal body postures in many other species. 2. Compensatory head-movements during optokinetic, vestibular, and combined optokinetic and vestibular stimulation in restrained geckos also revealed a dominant role of vision in guiding postural control in these animals. Vestibular influences on head-position are weak as long as optokinetic cues are absent. With optokinetic stimulation present vestibular afferents significantly increase the gain of the optokinetic response. This effect is the more obvious the higher the optokinetic stimulation speed is. 3. When a head-position deviating from the normal position has been actively assumed in response to either one of the above conditions it is not instantaneously abolished after the inducing stimulus ceases to be present. The head returns to a position normal with respect to the body by a slow drift that takes several minutes. This drift is faster when visual stabilization is interrupted by darkness as compared to a situation with the experimental room illuminated. 4. We conclude that geckos have integrators through which postural change commands (e.g. from the visual system) are fed before interacting with postural control circuits. These mechanisms maintain actively assumed abnormal postures after cessation of the inducing command. Comparative investigations suggest that such mechanisms are present in many species of lizards and are especially well developed in animals that frequently assume different body orientations with respect to the gravity vector in their habitat.

The Optokinetic Basis of Head-Bobbing in the Pigeon

ABSTRACT Head-bobbing of pigeons during walking and landing was studied using high-speed motion photography. The analysis of film records indicated that head-bobbing whilst walking consists of two phases: one where the head is ‘locked’ in space but moves backward relative to its forward moving body; and another where it is thrust rapidly forward to a new position. The fact that head-bobbing is abolished when pigeons walk on a treadmill suggests it is primarily a visual response rather than an equi-libratory response. Data are presented which show that stabilization during the ‘lock’ phase allows a small degree of slippage which is the probable source of error signals for compensatory head movements. The head-bobbing that appears to occur during landing is shown to be illusory.

Return eye movements, an ocular compensatory reflex in the alert cat and monkey

Eye movements induced by ampullary nerve stimulation in the alert cat and monkey are biphasic in nature. The eyes initially deviate from their original position in the orbit in directions detailed in previous studies. The initial deviations are generally interrupted or followed by active movements in the opposite direction. These opposing movements are the subject of this report. They have been designated “return eye movements” since they tend to return the eyes toward or past their initial position in the orbit. They are a central oculomotor reflex. This reflex serves to maintain the visual angle in space by opposing sudden unexpected shifts of the retina and projected visual field. It also appears to coordinate compensatory head and eye movements during impulses of angular acceleration. The ease of eliciting this ocular reflex in the cat and monkey suggests that it plays an important role in ocular compensation in these animals and probably in man as well.