Kevin J. Quinn

The latency of the cat vestibulo-ocular reflex before and after short- and long-term adaptation

Latencies of normal and adapted feline vestibulo-ocular reflex (VOR) were studied in five cats by applying ± 20°/s horizontal head velocity steps (4000°/s2 acceleration) and measuring the elicited horizontal or vertical reflex eye responses. Normal VOR latency was 13.0 ms ± 1.9 SD. Short-term adaptation was then accomplished by using 2 h of paired horizontal sinusoidal vestibular stimulation and phase-synchronized vertical optokinetic stimulation (cross-axis adaptation). For long-term adaptation, cats wore ×0.25 or ×2.2 magnifying lenses for 4 days. The cats were passively rotated for 2 h/day and allowed to walk freely in the laboratory or their cages for the remainder of the time. The latency of the early (primary) adaptive response was 15.2ms±5.2 SD for crossaxis adaptation and 12.5 ms±3.9 SD for lens adaptation. This short-latency response appeared within 30 min after beginning the adaptation procedure and diminished in magnitude overnight. A late (secondary) adaptive response with latency of 76.8 ms±7.0 SD for cross-axis adaptation and 68.1 ms±8.8 SD for lens adaptation appeared after approximately 2 h of adaptation. It had a more gradual increase in magnitude than the primary response and did not diminish in magnitude overnight. These data suggest that brainstem VOR pathways are a site of learning for adaptive VOR modification, since the primary latency is short and has a similar latency to that of the normal VOR.

Frequency dependence of cat vestibulo-ocular reflex direction adaptation: Single frequency and multifrequency rotations

Vertical and horizontal vestibulo-ocular reflex (VOR) eye movements were recorded in alert cats during horizontal rotation in total darkness before and after a 2 h vestibulo-ocular reflex direction adaptation procedure. Adaptation stimuli were whole body horizontal vestibular rotation coupled to synchronous vertical optokinetic motion. The waveform of the adaptation stimuli was either a sinusoid at 0.05, 0.1, 0.25, 0.5, or 1 Hz, or a sum of sinusoids containing 0.2, 0.3, 0.5, 0.7, 1.1, and 1.7 Hz. Exposure to single frequency stimuli produced adaptive vertical VOR with a gain that was greatest near the training frequency; adaptive VOR phases were advanced below, accurate at, and lagged above the training frequency. Exposure to the multifrequency waveform produced a uniform modest increase in gain across frequencies, with accurate adaptive VOR phase.

Eyeball retraction latency in the conscious rabbit measured with a new photodiode technique

A new technique is described for accurate, reliable measurement of eyeball retraction in the rabbit. A narrow film strip, on which a linear light intensity grating has been exposed, is attached to a contact lens which is placed on the animals cornea. The other end of the intensity grating slides between a photodiode and an LED. The contact lens-film grating assembly moves freely with eyeball retraction and relaxation, causing changes in photodiode output. This device appears to be well tolerated by the animal. Large amplitude eyeball retractions occur in response to air puff stimulation directed at the upper or lower eyelid and to periorbital shock. Average eye retraction latency to stimulation of the abducens (VI) nerve with a chronically implanted stimulating electrode was 5.3 ms (S.D. = 0.75 ms) in the conscious rabbit as measured with our device. Latency to periorbital electrical shock was 9.3 ms (S.D. = 2.1 ms). Eye retraction latency decreased with increasing shock amplitudes. Rabbits readily acquired classically conditioned eyeball retractions, monitored with this device, when a white noise auditory stimulus was paired with an air puff directed at the eyelid.

Simulation of adaptive mechanisms in the vestibulo-ocular reflex

The vestibulo-ocular reflex (VOR), which stabilizes the eyes in space during head movements, can undergo adaptive modification to maintain retinal stability in response to natural or experimental challenges. A number of models and neural sites have been proposed to account for this adaptation but these do not fully explain how the nervous system can detect and correct errors in both gain and phase of the VOR. This paper presents a general error correction algorithm based on the multiplicative combination of three signals (retinal slip velocity, head position, head velocity) directly relevant to processing of the VOR. The algorithm is highly specific, requiring the combination of particular sets of signals to achieve compensation. It is robust, with essentially perfect compensation observed for all gain (0.25X–4.0X) and phase (-180°–+180°) errors tested. Output of the model closely resembles behavioral data from both gain and phase adaptation experiments in a variety of species. Imposing physiological constraints (no negative activation levels or changes in the sign of unit weights) does not alter the effectiveness of the algorithm. These results suggest that the mechanisms implemented in our model correspond to those implemented in the brain of the behaving organism. Predictions concerning the nature of the adaptive process are specific enough to permit experimental verification using electrophysiological techniques. In addition, the model provides a strategy for adaptive control of any first order mechanical system.

Modeling learning in brain stem and cerebellar sites responsible for VOR plasticity

A simple model of vestibuloocular reflex (VOR) function was used to analyze several hypotheses currently held concerning the characteristics of VOR plasticity. The network included a direct vestibular pathway and an indirect path via the cerebellum. An optimization analysis of this model suggests that regulation of brain stem sites is critical for the proper modification of VOR gain. A more physiologically plausible learning rule was also applied to this network. Analysis of these simulation results suggests that the preferred error correction signal controlling gain modification of the VOR is the direct output of the accessory optic system (AOS) to the vestibular nuclei vs. a signal relayed through the cerebellum via floccular Purkinje cells. The potential anatomical and physiological basis for this conclusion is discussed, in relation to our current understanding of the latency of the adapted VOR response.

Preferred axis of rotation of floccular Purkinje cells in the decerebrate cat

Responses of 35 Purkinje cells in decerebrate cats were recorded during 0.5 Hz rotations in 4-11 vertical planes and the horizontal plane to determine their semicircular canal input. Most neurons received convergent input from two canals (21 neurons) or 3 canals (5 neurons). Few Purkinje cells were maximally sensitive to rotations about an axis appropriate to their inferior olivary input as determined by Gerrits and Voogd [15,24,27,49].

Chronic recording of the vestibulo-ocular reflex in the restrained rat using a permanently implanted scleral search coil

A technique is described which allows accurate long-term monitoring of eye movements in the rat using permanently implanted scleral search coils. Search coils permanently sutured around the sclera yield vestibulo-ocular reflex (VOR) gain and phase values which are comparable to those reported previously in the literature using acutely implanted coils or electrooculographic electrodes. Considerations related to strain, sex and surgical procedures which permit measurement of responses in the chronically restrained rat are described. VOR gain and phase show a time course to their recovery following the implant surgery, with asymptotic performance typically attained approximately 10 days post-surgically. This technique, with the ability to monitor eye movements over weeks to months, appears ideal for development of rodent models of reflex adaptation which require observation of reflex behavior over extended periods of time. Development of a chronic procedure for monitoring eye movement in rodents is especially important given their initial response to restraint (extensive struggling). Finally, adaptation of this technique to smaller species (e.g., mouse) appears technically feasible which should permit the application of transgenic and knockout techniques to the determination of various vestibular reflex functions requiring long-term monitoring.

Vestibuloocular reflex arc analysis using an experimentally constrained neural network

The primary function of the vestibuloocular reflex (VOR) is to maintain the stability of retinal images during head movements. This function is expressed through a complex array of dynamic and adaptive characteristics whose essential physiological basis is a disynaptic arc. We present a model of normal VOR function using a simple neural network architecture constrained by the physiological and anatomical characteristics of this disynaptic reflex arc. When tuned using a method of global optimization, this network is capable of exhibiting the broadband response characteristics observed in behavioral tests of VOR function. Examination of the internal units in the network show that this performance is achieved by rediscovering the solution to VOR processing first proposed by Skavenski and Robinson (1973). Type I units at the intermediate level of the network possess activation characteristics associated with either pure position or pure velocity. When the network is made more complex either through adding more pairs of internal units or an additional level of units, the characteristic division of unit activation properties into position and velocity types remains unchanged. Although simple in nature, the results of our simulations reinforce the validity of bottom-up approaches to modeling of neutral function. In addition, the architecture of the network is consistent with current ideas on the characteristics and site of adaptation of the reflex and should be compatible with current theories regarding learning rules for synaptic modification during VOR adaptation.

Changes in sensitivity of vestibular nucleus neurons induced by cross-axis adaptation of the vestibulo-ocular reflex in the cat

In alert, chronically-prepared cats, we studied response characteristics of well-isolated vestibular nucleus neurons (n = 9) while pairing yaw rotation with a pitch optokinetic stimulus, resulting in cross-axis adaptation of the horizontal vestibulo-ocular reflex. Each neurons sensitivity to whole body rotation in a variety of axes in three-dimensional space was determined. When tested in darkness following adaptation, neurons showed statistically significant increases in sensitivity to yaw but not vertical plane rotations, suggesting participation in reflex plasticity.

Processing of spatial information by floccular and non-floccular target neurons in the alert cat

In five alert chronically-prepared cats we studied the response to sinusoidal 3-D whole body rotation of well-isolated vestibular nucleus neurons which were tested for monosynaptic input from the vestibular labyrinth, direct projection to the oculomotor nucleus and, in some cases, inhibition from cerebellar flocculus stimulation. Neurons directly inhibited by flocculus stimulation had significantly greater horizontal-vertical semicircular canal signal convergence than did neurons not inhibited by flocculus stimulation.