Binocular Optokinetic Stimulation Research Articles

Cerebellar nodulectomy impairs spatial memory of vestibular and optokinetic stimulation in rabbits.

Natural vestibular and optokinetic stimulation were used to investigate the possible role of the cerebellar nodulus in the regulation and modification of reflexive eye movements in rabbits. The nodulus and folium 9d of the uvula were destroyed by surgical aspiration. Before and after nodulectomy the vertical and horizontal vestibuloocular reflexes (VVOR, HVOR) were measured during sinusoidal vestibular stimulation about the longitudinal (roll) and vertical (yaw) axes. Although the gain of the HVOR (G(HVOR) = peak eye movement velocity/peak head velocity) was not affected by the nodulectomy, the gain of the VVOR (G(VVOR)) was reduced. The gains of the vertical and horizontal optokinetic reflexes (G(VOKR), G(HOKR)) were measured during monocular, sinusoidal optokinetic stimulation (OKS) about the longitudinal and vertical axes. Following nodulectomy, there was no reduction in G(VOKR) or G(HOKR). Long-term binocular OKS was used to generate optokinetic afternystagmus, OKAN II, that lasts for hours. After OKAN II was induced, rabbits were subjected to static pitch and roll, to determine how the plane and velocity of OKAN II is influenced by a changing vestibular environment. During static pitch, OKAN II slow phase remained aligned with earth-horizontal. This was true for normal and nodulectomized rabbits. During static roll, OKAN II remained aligned with earth-horizontal in normal rabbits. During static roll in nodulectomized rabbits, OKAN II slow phase developed a centripetal vertical drift. We examined the suppression and recovery of G(VVOR) following exposure to conflicting vertical OKS for 10-30 min. This vestibular-optokinetic conflict reduced G(VVOR) in both normal and nodulectomized rabbits. The time course of recovery of G(VVOR) after conflicting OKS was the same before and after nodulectomy. In normal rabbits, the head pitch angle, at which peak OKAN II velocity occurred, corresponded to the head pitch angle maintained during long-term OKS. If the head was maintained in a "pitched-up" or "pitched-down" orientation during long-term OKS, the subsequently measured OKAN II peak velocity occurred at the same orientation. This was not true for nodulectomized rabbits, who had OKAN II peak velocities at head pitch angles independent of those maintained during long-term OKS. We conclude that the nodulus participates in the regulation of compensatory reflexive movements. The nodulus also influences "remembered" head position in space derived from previous optokinetic and vestibular stimulation.

Olivofloccular circuit in oculomotor control: binocular optokinetic stimulation

The metabolic activation of the olivocerebellar pathway during binocular optokinetic stimulation was studied in the guinea pig, by means of the semiquantitative 14C-2-deoxyglucose (2DG) technique. The experimental group underwent binocular horizontal stimulation, whereas the control animals were either kept in the dark or allowed to view a stationary pattern. The local metabolic activity index in the dorsal cap of the inferior olive was higher on the side contralateral to the eye that had been stimulated in the temporonasal (T-N) direction in the horizontal group; in contrast, the floccular region showed higher activity on the side ipsilateral to the T-N-stimulated eye. These findings support the involvement of the olivocerebellar pathway in the horizontal optokinetic response. A phylogenetic hypothesis is suggested to explain inconsistent results found in the literature.

Optokinetic and Vestibular Stimulation Determines the Spatial Orientation of Negative Optokinetic Afternystagmus in the Rabbit

Prolonged binocular optokinetic stimulation (OKS) in the rabbit induces a high-velocity negative optokinetic afternystagmus (OKAN II) that persists for several hours. We have taken advantage of this uniform nystagmus to study how changes in static head orientation in the pitch plane might influence the orientation of the nystagmus. After horizontal OKS, the rotation axis of the OKAN II remained almost constant in space as it was kept aligned with the gravity vector when the head was pitched by as much as 80 degrees up and 35 degrees down. Moreover, during reorientation, slow-phase eye velocity decreased according to the head pitch angle. Thereafter, we analyzed the space orientation of OKAN II after optokinetic stimulation during which the head and/or the OKS were pitched upward and downward. The rotation axis of OKAN II did not remain aligned with an earth vertical axis nor a head vertical axis, but it tended to be aligned with that of the OKS respace. The slow-phase eye velocity of OKAN II was also affected by the head pitch angle during OKS, because maximal OKAN II velocity occurred at the same head pitch angle as that during optokinetic stimulation. We suggest that OKAN II is coded in gravity-centered rather than in head-centered coordinates, but that this coordinate system may be influenced by optokinetic and vestibular stimulation. Moreover, the velocity attenuation of OKAN II seems to depend on the mismatch between the space-centered nystagmus rotation axis orientation and that of the "remembered" head-centered optokinetic pathway activated by OKS.

Optokinetically evoked expression of corticotropin-releasing factor in inferior olivary neurons of rabbits

We investigated the influence of both binocular and monocular optokinetic stimulation on the expression of corticotropin-releasing factor (CRF), a neuropeptide, in inferior olivary neurons. Rabbits were placed at the center of a cylindrical optokinetic drum that rotated at a constant velocity of 5 degrees/sec, stimulating one eye in the posterior-->anterior direction and the other eye in the anterior-->posterior direction. After 48 hr of optokinetic stimulation, rabbits were killed and the brains were prepared for immunohistochemistry. An antiserum to rat/human CRF was used to label brain-stem sections of optokinetically stimulated rabbits. The density of CRF-specific reaction product within individual olivary neurons was analyzed with a computer-based densitometer. Binocular optokinetic stimulation for 48 hr caused a 20-70% increase in the optical density of "stimulated" dorsal cap neurons, measured relative to the optical density of control ("unstimulated") olivary neurons in the same histological section. This elevated expression of CRF lasted approximately 48 hr. When a delay of 18 hr was interposed between optokinetic stimulation and death of the rabbit, during which the rabbits were deprived of pattern vision, then both dorsal caps were densely labeled. Monocular optokinetic stimulation for 48 hr in the anterior-->posterior direction caused no change in CRF expression in either dorsal cap if the rabbit was immediately killed. However, following monocular anterior-->posterior stimulation, the dorsal cap contralateral to the "null-stimulated" eye was densely labeled if the rabbit was deprived of pattern vision for 18 hr prior to death. We infer that stopping prolonged "null stimulation" causes a rebound in activity in the stimulated dorsal cap. This "rebound" must have its origin at the level of the dorsal cap or more peripherally in the optokinetic pathway.

Three-dimensional organization of optokinetic responses in the rabbit.

1. Three-dimensional rotations of both eyes were measured in alert rabbits during optokinetic stimulation about axes lying in the horizontal plane or about an earth-vertical axis, with either one or both eyes viewing the stimulus. Optokinetic stimulus speed was 2 degrees /s, either continuous or alternating in polarity (triangular stimulus). In addition to the gains of the responses, the orientations of the response axes relative to the stimulus axes were determined. 2. In comparison to the response to constant-speed optokinetic stimulation about the vertical axis, the response to constant-speed optokinetic stimulation about horizontal axes was characterized by the lack of a speed buildup. In many cases, slow phase tracking was good as long as the eye was within the central oculomotor range but deteriorated when eye deviation became more eccentric and fast phases failed to be generated. These features suggest that the optokinetic reflex about horizontal axes functions as a position-control system, rather than as a velocity-control system. 3. Binocular optokinetic stimulation at constant speed (2 degrees/s) about the roll axis (0 degrees azimuth horizontal axis) elicited disconjugate responses. Although the gain of the response was not significantly different in the two eyes (0.38 for downward and 0.44 for upward stimulation), the response axes of the two eyes differed by as much as 51 degrees. 4. Monocular, horizontal axis optokinetic stimulation at constant speed elicited responses that were grossly dissociated between the two eyes. The magnitude of the responses was anisotropic in that it varied with the azimuthal orientation of the stimulus axis; the maximum gain for each eye (0.41 for the seeing and 0.33 for the covered eye) was at 135 degrees azimuth for each eye. The axis orientation and direction (sense of rotation) of the optokinetic stimulus eliciting the maximal response for each eye coincided with the optic flow normally associated with the maximal excitation of the corresponding ipsilateral anterior canal. 5. Binocular, triangular optokinetic stimulation with small excursions (+/- 10 degrees), which avoided the saturation problems of constant-speed stimulation, elicited adequate responses without systematic directional asymmetries. Gain was approximately 0.9 for all stimulus axis orientations in the horizontal plane. 6. During monocular stimulation with triangular stimuli, the response of the seeing eye showed a gain of approximately 0.5 for all orientations of the stimulus axis. In contrast, the covered eye showed anisotropic responses, with a maximum gain of approximately 0.5 during stimulation of the seeing eye about its 45 degree axis.(ABSTRACT TRUNCATED AT 400 WORDS)

Unilateral cholinergic stimulation of the rabbit's cerebellar flocculus: asymmetric effects on optokinetic responses

In previous work, we have demonstrated an acceleration of the buildup of slow-phase velocity of optokinetic nystagmus (OKN) after bilateral floccular injection of the aselective cholinergic agonist carbachol (Tan and Collewijn 1991; Tan et al. 1992a). In the present study we investigated the effects of unilateral floccular injections of carbachol. Such unilateral injections specifically enhanced the buildup of OKN slow-phase velocity in the direction toward the injected flocculus (ipsiversive). During binocular optokinetic stimulation, this enhancement was expressed in the motion of both eyes. Acceleration of the eye contralateral to the injected flocculus increased from 1 to about 2 degrees/s2, while the acceleration of the ipsilateral eye increased from 1 to about 1.5 degrees/s2. In contrast, buildup of contraversive OKN was unchanged. No changes were found in the steady-state OKN and optokinetic afternystagmus (OKAN). Monocular optokinetic stimulation was only effective in the nasal direction, and the effects of unilateral injection of carbachol were disconjugate. Ipsiversive OKN was enhanced only in the contralateral, seeing eye, while the response of the ipsilateral, covered eye was unchanged. We hypothesize that the directionally specific effect of unilateral cholinergic floccular stimulation on OKN is due to enhancement of predominantly the excitatory phase of modulation of the Purkinje cell's simple-spike activity by carbachol, without a marked effect of carbachol on the inhibitory phase of simple-spike modulation.

Binocular interaction and signal components of optokinetic responses of climbing fiber afferents in the cerebellar flocculus and nodulus of the pigmented rabbit

Under anesthesia with N 2O (70%) and halothane (2–4%), Purkinje cells were extracellularly recorded in the flocculus and nodulus of immobilized pigmented rabbits, and complex spike responses to optokinetic stimulation (OKS) delivered simultaneously to both the ipsi- and contralateral eyes (binocular OKS) were compared with those to OKS monocularly delivered to the ipsi- or contralateral eye (monocular OKS). The complex spike responses to binocular OKS were an approximate summation of monocular responses to ipsiand contralateral OKS. The complex spike modulation did not correlate with rhythmical slow and quick nystagmic discharges of the oculomotor nerve evoked by horizontal OKS. This suggests that complex spike responses originate largely from ‘retinal slip’ signals rather than from ‘final motor command’ signals represented in the discharges of the oculomotor nerve.

Optokinetic stimulation increases corticotropin-releasing factor mRNA in inferior olivary neurons of rabbits

Stimulus-specific changes in levels of corticotropin-releasing factor (CRF) mRNA in inferior olivary neurons were studied in unanesthetized rabbits. The possible functional importance of CRF, a neuropeptide that is expressed in all inferior olivary neurons, in cerebellar synaptic transmission was investigated in a subpopulation of inferior olivary neurons, the caudal dorsal cap. Previous studies have shown that unidirectional, binocular optokinetic stimulation increases the level of discharge in neurons located in one of the caudal dorsal caps of the inferior olive and decreases the level of discharge in neurons in the opposite dorsal cap. We investigated the influence of prolonged (1-144 hr), unidirectional, binocular, optokinetic stimulus on the levels of CRF mRNA in dorsal cap neurons, measured with the technique of hybridization histochemistry. Rabbits were placed at the center of a cylindrical optokinetic drum that rotated at a constant velocity of 5 deg/sec, stimulating one eye in the posterior-to-anterior direction and the contralateral eye in the anterior-to-posterior direction. Posterior-to-anterior stimulation of the left eye evoked increased activity of inferior olivary neurons located in the right caudal dorsal cap. Conversely, anterior-to-posterior stimulation of the right eye evoked decreased activity of neurons in the left caudal dorsal cap. The levels of CRF mRNA in dorsal cap neurons that were activated by prolonged optokinetic stimulation were increased by a factor of 4 to 7 after 48 hr of stimulation and by more than a factor of 10 after 144 hr of optokinetic stimulation. These optokinetically induced increases in CRF mRNA decayed to background levels after 30 hr. Our observations implicate CRF in visual olivocerebellar function and suggest that CRF may play a role in the plastic control of eye movement mediated by the visual olivocerebellar system.

Responses of prepositus hypoglossi neurons to optokinetic and vestibular stimulations in the rat

The responses of 47 nucleus prepositus hypoglossi neurons to vestibular optokinetic stimulations in the horizontal plane were recorded in immobilized, pigmented rats. During sinusoidal vestibular stimulation in the dark, type II (62%) and type I (38%) responses were recorded. In addition to the sinusoidal modulation of firing rate, units often showed fast rhythmic increases or decreases in firing (nystagmic modulation). The mean phase of the response relative acceleration measured at 0.025 and 0.2 Hz were 19 and 84 deg., respectively. Some units (25%) showed larger phase-lags. The sensitivities of unit responses at 0.025 and 0.2 Hz were 1.6 and 0.5 spikes × s −1/deg × s −2, respectively. The responses of NPH neurons to binocular optokinetic stimulation were divided in 2 classes: (i) neurons with unidirectional responses (18%) were excited by stimuli moving towards the side of recording and showed no change in firing on oppositely directed stimulation; all of them showed a type II pattern during vestibular stimulation; (ii) bidirectional responses showed an increase in one direction and a decrease in firing for stimulation in the opposite direction. In every case the optokinetic responses were synergistic with the vestibular responses, which consisted of both type I and type II units. On the basis of the directionality of their optokinetic response, the value of their time constants and the shape of their velocity tuning curves, it is suggested that unidirectional type II NPH neurons could serve as relays in the optokinetic pathways between NRTP (or PT) and vestibular neurons. Some other neurons, having time constants particularly long and different for the rising and falling of the response, probably serve other functions.

Responses of units in the rat cerebellar flocculus during optokinetic and vestibular stimulation

The simple (SS) and complex spike (CS) responses of Purkinje (P-cells) and non-Purkinje (non P-cells) in the cerebellar flocculus were studied in alert pigmented rats (DA-HAN) during binocular and monocular optokinetic stimulation (OKS), vestibular stimulation and a combination of the two. Of a total of 98 P-cells whose SS discharges were activated by rotary stimulation of the horizontal canal in the dark (type I and type II P-cells), the vast majority (72%) responded to constant velocity binocular OKS that was produced by means of a horizontal shadow projector system. The remaining P-cells responded only to vestibular stimulation (19%), to OKS or to the presumed fast components of optokinetic and vestibular nystagmus (9%). The optokinetic responses of P-cells were generally bidirectional but asymmetrical, i.e., the increases in rate in one direction were larger in magnitude than decreases on opposite OKS and were synergistic with the semicircular canal input. During constant velocity OKS, the discharge of a few P-cells rose approximately exponentially, outlasted the stimulus by as much as 10-13.5s and, thus, resembled OKS responses of vestibular nucleus neurons. However, the majority exhibited a phasic-tonic response governed by a short "time constant" of from 0.5-3s. The velocity tuning curves of vestibular/OKS responding P-cells showed peak sensitivities with retinal slip velocities of 1.5-2 degrees/s. This is higher than the ca. 1 degree/s determined for other relay nuclei of the horizontal optokinetic pathway. The responses of non P-cells suggest that they originate from mossy fiber projections from vestibular, visual (optokinetic) and saccadic eye movement-related areas of the brainstem. Most of the units carried a combined vestibular and optokinetic signal. The majority showed a bidirection-selective response to OKS, and a small percentage showed unidirectional responses only. Monocular testing of P-cells revealed that most received a bidirection-selective, but asymmetrical, OKS input. Slightly more than half of these had a strongest OKS drive from the contralateral eye; the remaining units were driven most strongly by the ipsilateral eye. Unidirection-selective P-cells, driven by OKS to the ipsi- or contralateral eye, were uncommon; yet this class is common among other portions of the horizontal optokinetic system (e.g., vestibular nuclei, praepositus hypoglossi nucleus, nucleus reticularis tegmenti pontis).(ABSTRACT TRUNCATED AT 400 WORDS)

Optokinetic visual detection in the rat visual centres. A [14C]-2-deoxy-D-glucose study.

Following forty-five min of binocular optokinetic stimulation (OKS) the autoradiographic maps of [14C]-2-deoxy-D-glucose (2DG) assumption of Long-Evans brain reveal clearly different patterns of optical density within visual centres. The most superficial layers of superior colliculus (SC) and a pretectal area including the nucleus of the optic tract (NOT) appear symmetrically, strongly darker than other visual structures such as lateral geniculate nucleus (LGN) and visual cortex (VC). Whereas the lack of metabolic increase at LGN and VC levels entirely confirms the non-involvement of the geniculo-cortical path in mediating the optomotor response following OKS in Rodents, it is postulated that the symmetrical increase of 2DG uptake even upon unidirectional OKS found even at pretectal level may represent a commissural transfer of visual information between homologous pretectal areas like the nuclei of the optic tract.