Otolith-visual interaction in the control of eye movement produced by sinusoidal vertical linear acceleration in alert cats

Summary 1. Eye movement responses were examined in alert cats during sinusoidal vertical linear acceleration. Stimulus frequencies of 0.20–0.85 Hz with a constant amplitude of 10.5 cm (corresponding to 0.02–0.31 g) were used. A random visual pattern was presented to give sinusoidal vertical optokinetic stimuli of similar amplitude and frequency to the up-down motion of the cat. 2. Sinusoidal linear acceleration in the presence of a stationary visual pattern produced robust eye movement responses with near compensatory phase at all stimulus frequencies tested. With both eyes covered, a vertical linear vestibulo-ocular reflex (LVOR) was frequently produced at a stimulus strength corresponding to 0.04–0.31 g. The evoked LVOR was always small, and the overall mean response phase values advanced by as much as 70 ° at frequencies below 0.56 Hz, indicating that the otolith signals activated by sinusoidal linear acceleration were not, by themselves, converted into compensatory eye position signals under these experimental conditions. 3. Optokinetic stimulation alone produced more lag of response phase as stimulus frequency increased, and the gain of evoked eye movement responses was smaller at higher stimulus frequencies compared to the gain during linear acceleration in the light. Bilateral labyrinthectomies resulted in a significant change of the eye movement responses during linear acceleration when visual inputs were allowed: there was more phase lag at higher stimulus frequencies and a decreased gain at all frequencies tested. These results indicate that the interaction of otolith and visual inputs produces robust eye movement responses with near compensatory phase during sinusoidal linear acceleration in the light.     

The interstitial nucleus of Cajal in the midbrain reticular formation and vertical eye movement.

Bilateral lesions of the midbrain reticular formation within, and in the close vicinity of, the interstitial nucleus of Cajal (INC) result in the severe impairment of the ability to hold eccentric vertical eye position after saccades, phase advance and decreased gain of the vestibulo-ocular reflex (VOR) induced by sinusoidal vertical rotation. In addition, the INC region of alert animals contains many burst-tonic and tonic neurons whose activity is closely correlated with vertical eye movement, not only during spontaneous saccades, but also during the VOR, smooth pursuit and optokinetic eye movements. Although their activity is closely related to these conjugate vertical eye movements, it is different from the oculomotor motor neuron activity. These results indicate that the INC region is involved in, and indispensable for, some aspects of eye position generation during vertical eye movement. Further comparison of INC neuron discharge with eye movements during two special conditions indicates that the INC region alone cannot produce eye position signals. First INC neuron discharge shows no response or an 80 degrees phase advance (close to the expected value if there is no integration) in the dark compared to the light during sinusoidal vertical linear acceleration in alert cats. Second, during rapid-eye-movement (REM) sleep, the discharge of INC neurons is no longer correlated with eye position. These results imply that the INC is not the entire velocity-to-position integrator, but that it has to work with other region(s) to perform the integration. A close functional linkage has been described between vertical-eye-movement-related neurons in the INC region and vestibulo-ocular relay neurons related to the vertical semicircular canals in the vestibular nuclei. It has been suggested that both are the major constituents of the common neural integrator circuits for vertical eye movements.     

Latencies of response of eye movement-related neurons in the region of the interstitial nucleus of Cajal to electrical stimulation of the vestibular nerve in alert cats

Summary Recent studies have shown that the interstitial nucleus of Cajal (INC) in the midbrain reticular formation is involved in the conversion of vertical semicircular canal signals into eye position during vertical vestibuloocular reflexes. Secondary vestibulo-ocular relay neurons related to the vertical canals, which constitute the majority of output neurons sending signals from the vestibular nuclei directly to the oculomotor nuclei, have been shown to project axon collaterals to the region within and near the INC. To understand how the INC is involved in the signal conversion, latencies of response of neurons in the INC region to electrical stimulaton of the vestibular nerve were examined in alert cats. The responses of 96 cells whose activity was clearly modulated by sinusoidal pitch rotation (at 0.31 Hz) were analyzed. These included 41 cells whose activity was closely correlated with vertical eye movement (38 burst-tonic and 3 tonic neurons), and 55 other cells (called pitch cells as previously). Twenty nine of the 96 cells (30%) were activated at disynaptic latencies following single shock stimulation of the contralateral vestibular nerve. Disynaptically activated cells were significantly more frequent for pitch cells than for eye movement-related cells (25/55 = 45% vs 4/41 = 10%; p < 0.001, Chi-square test). Conversely, cells that did not receive short-latency activation (< 6 ms) were more frequent among eye movement-related cells than pitch cells (26/41 = 63% vs 13/55 = 24%; p < 0.001, Chi-square test). Pitch cells showed significantly less phase lag (re head acceleration) than eye movement-related cells during sinusoidal pitch rotation (mean ± SD 124° ± 17° vs 138° ± 14°. p < 0.01, t-test). These results suggest that 1) cells in the INC region other than burst-tonic and tonic neurons mainly receive direct inputs from secondary vestibulo-ocular relay neurons, and that 2) vertical canal signals reach eye movement-related neurons mainly polysynaptically.     

Human eye movement response to z-axis linear acceleration: the effect of varying the phase relationships between visual and vestibular inputs

We investigated the effect of systematically varying the phase relationship between 0.5-Hz sinusoidal z-axis optokinetic (OKN) and linear acceleration stimuli upon the resulting vertical eye movement responses of five humans. Subjects lay supine on a linear sled which accelerated them sinusoidally along their z-axis at 0.4 g peak acceleration (peak velocity 1.25 m/s). A high-contrast, striped z-axis OKN stimulus moving sinusoidally at 0.5 Hz, 70°/s peak velocity was presented either concurrently or with the acceleration stimulus or alone. Subjects' vertical eye movements were recorded using scleral search coils. When stimuli were paired in the naturally occurring relationship (e.g., visual stripes moving upward paired with downward physical acceleration), the response was enhanced over the response to the visual stimulus presented alone. When the stimuli were opposed (e.g., visual stripes moving upward during upward physical acceleration, a combination that does not occur naturally), the response was not significantly different from the response to the visual stimulus presented alone. Enhancement was maximized when the velocities of the visual and motion stimuli were in their normal phase relationship, while the response took intermediate values for other phase relationships. The phase of the response depended upon the phase difference between the two inputs. We suggest that linear self-motion processing looks at agreement between the two stimuli — a sensory conflict model.     

Functional coupling of the stabilizing eye and head reflexes during horizontal and vertical linear motion in the cat

Summary The otolith contribution and otolith-visual interaction in eye and head stabilization were investigated in alert cats submitted to sinusoidal linear accelerations in three defined directions of space: up-down (Z motion), left-right (Y motion), and forward-back (X motion). Otolith stimulation alone was performed in total darkness with stimulus frequency varying from 0.05 to 1.39 Hz at a constant half peak-to-peak amplitude of 0.145 m (corresponding acceleration range 0.0014–1.13 g) Optokinetic stimuli were provided by sinusoidally moving a pseudorandom visual pattern in the Z and Y directions, using a similar half peak-to-peak amplitude (0.145 m, i.e., 16.1°) in the 0.025–1.39 Hz frequency domain (corresponding velocity range 2.5°–141°/s). Congruent otolith-visual interaction (costimulation, CS) was produced by moving the cat in front of the earth-stationary visual pattern, while conflicting interaction was obtained by suppressing all visual motion cues during linear motion (visual stabilization method, VS, with cat and visual pattern moving together, in phase). Electromyographic (EMG) activity of antagonist neck extensor (splenius capitis) and flexor (longus capitis) muscles as well as horizontal and vertical eye movements (electrooculography, EOG) were recorded in these different experimental conditions. Results showed that otolith-neck (ONR) and otolith-ocular (OOR) responses were produced during pure otolith stimulation with relatively weak stimuli (0.036 g) in all directions tested. Both EMG and EOG response gain slightly increased, while response phase lead decreased (with respect to stimulus velocity) as stimulus frequency increased in the range 0.25–1.39 Hz. Otolith contribution to compensatory eye and neck responses increased with stimulus frequency, leading to EMG and EOG responses, which oppose the imposed displacement more and more. But the otolith system alone remained unable to produce perfect compensatory responses, even at the highest frequency tested. In contrast, optokinetic stimuli in the Z and Y directions evoked consistent and compensatory eye movement responses (OKR) in a lower frequency range (0.025–0.25 Hz). Increasing stimulus frequency induced strong gain reduction and phase lag. Oculo-neck coupling or eye-head synergy was found during optokinetic stimulation in the Z and Y directions. It was characterized by bilateral activation of neck extensors and flexors during upward and downward eye movements, respectively, and by ipsilateral activation of neck muscles during horizontal eye movements. These visually-induced neck responses seemed related to eye velocity signals. Dynamic properties of neck and eye responses were significantly improved when both inputs were combined (CS). Near perfect compensatory eye movement and neck muscle responses closely related to stimulus velocity were observed over all frequencies tested, in the three directions defined. The present study indicates that eye-head coordination processes during linear motion are mainly dependent on the visual system at low frequencies (below 0.25 Hz), with close functional coupling of OKR and eye-head synergy. The otolith system basically works at higher stimulus frequencies and triggers Synergist OOR and ONR. However, both sensorimotor subsystems combine their dynamic properties to provide better eyehead coordination in an extended frequency range and, as evidenced under VS condition, visual and otolith inputs also contribute to eye and neck responses at high and low frequency, respectively. These general laws on functional coupling of the eye and head stabilizing reflexes during linear motion are valid in the three directions tested, even though the relative weight of visual and otolith inputs may vary according to motion direction and/or kinematics.     

Carbachol effects on hippocampal neurons in vitro: dependence on the rate of rise of carbachol tissue concentration

Summary Extracellular activity from vestibular nuclei neurons and vertical eye movements were recorded in the alert cat during sinusoidal optokinetic stimulation in the vertical plane at frequencies varying from 0.0125 Hz to 0.75 Hz. Among a population of 96 vestibular units located in and around Deiters' nucleus, 73 neurons (76%) displayed a firing rate modulation which followed the input at the standard parameters of visual stimulation (0.05 Hz; 10.1 deg/s or 9.1 cm/s peak to peak velocity). Two different patterns of modulation were found. In 42 cells (57%) an increase in the firing rate was observed during motion of the visual scene in the downward direction, while 31 neurons (43%) showed the opposite behavior, with an enhanced firing rate during upward movement. The phase of the neuronal responses was close (± 45°) to the velocity peaks (+90°: downward and -90°: upward) of visual scene motion for 65 among the 73 neurons. Mean values of phase was-6.1 ± 19.5° (SD) and -3.2 ± 15.5° (SD) with respect to the +90° and -90° velocity peaks, respectively. In the frequency range 0.0125–0.75 Hz, the phase of the neuronal responses remained almost stable, with only a slight lag which reaches -22° at the 0.25 Hz visual stimulation. The firing rate modulation was found to be predominant at low frequencies (0.0125 Hz–0.25 Hz), with three distinct peaks of modulation occurring either at 0.025 Hz, 0.10 Hz or 0.25 Hz, depending on the recorded cells. Above 0.5 Hz, the cell modulation was very poorly developed or even absent. A gain attenuation was observed in all units, which was more important in cells showing a peak of modulation at 0.025 Hz as compared with the others (-20.7 dB vs -9.6 dB, respectively, in the 0.025 Hz–0.25 Hz decade). The gain of the optokinetic reflex (OKR) progressively decreased from mean values of 0.78 ± 0.15 to 0.05 ± 0.06 in the 0.025 Hz–0.5 Hz frequency range. A close correlation was observed between the OKR slow phase velocity and the modulation of the neuronal responses in the two cell populations with maximal modulations at 0.10 Hz or 0.25 Hz. No correlations were noticed in the third population characterized by a peak of modulation at 0.025 Hz. In all units, the phase of eye movement velocity and of neuronal responses were both related to the velocity of the visual surround motion. These correlations were also found when varying the amplitude of the visual stimulation at a fixed frequency. Saturation was observed in the unit responses at velocities above 68.5°/s. When considering both the gain attenuation in the frequency range and the correlation between firing rate modulation and OKR slow phase velocity, two rather different cell populations can be distinguished: one with neurons peaking at 0.025 Hz (strong gain attenuation; no correlation with OKR velocity) and one with neurons peaking at 0.10 Hz or 0.25 Hz (slight gain attenuation; correlation with OKR velocity). This study points to the influence of visual motion cues on vestibular nuclei unit activity in the low-frequency range. A velocity coding of visual — surround motion in the vertical plane is performed by vestibular neurons. Our results in the alert cat suggest that both retinal (retinal slip) and extraretinal (proprioceptive afferences from eye muscles, efference copy) inputs can be involved in this visually induced modulation of vestibular nuclei neurons.     

Spatial properties of vertical eye movement-related neurons in the region of the interstitial nucleus of Cajal in awake cats

Summary 1. Maximal activation directions of vertical burst-tonic and tonic neurons in the region of the interstitial nucleus of Cajal (INC) were examined in alert cats during vertical vestibulo-ocular reflex induced by sinusoidal rotation (at 0.11 Hz±10 deg, or 0.31 Hz±5 deg) in a variety of vertical planes using a null point analysis. The results were compared with the angles of anatomical and functional planes of vertical canals reported by Blanks et al. (1972) and Robinson (1982), and with the angles of vertical eye muscles measured in this study and by Ezure and Graf (1984). 2. Maximal activation directions of 23 cells (21 burst-tonic and 2 tonic neurons) were determined from their responses during rotation in 4 or more different vertical planes. All cells showed sinusoidal gain curves and virtually constant phase values except near the null regions, suggesting that their responses were evoked primarily by canal inputs. Phase values of 5 cells near the null regions depended on the rotation plane, suggesting additional otolith inputs. We used a measurement error range of ±10 deg for calculating the maximal activation directions from the null regions of individual cells and the values of error ranges of null calculation. Of the 23, the maximal activation directions of 7 cells were outside the measurement error ranges of vertical eye muscle angles and within the ranges of vertical canal angles (class A), those of 5 cells were within the ranges of eye muscle angles and outside the ranges of vertical canal angles (class B), and those of the remaining 11 cells were in the overlapping ranges for both angles (class C). Even if only the cells in which 5 or more measurement points were taken to determine maximal activation directions (n = 15), the results were similar. During vertical rotation with the head orientation +60 deg off the pitch plane, dissociation of cell activity and vertical compensatory eye movement was observed in 5 cells in class A or C that had null angles near +45 deg. These results suggest that the cells in class A and B carried individual vertical canal and oculomotor signals, respectively, although it is difficult to tell for the majority of cells (class C) which signals they reflected. Some cells in class A and C were antidromically activated from the medial longitudinal fasciculus at the level of abducens nucleus, suggesting that the signals carried by these cells may be sent to the lower brainstem. 3. Most burst-tonic neurons did not respond to horizontal rotation; significant responses were obtained in only 3 of 10 cells tested for which the gain was only 14–17% of their maximal vertical gain. There was no clear difference in gain or phase values of the responses to vertical rotation, or in eye position sensitivity (during spontaneous saccades) between cells whose responses coincided with individual vertical canal angles and those matching the angles of vertical recti muscles. The values of phase lag (re head acceleration during pitch rotation) and eye position sensitivity of these cells are still smaller compared to those of extraocular motoneurons reported by Delgado-Garcia et al. (1986), although they were larger than those of secondary vestibulo-ocular neurons (Perlmutter et al. 1988). All these results suggest that the signals carried by burst-tonic and tonic neurons in the INC region are different from oculomotor signals. 4. Similar analysis was done for comparison for 19 other cells that did not show close correlation with spontaneous eye movement but whose activity was clearly modulated by pitch rotation (pitch cells). More than a half (10/19) had maximal activation directions outside the measurement error ranges of individual vertical canal angles, and many shifted towards roll. Horizontal rotation produced responses with higher gain than burst-tonic neurons, suggesting a difference in the spatial response properties of burst-tonic and tonic neurons on one hand and pitch cells on the other.     

Activity of eye-movement-related neurons in the region of the interstitial nucleus of Cajal during sleep

Activity of vertical burst-tonic neurons in the region of the interstitial nucleus of Cajal (INC) in cats that showed a close correlation with spontaneous vertical eye movement during the waking state was compared to that during sleep. All the cells tested maintained high and regular discharge rates similar to those during the waking state when the eye was near the primary position. However, a significant correlation between tonic discharge rates and vertical eye position change seen during the waking state was lost during slow drifting eye movement during sleep, indicating that they are not involved in such eye movement. Upward (or downward) burst-tonic neurons showed bursts (or decreased activity) during upward rapid-eye movements (REMs) accompanied by failure of eye position holding with almost exponential decay during REM sleep. However, the increased (or decreased) activity was not maintained and quickly returned to near-previous discharge rates. Despite the fact that a significant positive correlation was seen between average discharge rates during vertical saccades and tonic rates after saccades for these neurons during the waking state, the same cells lost such a correlation during vertical REMs with eye position holding failure. The close correlation between presence or absence of tonic activity related to preceding bursts of burst-tonic neurons, on the one hand, and holding or failure of vertical eye position after vertical saccades or REMs, on the other, suggests that these neurons receive excitatory and inhibitory burst inputs, and also that they are involved in some aspect of vertical eye position generation, but that the INC region alone cannot convert the burst signals into eye position.     

Vertical eye movement-related type II neurons with downward on-directions in the vestibular nucleus in alert cats

The vestibular nuclei and the interstitial nucleus of Cajal (INC) have been regarded as key elements of the velocity-to-position integrator for vertical eye movements. This paper reports a class of type II vestibular neurons that receives input from the INC and carries vertical eye movement signals that appear to represent an intermediate stage of the integration process. Extracellular recordings were made from neurons in and near the vestibular nuclei in alert cats. We encountered 39 neurons that exhibited an intense burst of spikes for downward saccades and a position-related tonic activity during intersaccadic intervals (d-type II neurons). They had a very high saccadic sensitivity (4.3±2.7 spikes/deg, mean ± SD) as well as a high position sensitivity (3.2±1.6 (spikes/sec)/deg). Unlike the bursts of motoneurons, the bursts of these neurons declined gradually with an exponential-like time course and lasted well beyond the end of saccades. The mean time constant of the burst decay was 139±43 ms. The d-type II neurons were excited with disynaptic or trisynaptic latencies following stimulation of the contralateral vestibular nerve. The responses to vertical head rotations suggested inputs from the contralateral posterior canal. The d-type II neurons were excited with short latencies following stimulation of the ipsilateral INC, suggesting that they receive a direct excitatory input from vertical eye movement-related INC neurons with downward on-directions. The d-type II neurons were located in the rostral portion of the vestibular nuclei and the underlying reticular formation. These results suggest that d-type II neurons may be interposed between the burst-tonic neurons in the INC and pure tonic neurons in the vestibular nuclei and contribute to the oculomotor velocity-to-position integration.     

A comparison of the horizontal and vertical optokinetic reflexes of the rabbit

Summary The horizontal and vertical monocular optokinetic reflexes of the rabbit were measured under closed-loop and open-loop conditions. A random noise, optokinetic stimulus subtending 70×70 deg was presented to the left eye of rabbits placed in front of a rear projection tangent screen. The position of the right eye (nonstimulated) was measured using an infrared light projection technique. During open-loop optokinetic stimulation the eye position signal was fed back to sum with a time-integrated velocity command signal driving the optokinetic stimulus. The dynamics of eye movements evoked by horizontal and vertical optokinetic stimulation were different. Horizontally evoked eye movements never exceeded a deviation of 15 deg before being interrupted by resetting saccades, which returned the eye past the primary position. By contrast, vertical eye deviations greater than 20 deg were often maintained for intervals exceeding 10 s without resetting. The closed-loop gain of optokinetically evoked horizontal eye movements was higher for monocular posterior-anterior optokinetic stimulation than for anterior-posterior stimulation. The vertical optokinetic gain for up-down stimulation was slightly greater than the gain for down-up stimulation. The vertical up-down, open-loop optokinetic gain was greater than the down-up gain over a range of retinal slip velocities of 0.5–5.0 deg/s. Measurement of the horizontal vestibulo-ocular reflex during simultaneous horizontal optokinetic stimulation demonstrated that visual and vestibular information combine linearly to produce reflex eye movements. These data suggest that the higher gain of the horizontal optokinetic reflex may compensate in part for the reduced gain of the horizontal vestibulo-ocular reflex at lower angular accelerations of the head. An equivalent vertical optokinetic gain would be obviated by the contribution of the utricular otoliths to the vertical vestibulo-ocular reflex at low frequencies of head movement.This research was supported by the National Institutes of Health Grant EY00848 and the Oregon Lions Sight and Hearing Foundation     

Eye movements during combined pursuit, optokinetic and vestibular stimulation in macaque monkey

 During natural behaviour in a visual environment, smooth pursuit eye movements (SP) usually override the vestibular-ocular reflex (VOR) and the optokinetic reflex (OKR), which stem from head-in-space and scene-relative-to-eye motion, respectively. We investigated the interaction of SP, VOR, and OKR, which is not fully understood to date. Eye movements were recorded in two macaque monkeys while applying various combinations of smooth eye pursuit, vestibular and optokinetic stimuli (sinusoidal horizontal rotations of visual target, chair and optokinetic pattern, respectively, at 0.025, 0.05, 0.1, 0.2, 0.4, and 0.8 Hz, corresponding to peak stimulus velocities of 1.25–40°/s for a standard stimulus of ±8°). Slow eye responses were analysed in terms of gain and phase. During SP at mid-frequencies, the eyes were almost perfectly on target (gain 0.98 at 0.1 Hz), independently of a concurrent vestibular or optokinetic stimulus. Pursuit gain at lower frequencies, although being almost ideal (0.98 at 0.025 Hz with pursuit-only stimulation), became modified by the optokinetic input (gain increase above unity when optokinetic stimulus had the same direction as target, decrease with opposite direction). At higher stimulus frequencies, pursuit gain decreased (down to 0.69 at 0.8 Hz), and the pursuit response became modified by vestibular input (gain increase during functionally synergistic combinations, decrease in antagonistic combinations).Thus, the pursuit system in monkey dominates during SP-OKR-VOR interaction, but it does so effectively only in the mid-frequency range. The results can be described in the form of a simple dynamic model in which it is assumed that the three systems interact by linear summation. In the model SP and OKR dominate VOR in the low- to mid-frequency/velocity range, because they represent closed loop systems with high internal gain values (>>1) at these frequencies/velocities, whereas the VOR represents an open loop system with about unity-gain (up to very high frequencies). SP dominance over OKR is obtained by allowing an ’attentional/volitional’ mechanism to boost SP gain and a predictive mechanism to improve its dynamics. Received: 27 November 1998 / Accepted: 8 March 1999     

Neuronal activity related to vertical eye movement in the region of the interstitial nucleus of Cajal in alert cats

Summary (1) Discharge characteristics of neurons in the region of the interstitial nucleus of Cajal (INC) were studied in alert cats during spontaneous or visually induced eye movement and sinusoidal vertical (pitch) rotation. Activity of a majority of cells (n = 68) was closely related to vertical eye position with or without bursting activity during on-direction saccades. They were called vertical burst-tonic (n = 62) and tonic (n = 6) neurons. Mean discharge rates for individual cells when the eye was near the primary position ranged from 35 to 133 (mean 75) spikes/s with a coefficient of variation (CV) ranging from 0.04 to 0.29 (mean 0.15). Average rate position curves were linear for the great majority of these cells with a mean slope of 3.9 ± 1.2 SD spikes/s/deg. (2) The burst index was defined as the difference in discharge rate between maximal rate during an on-direction saccade and the tonic rate after the saccade. The values of mean burst index for individual cells ranged from 8 to 352 (mean 135) spikes/s. Tonic neurons had a burst index lower than 60 spikes/s and were distributed in the lower end of the continuous histogram, suggesting that burst-tonic and tonic neurons may be a continuous group with varying degrees of burst components. During off-direction saccades, a pause was not always observed, although discharge rate consistently decreased and pauses were seen when saccades were made further in the off-direction toward recruitment thresholds. Significant positive correlation was observed between average discharge rate during off- as well as on-direction saccades and tonic discharge rate after saccades for individual cells, which was not due to cats making saccades mainly from the primary position. (3) During pitch rotation at 0.11 Hz (±10 deg), burst-tonic and tonic neurons had mean phase lag and gain of 128 (±13 SD) deg and 4.2 (±1.7 SD) spikes/s/deg/s² relative to head acceleration. During pitch rotation of a wide frequency range (0.044–0.495 Hz), the values of phase lag were mostly constant (120–140 deg), while simultaneously recorded vertical VOR showed the mean phase lag of 178 deg. Vertical eye position sensitivity and pitch gain (re head position) showed significant positive correlation. (4) Comparison of the discharge characteristics of vertical burst-tonic and tonic neurons with those of secondary vestibulo-ocular neurons (Perlmutter et al. 1988) and extraocular motoneurons (Delgado-Garcia et al. 1986) in alert cats suggests that signals carried by burst-tonic and tonic neurons are partially processed signals in vertical VOR and saccades, and different from oculomotor signals. (5) The INC region also contained many cells that did not belong to the above groups but whose activity was clearly modulated by pitch rotation (called pitch cells for the present study, n = 44). Many (n = 23) showed some correlation with vestibular quick phases, and some (n = 12) with visually elicited eye movement, although they showed significantly lower and more irregular discharge rates than burst-tonic and tonic neurons (mean discharge rate when the eye was near the primary position 34, range 3–91, spikes/s; mean CV 0.61, range 0.15–1.7). During pitch rotation they showed the mean phase lag and gain of 119(±26 SD) deg and 3.2(±2.1 SD) spikes/s/deg/s². Some cells showed a much lower phase lag of about 90 deg. (6) More than half the burst-tonic, tonic and pitch cells tested were antidromically activated by stimuli applied to the ponto-medullary medial longitudinal fasciculus at the level of abducens nucleus, while none of them were activated from the inferior olive, suggesting that vertical eye position signals carried by some burst-tonic and tonic neurons are carried to the lower brainstem.     

Influence of otolithic stimulation by horizontal linear acceleration on optokinetic nystagmus and visual motion perception

Summary Several studies in the past have demonstrated the existence of an Otolith-Ocular Reflex (OOR) in man, although much less sensitive than canal ocular reflex. The present paper 1 confirms these previous results. Nystagmic eye movements (L-nystagmus) appear in the seated subject during horizontal acceleration along the interaural axis in the dark for an acceleration level (1 m/s²) about ten times the perception threshold with a sensitivity of about 0.035 rad/m.When sinusoidal linear acceleration is combined with optokinetic stimulation, the recorded nystagmus slow phase velocity exhibits strong periodic modulation related to subject motion. This marked effect of linear acceleration on the optokinetic nystagmus (OKN) appears at a level (0.1 m/s²) close to the acceleration perception threshold and has a 4-fold higher sensitivity than L-nystagmus. Modulation of OKN can reach a peak-to-peak amplitude as great as 20 °/s; for a given optokinetic field size it increases with the velocity of the optokinetic stimulus, i.e. with the slow phase eye velocity. In parallel with changes in OKN slow phase velocity, linear acceleration induces a motion related decrease in the perceived velocity of the visual scene and modifications in selfmotion perception.The results are interpreted in terms of a mathematical model of visual-vestibular interaction. They show that sensory interaction processes can magnify the contribution given to the control of eye movements by the otolithic system and provide a way of exploring its function at low levels of acceleration.The present work has been presented at III European Neurosciences Meeting, Rome, September 1979     

Distribution of optokinetic sensitivity across the retina of mice in relation to eye orientation

We examined the effects of stimulus size and location on the mouse optokinetic response (OKR). To this end, we recorded initial OKRs elicited by a brief presentation of horizontally moving grating patterns of different vertical widths and locations in the visual field. Large-field stimuli generated large sustained OKRs, whereas visual stimuli of narrower vertical widths elicited weaker sustained responses at the later period (400–500 ms after the onset of stimulus motion). However, even stimuli of only 5° vertical width elicited detectable transient responses at the initial open-loop period (100–200 ms after the onset of stimulus motion). Presenting 5°-width stimuli at different vertical locations (−10° to +35° relative to the horizon) revealed the spatial distribution of optokinetic sensitivity across the retina. The most sensitive part of the visual field was located at +25°. In addition, we examined the vertical orientation of the eye under our stereotaxic set-up. We observed the optic disc using a hand-held fundus camera and determined the ocular orientation. All eye orientations were distributed in the range of +20–30° relative to the horizon (25.2±2.5°). Thus, the direction of the most sensitive visual field matched the angle of eye orientation. These findings indicate that the spatial distribution of visual field sensitivity to optokinetic stimuli coincides with the distribution of retinal ganglion cell density.     

Response properties of single units in the lateral terminal nucleus of the accessory optic system in the behaving primate

1. To determine the potential role of the primate accessory optic system (AOS) in optokinetic and smooth-pursuit eye movements, we recorded the activity of 110 single units in a subdivision of the AOS, the lateral terminal nucleus (LTN), in five alert rhesus macaques. All monkeys were trained to fixate a stationary target spot during visual testing and to track a small spot moving in a variety of visual environments. 2. LTN units formed a continuum of types ranging from purely visual to purely oculomotor. Visual units (50%) responded best for large-field (70 x 50 degrees), moving visual stimuli and had no response associated with smooth-pursuit eye movement; some responded during smooth pursuit in the dark, but the response disappeared if the target was briefly extinguished, indicating that their smooth-pursuit-related response reflected activation of a parafoveal receptive field. Eye movement and visual units (36%) responded both for large, moving visual stimuli and during smooth-pursuit eye movements made in the dark. Eye movement units (14%) discharged during smooth-pursuit or other eye movements but showed no evidence of visual sensitivity. 3. Essentially all (98%) LTN units were direction selective, responding preferentially during vertical background and/or smooth-pursuit movement. The vast majority (88%) preferred upward background and/or eye movement. During periodic movement of the large-field visual background while the animal fixated, their firing rates were modulated above and below rather high resting rates. Although LTN units typically responded best to movement of large-field stimuli, some also responded well to small moving stimuli (0.25 degrees diam). 4. LTN units could be separated into two populations according to their dependence on visual stimulus velocity. For periodic triangle wave stimuli, both types had velocity thresholds less than 3 degrees/s. As stimulus velocity increased above threshold, the activity of one type reached peak firing rates over a very narrow velocity range and remained nearly at peak firing for velocities from approximately 4-80 degrees/s. The firing rates of the other type exhibited velocity tuning in which the firing rate peaked at an average preferred velocity of 13 degrees/s and decreased for higher velocities. 5. A close examination of firing rates to sinusoidal background stimuli revealed that both unit types exhibited unusual behaviors at the extremes of stimulus velocity.(ABSTRACT TRUNCATED AT 400 WORDS)     

Visual and oculomotor signals in nucleus reticularis tegmenti pontis in alert monkey

A small region in the dorsal midline portion of the nucleus reticularis tegmenti pontis (NRTP) in monkeys contains neurons that respond to focal visual stimuli or during saccadic eye movements or both. None of these cells or any others in this region respond to the motion of large visual fields (optokinetic stimulation), although such responses were specifically sought. Thus, this group of NRTP neurons forms a completely different set of cells than those previously described in more rostral but closely adjacent portions of the pontine nuclei which respond well to optokinetic stimulation. The most frequently encountered cell type in this region of NRTP (153 neurons) produced a high-frequency burst of discharges during saccadic eye movements. Neural discharge (burst intensity or duration) was not related to saccade metrics. Instead, peak burst frequency and/or the number of spikes in a unit's burst reached a maximum when the saccade moved the eyes to a circumscribed region (movement field) of the animal's visual field. There were two subtypes of these burst neurons. In one type (44%) the movement fields were smaller and entirely contained within the oculomotor range. In the other type (56%) the movement fields consisted of a whole sector (some as wide as 180 degrees) of the entire oculomotor range. All the neurons in this sample that we were able to test in total darkness continued to produce bursts of discharges of similar profile during spontaneous saccades into their movement field. All the movement fields were retinotopically organized, although a few cells (22%) showed a marked variation of burst metrics with initial eye position. Another small group of cells in NRTP (8 neurons) responded to small spots of light turned on within a circumscribed region of the visual field while the animal maintained fixation on a separate spot of light. These visual neurons produced no saccade-related discharge. A larger group of neurons (24 out of 52 tested cells) produced both a visual response and a saccadic burst. The visual field of this type of cell was always smaller and was contained within the movement field of the cell. The response of both types of NRTP visual neurons was enhanced when the visual stimulus was to be the target for a saccadic eye movement. On double-saccade trials the visual stimulus was never present in the hemifield containing the cell's visual field.(ABSTRACT TRUNCATED AT 400 WORDS)     

The velocity response of vestibular nucleus neurons during vestibular,visual, and combined angular acceleration

Summary In alert Rhesus monkeys neuronal activity in the vestibular nuclei was measured during horizontal angular acceleration in darkness, acceleration of an optokinetic stimulus, and combined visual-vestibular stimulation. The working ranges for visual input velocity and acceleration extend up to 60 °/s and 5 °/s². The corresponding working range for vestibular input acceleration is wider and time-dependent. During combined stimulation, that is acceleration of the monkey in the light, a linear relation between neuronal activity and velocity could be established for all neurons. Type I vestibular plus eye movement neurons displayed the greatest sensitivity and had a small linear range of operation. Other vestibular neurons were less sensitive but had a larger range of linear response to different values of acceleration. Accelerating the animal and visual surround, simultaneously but in opposite directions, results in neuronal activity proportional to relative velocity over a limited range.Supported by a grant from the Swiss National Foundation for Scientific Research 3.672-0.77     

Visual sensory substitution in vestibular compensation: neuronal substrates in the alert cat

The purpose of this study was to investigate adaptive changes in the activity of vestibular nuclei neurons unilaterally deprived of their primary afferent inputs when influenced by visual motion cues. These neuronal changes might account for the established role that vision plays in the compensation for posturo-kinetic deficits after the loss of vestibular inputs. Neuronal recordings were made in alert, non-paralysed cats that had undergone unilateral vestibular nerve sections. The unit responses collected in both Deiters' nuclei were compared to those previously recorded in intact cats. We analysed the extracellular activity of Deiters' nucleus neurons, as well as the optokinetic reflex (OKR) evoked during sinusoidal translation of a whole-field optokinetic stimulus in the vertical plane. In intact cats, we found the unit firing rate closely correlated with the visual surround translation velocity, and the relationship between the discharge rate and the motion frequency was tuned around an optimal frequency. The maximum firing rate modulation was generally below the 0.25 Hz stimulus frequency; unit responses were weak or even absent above 0.25 Hz. From the 4th day to the end of the 3rd week after ipsilateral deafferentation, a majority of cells was found to display maximum discharge modulation during vertical visual stimulation at 0.50 Hz, and even at 0.75 Hz, indicating that the frequency bandwidth of the visually induced responses of deafferented vestibular nuclei neurons had been extended. Consequently, the frequency-dependent attenuation in the sensitivity of vestibular neurons to visual inputs was much less pronounced. After the first 3 weeks postlesion, the unit response characteristics were very similar to those observed prior to the deafferentation. On the nucleus contralateral to the neurectomy, the maximum modulation of most cells was tuned to the low frequencies of optokinetic stimulation, as also seen prior to the lesion. We found, however, a subgroup of cells displaying well-developed responses above 0.50 Hz. Under all experimental conditions, the neuronal response phase still remained closely correlated with the motion velocity of the vertical sinusoidal visual pattern. We hypothesize that Deiters' neurons deprived of their primary afferents may transiently acquire the ability to code fast head movements on the basis of visual messages, thus compensating, at least partially, for the loss of dynamic vestibular inputs during the early stages of the recovery process. Since the overall vertical OKR gain was not significantly altered within the 0.0125 Hz–1 Hz range of stimulation after the unilateral neurectomy, it can be postulated that the increased sensitivity of deafferented vestibular neurons to visual motion cues was accounted for by plasticity mechanisms operating within the deafferented Deiters' nucleus. The neuroplasticity mechanisms underlying this rapid and temporary increase in neuronal sensitivity are discussed.     

Analysis of signal content of Purkinje cell responses to optokinetic stimuli in the rabbit cerebellar flocculus by selective lesions of brainstem pathways

The heterogeneous signal content of floccular Purkinje cell responses to optokinetic stimuli was analyzed in alert rabbits by means of selective lesions to brainstem pathways. Extracellular spike activities of Purkinje cells were recorded from rostral areas of the flocculus where local electrical stimulation elicited abduction of the ipsilateral eye. Chronic unilateral destruction of the nucleus reticularis tegmenti pontis, interrupting the visual mossy fiber afferent pathway to the flocculus, reduced the gain of the optokinetic eye movement (OKR) to one-third of the control. Concomitantly, simple spike responses of Purkinje cells to optokinetic stimuli were reduced to less than one-third of the control values. Severance of the visual climbing fiber afferent pathway by rostral inferior olivary lesions reduced the OKR gain little, and decreased the simple spike responses of the Purkinje cells only slightly. Bilateral lesions of the rostral half of the medial vestibular nucleus and rostro-ventral part of the lateral vestibular nucleus, which reduced the eye velocity in the OKR to less than one-third of the control value, did not induce any appreciable change in the simple spike responses of the Purkinje cells. It is concluded that visual mossy fiber signals are the most dominant factor which determines Purkinje cell responses to optokinetic stimuli, while visual climbing fiber signals and eye velocity mossy fiber signals make only subsidiary contributions.     

Response properties of neurons in posterior parietal cortex of monkey during visual-vestibular stimulation. II. Optokinetic neurons

Recordings have been made from single neurons in area 7a or PG (11) in alert monkeys. Studies were limited to those neurons that were activated during optokinetic stimulation in a particular direction but not during foveal pursuit of a small moving target in the dark. Neurons responding in this way were called optokinetic. There was a considerable number of passive visual neurons, which responded to the movement of a visual stimulus during visual fixation but did not respond during optokinetic nystagmus (OKN). Most optokinetic neurons (46/51) also responded during suppression of OKN and usually displayed the same directional preference (43/46). Average discharge rates during constant-velocity optokinetic stimulation in the preferred direction increased monotonically with increases in stimulus velocity in the range 0-60 degrees/s (9/9), and most (7/9) tended to saturate at higher velocities. While the monkey fixated a stationary target light in the dark, most optokinetic neurons (20/24) responded to small moving visual stimuli, and more than half of them (13/20) had the same directional preferences as during OKN. When the chair in which the monkey was seated was oscillated sinusoidally in combination with optokinetic stimulation, most optokinetic neurons seemed to fall into one of two groups; one mainly responded when the animal was oscillated inside a stationary cylinder, and the other when the chair and the lighted cylinder were moved in synchrony together. The results suggest that some of the optokinetic neurons in area 7a or PG may receive extraretinal inputs similar to those that have been suggested to impinge on visual tracking neurons.