1. The effects of electrical pulse stimulation and temporary pharmacological inactivation of the ipsilateral cerebellar flocculus on the activity of single Y group cells were studied in three alert squirrel monkeys. The extent of the flocculus was mapped by multiunit recording and by electrical pulse train stimulation, which elicited slow eye movement. 2. Single electrical pulse stimulation of the flocculus (0.1-ms constant current, 25-400 microA) resulted in inhibition of all 24 Y cells examined. The inhibition was evidenced as a cessation of cell firing for varying periods [8.8 +/- 2.4 (SD) ms] after the stimulus. The latency of inhibition (0.71 +/- 0.34 ms) suggests that the effect was due to direct activation of Purkinje cells monosynaptically projecting to the Y group. 3. The gamma-aminobutyric acid (GABA) agonist muscimol was used to temporarily inactivate the flocculus while recording from single Y neurons. After control responses of cells under various behavioral paradigms were collected, muscimol (total volume of 3-4 microliters of 2.0% muscimol in saline) was injected in the flocculus through a pair of fine syringes. With this technique, the contribution of the flocculus to the signal content of Y group cells was examined, both in the animals with normal vestibuloocular reflex (VOR) gain (5 cells in 3 animals) and after adaptation of the VOR to either high (5 cells in 1 animal) or low gain (7 cells in 2 animals). 4. In the normal animal, pharmacological floccular inactivation resulted in increased dc firing and in the loss of normal modulation with eye velocity. Modulation during visual-vestibular interactions was also lost, so cell responses did not differ from those during the VOR in darkness. Only minor changes (usually gain increases) in the latter response were noted after flocculus inactivation. The results suggests an extrafloccular input source to the Y group, conveying head velocity information. We believe that this input originates in the brain stem, probably in the superior vestibular nucleus. 5. To examine whether the adapted responses of Y cells during the VOR in darkness are due to their floccular input, single cells were studied before and after pharmacological floccular inactivation, in animals whose VOR had been adapted.(ABSTRACT TRUNCATED AT 400 WORDS)
1. Using single-unit recording and microstimulation methods, a group of flocculus target neurons (FTNs) were identified in the superior vestibular nucleus (SVN) and were studied using visual-vestibular interaction paradigms in alert squirrel monkeys. The response properties of these FTNs were characterized and compared with those of flocculus projecting neurons (FPNs). 2. FTNs were monosynaptically inhibited by single-pulse flocculus stimulation. The mean inhibition latency was 1.0 +/- 0.57 (SD) ms (n = 40) and the mean inhibition period was 6.7 +/- 2.69 ms. FTNs were also monosynaptically activated by VIIIth nerve stimulation. The mean response latency was 1.10 +/- 0.25 ms (n = 12). This is about the same as that of the FPNs (1.14 +/- 0.16 ms, n = 17). 3. The most characteristic response property of the FTNs is their firing rate modulation during visual following eye movements induced by sinusoidal rotation of an optokinetic drum at 0.5 Hz. This modulation was mainly related to eye velocity and was therefore termed a visual following eye velocity signal. The average eye velocity gain for all FTNs is 0.79 spikes.s-1.deg-1.s-1. In contrast, the responses of FPNs were not modulated under the same conditions. 4. Even though FTNs are inhibited by the flocculus, they have a relatively higher mean firing rate (124 +/- 23 spikes/s, n = 45) than FPNs (66 +/- 28 spikes/s, n = 42). The underlying mechanism may be related to commissural facilitation of FTNs and commissural inhibition of FPNs. 5. Thirty FTNs were identified as upward eye velocity FTNs because their firing rate increased for upward eye velocity during a visual following eye movement. The mean eye velocity sensitivity was 1.09 spikes.s-1.deg-1.s-1. Most of these cells also modulated during vestibuloocular reflex (VOR) in the dark, with firing rate increasing for downward head velocity. During VOR suppression the firing rate either did not modulate or modulated in phase with head or drum velocity with a smaller amplitude in comparison with the response during visual following. For all cells (with 1 exception) the response during a visual following eye movement can be approximately predicted by a linear vectorial subtraction of the response during VOR suppression and the response during VOR in the dark [modulation response vector of FTNs during visual following of the optokinetic stimulus (OKR) approximately modulation response vector of FTNs during VOR suppression-modulation response vector of FTNs during VOR in the dark].(ABSTRACT TRUNCATED AT 400 WORDS)
1. The activity of 113 Y group neurons was recorded extracellularly in 5 alert squirrel monkeys. Sixty-two cells were recorded in naive animals, and 51 cells were recorded after adaptation of the vestibuloocular reflex (VOR) with the use of telescopic lenses. The animals were lying on their right side, so that head rotation was in the vertical (pitch) plane and optokinetic stimulation elicited vertical eye movement. The responses of most cells, as well as the concurrent eye movement, were studied during 1) the VOR, elicited in darkness or in light by sinusoidal head rotation, 2) visual following, elicited by sinusoidal rotation of a full-field optokinetic drum around the stationary animal, and 3) paradigms of visual-vestibular interaction, elicited by combined sinusoidal vestibular and optokinetic stimulation. Stimulation parameters for both head and drum velocity were usually 0.5 Hz, 35 degrees/s peak velocity. 2. Y group cells respond vigorously during visual following and during suppression of the VOR (produced by in-phase rotation of the head and the optokinetic drum); the response is approximately in-phase with eye velocity during visual following, and approximately in-phase with head velocity during suppression of the VOR. During the VOR in darkness, Y cells usually exhibit only slight modulation. The results suggest a linear interaction of visual following and vestibular signals on Y cells during vertical visual-vestibular interaction. Taking into account the excitatory projection of Y cells to superior rectus and inferior oblique motoneurons, a causal role of the Y group in rapid modification of VOR gain during visual-vestibular interaction is suggested. 3. Nine Y neurons from two animals were recorded continuously, for periods ranging from 30 min to 5 h, while the VOR was being adapted to higher or lower gain. Progressive changes of the gain of the VOR in darkness were evident after approximately 30 min from the initiation of head rotation under visual-vestibular mismatch. Consistent changes of the gain and/or phase of the neuronal response during the VOR in darkness were noted in all cases. The phase of the neuronal response gradually approximated head velocity phase during adaptation of the VOR to low gain, increases in the neuronal gain thereafter ensued; the opposite changes were observed during adaptation of the VOR to high gain. 4. Sixteen Y cells were recorded from 1 animal chronically adapted to high VOR gain with the use of magnifying lenses, and 35 cells were recorded from 2 animals chronically adapted to low VOR gain with the use of miniaturizing lenses.(ABSTRACT TRUNCATED AT 400 WORDS)
Neurons in the Y group of the vestibular nuclei are activated disynaptically from the ipsilateral VIIIth nerve and polysynaptically from the contralateral nerve. The ipsilateral anterior and posterior semicircular canals project to the Y group via interneurons in the vestibular nuclei. Candidate interneurons located in the rostrolateral corner of the superior (SVN) and in the caudal medial (MVN) vestibular nuclei were retrogradely labeled by the iontophoretic injection of biocytin into the Y group. The physiology of these interneurons named Y-group projecting neurons (YPNs) was studied in the SVN. SVN-YPNs were activated antidromically by electric pulse stimulation in the Y group. The properties of SVN-YPNs are distinct from those of SVN flocculus projecting neurons (FPNs). Namely, YPNs have a lower resting rate than FPNs, have more irregular interspike intervals, show a different phase and gain during the vestibuloocular reflex, and are located differentially within the SVN. After the injection of biocytin into the Y group, the locations of Purkinje cells that project to the Y group were confined to the vertical zones of the flocculus and ventral paraflocculus. However, mossy fibers originating in the Y group terminate in both the vertical and horizontal zones of the flocculus and ventral paraflocculus as well as in the ipsilateral nodulus.
1. Properties of superior vestibular nucleus (SVN) neurons and their projection to the cerebellar flocculus were studied in alert squirrel monkeys by using chronic unit and eye movement recording and microstimulation techniques. Twenty-three cells were antidromically activated from the ipsilateral flocculus, and seventeen of these were also orthodromically activated from the ipsilateral VIIth nerve at monosynaptic latencies. Only 1 of these 23 units was also inhibited by flocculus stimulation. According to their response properties, 9 of the cells were pure vestibular, 2 were vestibular-pause, and 12 were position-vestibular cells. The mean eye position sensitivity of these position-vestibular cells was significantly lower than that of cells projecting to the oculomotor nucleus (OMN). No eye movement-only neurons were antidromically activated from the flocculus. No cells could be antidromically activated from both the oculomotor nucleus and the flocculus.
1. Spontaneous saccades, vestibuloocular responses (VOR), and optokinetic nystagmus were recorded in three squirrel monkeys before and after chemical or electrolytic lesion of the posterior commissure (PC). 2. PC lesions produced abnormal vertical eye movements, in particular, 1) Postsaccadic drifts, and 2) VOR gain reduction and phase advance more pronounced at lower frequencies of sinusoidal head rotation. Horizontal eye movements were much less affected (or normal). 3. We conclude that PC fibers are necessary for conveying the output of the vertical neural integrator to vertical oculomotor-neurons.
1. Seven upward eye velocity flocculus target neurons (FTNs) and two flocculus projecting neurons (FPNs) were studied before and after ipsilateral flocculus inactivation by injection of muscimol in the alert squirrel monkey. An additional seven FTNs and seven FPNs recorded from the corresponding FTN and FPN areas were recorded after injection. Response properties of FTNs and FPNs were characterized by visual-vestibular interaction paradigms and were compared before and after flocculus inactivation. 2. In FTNs the mean firing rate increased within 2-5 min after muscimol injection in the flocculus and reached a plateau level in approximately 10-20 min. The average mean firing rate for seven FTNs increased from 117 to 174 spikes/s, a net increase of 57 spikes/s (49%). Accompanying the large increase of the mean firing rate, a spontaneous nystagmus in the darkness developed with the slow phase directed upward and contralateral. 3. The firing rate modulation during visual following of a sinusoidal optokinetic drum (0.5 Hz) decreased within 2-5 min after muscimol injection in the flocculus and reached a level of 0 in approximately 10-20 min for all FTNs. After that, some cells remained unmodulated for the period of recording; other cells gradually reversed their phase and developed a modulation out of phase with drum velocity. The depletion of the visual following eye velocity signal on superior vestibular nucleus (SVN) FTNs accompanied a small but consistent decrease of visual following eye velocity amplitude. The average maximum decrease of eye velocity was 26 +/- 9% (mean +/- SD). 4. After flocculus inactivation, even though the modulation response at 0.5 Hz during visual following was abolished, a slow-component eye velocity signal with the same on direction was revealed by a constant-velocity optokinetic stimulus. It is concluded that there are at least two kinds of eye velocity signals during the optokinetic response. These signals are combined at the FTNs and are subsequently relayed to the oculomotor neurons. The source of the fast component is the flocculus, and the source of the slow component is another, as yet unidentified brain structure. 5. The effect of flocculus inactivation on the modulation amplitude during the vestibuloocular reflex (VOR) in darkness was variable: two cells did not change, two cells decreased, and three cells increased their amplitude. The response phase tended to move toward a phase lead, but the change was small. The effect on VOR suppression was more prominent.(ABSTRACT TRUNCATED AT 400 WORDS)
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