Inputs from the ipsilateral and contralateral vestibular apparatus to behaviorally characterized abducens neurons in rhesus monkeys

1995 ◽  
Vol 74 (6) ◽  
pp. 2445-2459 ◽  
Author(s):  
D. M. Broussard ◽  
R. C. DeCharms ◽  
S. G. Lisberger

1. We made extracellular recordings from neurons in the abducens nuclei of alert rhesus monkeys during electrical stimulation of the vestibular labyrinths with brief current pulses and during smooth pursuit, steady fixation, and the vestibuloocular reflex (VOR) evoked by passive head turns. The responses to electrical stimuli were compared with quantitative measures of the sensitivity of each neuron to eye position and eye velocity. We also compared the strengths of the vestibular inputs from the labyrinths ipsilateral and contralateral to the side of recording. 2. Abducens neurons showed transient excitation after a current pulse was applied to the contralateral labyrinth and transient inhibition after stimulation of the ipsilateral labyrinth. The latency of excitation had a mean value of 1.7 ms and a median value of 1.5 ms. Latency was unimodally distributed with little variation among neurons. Neurons with large responses showed a second phase of excitation that started 2.5 ms after the stimulus. 3. In two of three monkeys, the excitatory responses of abducens neurons to electrical stimulation of the contralateral labyrinth were approximately 3 times as large as their inhibitory responses to stimulation of the ipsilateral labyrinth. The difference in response size was not observed in the third monkey. The asymmetry in the size of the electrically evoked inputs from the two labyrinths was associated with a smaller asymmetry in responses of abducens neurons during the VOR evoked by passive head turns. The increase in firing rate during head rotation away from the side of the recording was almost always larger than the decrease in firing rate during head rotation toward the side of the recording. 4. The size of the neuronal response to electrical stimulation was correlated with the magnitude of the change in discharge rate during eye movements. Single or multiple regression of measures of response amplitude against eye position threshold, sensitivity to eye position, sensitivity to eye velocity, and baseline discharge rate yielded correlation coefficients that ranged from 0.26 to 0.92 in different monkeys. The existence of positive correlations is consistent with a role of the intrinsic properties of abducens neurons in determining recruitment order. However, the existence of large amounts of variability within most of the samples suggests that the recruitment order of abducens neurons also depends on the discharge properties of the afferents to each abducens neuron.

1995 ◽  
Vol 74 (1) ◽  
pp. 273-287 ◽  
Author(s):  
T. Kitama ◽  
Y. Ohki ◽  
H. Shimazu ◽  
M. Tanaka ◽  
K. Yoshida

1. Extracellular spikes of burster-driving neurons (BDNs) were recorded within and immediately below the prepositus hypoglossi nucleus in the alert cat. BDNs were characterized by short-latency activation after stimulation of the contralateral vestibular nerve (latency: 1.4-2.7 ms) and the ipsilateral superior colliculus (latency: 1.7-3.5 ms). Convergence of vestibular and collicular inputs was found in all of 85 BDNs tested. Firing of BDNs increased during contralateral horizontal head rotation and decreased during ipsilateral rotation. A burst of spikes was induced in association with contralateral saccades and quick phases of nystagmus. 2. BDNs showed irregular tonic discharges during fixation. There was no significant correlation between the firing rate during fixation and horizontal or vertical eye position in most BDNs. During horizontal sinusoidal head rotation, the change in firing rate was approximately proportional to and in phase with contralateral head velocity. The phase lag of the response relative to head angular velocity was 13.8 +/- 20.1 degrees (mean +/- SD) at 0.5 Hz and 7.2 +/- 13.5 degrees at 0.2 Hz on the average. The gain was 0.88 +/- 0.25 (spikes/s)/(degrees/s) at 0.5 Hz and 1.19 +/- 0.49 (spikes/s)/(degrees/s) at 0.2 Hz. 3. Quantitative analysis of burst activity associated with saccades or quick phases indicated that the ON direction of BDNs was contralateral horizontal. The number of spikes in the burst was linearly related to the amplitude of the contralateral component of rapid eye movements. The slope of regression line was, on the average, 1.14 +/- 0.48 spikes/deg. There was no significant difference between the mean slopes for saccades and quick phases. The number of spikes depended on the difference between initial and final horizontal eye positions and not on the absolute eye position in the orbit. The mean burst firing rate was proportional to the mean velocity of the contralateral component of rapid eye movements. The slope of the regression line was 0.82 +/- 0.34 (spikes/s)/(degrees/s). Significant correlation was also found between intraburst instantaneous firing rate and instantaneous component eye velocity. 4. Objects presented in the contralateral visual field elicited a brief burst of spikes in BDNs independent of any eye movement. Contralateral saccades to the target were preceded by an early response to the visual stimulus and subsequent response associated with eye movement. 5. Excitation of BDNs produced by stimulation of the ipsilateral superior colliculus was facilitated by contralateral horizontal head rotation. Therefore saccadic signals from the superior colliculus to BDNs may be augmented by vestibular signals during head rotation.(ABSTRACT TRUNCATED AT 400 WORDS)


1994 ◽  
Vol 72 (2) ◽  
pp. 909-927 ◽  
Author(s):  
S. G. Lisberger ◽  
T. A. Pavelko ◽  
D. M. Broussard

1. We have identified a group of brain stem cells called “flocculus target neurons” (or FTNs) because they are inhibited at monosynaptic latencies by stimulation of the flocculus and the ventral paraflocculus with single electrical pulses. We report the responses of FTNs, as well as those of other brain stem cells, during horizontal eye movements with the head stationary and during natural vestibular stimulation in monkeys. 2. FTNs discharged primarily in relation to eye movements. The majority (71%) showed increased firing for eye movement away from the side of the recording (“contraversive”), which is consistent with their inhibition by Purkinje cells that show increased firing for eye movement toward the side of recording. However, a significant and surprisingly large percentage (29%) of FTNs showed increased firing for eye movement toward the side of recording (“ipsiversive”). 3. The firing rate of FTNs showed strong modulation during pursuit of sinusoidal target motion with the head stationary and during the compensatory eye movements evoked by fixation of an earth-stationary target with sinusoidal head rotation. In addition, firing rate was related to eye position during steady fixation at different positions. Of the FTNs that showed increased firing for contraversive eye motion during pursuit with the head stationary, most had an infection in the relationship between firing rate and eye position so that the sensitivity to eye position was low for eye positions ipsilateral to straight-ahead gaze and high for eye positions contralateral to straight-ahead gaze. 4. When the monkey canceled the vestibuloocular reflex (VOR) by tracking a target that moved exactly with him during sinusoidal head rotation, the firing rate of FTNs was modulated much less strongly than during pursuit with the head stationary. In the FTNs that showed increased firing for contraversive eye motion during pursuit, firing rate during cancellation of the VOR increased for contraversive head motion during sinusoidal vestibular rotation at 0.4 Hz but was only weakly modulated during rotation at 0.2 Hz. 5. The position-vestibular-pause cells (PVP-cells), previously identified as interneurons in the disynaptic VOR pathways, were not inhibited by stimulation of the flocculus and ventral paraflocculus and had response properties that were different from FTNs. The majority (69%) showed increased firing for contraversive eye motion during pursuit and for ipsiversive head motion during cancellation of the VOR, whereas some (31%) showed the opposite direction preferences under both conditions.(ABSTRACT TRUNCATED AT 250 WORDS)


1958 ◽  
Vol 196 (1) ◽  
pp. 44-48 ◽  
Author(s):  
John W. Mason

Substantial plasma 17-OH-CS elevations invariably occurred during electrical stimulation of the amygdaloid complex in unanesthetized rhesus monkeys through chronically implanted electrodes. No evidence of localization of this effect within anatomical subdivisions of the amygdaloid complex was observed. Stimulation of the amygdala elicited plasma 17-OH-CS elevations (20 µg %/hr.) equal to those occurring with hypothalamic stimulation or injection of a large dose of ACTH (16 mg/kg), while no elevations were observed during putamen stimulation or under normal conditions.


1990 ◽  
Vol 63 (3) ◽  
pp. 502-522 ◽  
Author(s):  
R. Lal ◽  
M. J. Friedlander

1. Extracellular recordings were made from single neurons in layer A of the left dorsal lateral geniculate nucleus (LGNd) of anesthetized and paralyzed adult cats. Responses to retinotopically identical visual stimuli (presented through the right eye) were recorded at several positions of the left eye in its orbit. Visual stimuli consisted of drifting sinusoidal gratings of optimal temporal and spatial frequencies at twice threshold contrast. Visual stimulation of the left eye was blocked by a variety of methods, including intravitreal injection of tetrodotoxin (TTX). The change in position of the left eye was achieved by passive movements in a randomized and interleaved fashion. Of 237 neurons studied, responses were obtained from 143 neurons on 20-100 trials of identical visual stimulation at each of six eye positions. Neurons were classified as X- or Y- on the basis of a standard battery of physiological tests (primarily linearity of spatial summation and response latency to electrical stimulation of the optic chiasm). 2. The effect of eye position on the visual response of the 143 neurons was analyzed with respect to the number of action potentials elicited and the peak firing rate. Fifty-seven (40%) neurons had a significant effect [by one-factor repeated-measure analysis of variance (ANOVA), P less than 0.05] of eye position on the visual response by either criterion (number of action potentials or peak firing rate). Of these 57 neurons, 47 had a significant effect (P less than 0.05) with respect to the number of action potentials and 23 had a significant effect (P less than 0.05) by both criteria. Thus the permissive measure by either criterion and the conservative measure by both criteria resulted in 40% and 16%, respectively, of all neurons' visual responses being significantly affected by eye position. 3. For the 47 neurons with a significant effect of eye position (number of action potentials criterion), a trend analysis of eye position versus visual response showed a linear trend (P less than 0.05) for 9 neurons, a quadratic trend (P less than 0.05) for 32 neurons, and no significant trend for the 6 remaining neurons. The trends were approximated with linear and nonlinear gain fields (range of eye position change over which the visual response was modulated). The gain fields of individual neurons were compared by measuring the normalized gain (change in neuronal response per degree change of eye position). The mean normalized gain for the 47 neurons was 4.3. 4. The nonlinear gain fields were generally symmetric with respect to nasal versus temporal changes in eye position.(ABSTRACT TRUNCATED AT 400 WORDS)


1980 ◽  
Vol 58 (5) ◽  
pp. 574-576 ◽  
Author(s):  
J. Ciriello ◽  
F. R. Calaresu

In 10 cats anaesthetized with chloralose the electrical activity of spontaneously active hypothalamic units was recorded for changes in discharge rate during electrical stimulation of renal afferent nerves. The discharge rate of 141 single units was altered by stimulation of either the ipsilateral or contralateral renal nerves. Most of the responsive units were located in the regions of lateral preoptic nucleus, lateral hypothalamus, and paraventricular nucleus. These results demonstrate that renal afferent nerves provide information to hypothalamic structures known to be involved in the regulation of arterial pressure and fluid balance.


1991 ◽  
Vol 66 (6) ◽  
pp. 2084-2094 ◽  
Author(s):  
R. W. Blair ◽  
A. R. Evans

1. Medullary raphespinal neurons antidromically activated from the T2-T5 segments were tested for responses to electrical stimulation of cervical vagal and thoracic sympathetic afferents (by stimulating the left stellate ganglion), somatic probing, auditory stimuli, and visual stimuli in cats anesthetized with alpha-chloralose. A total of 99 neurons in the raphe nuclei were studied; the locations of 76 cells were histologically confirmed. Neurons were located in raphe magnus (RM, 65%), raphe obscurus (RO, 32%), and raphe pallidus (RPa, 4%). The mean conduction velocity of these neurons was 62 +/- 2.9 (SE) m/s with a range of 1.1-121 m/s. 2. A total of 60/99 tested neurons responded to electrical stimulation of sympathetic afferents. Quantitation of responses was obtained for 55 neurons. With one exception, all responsive neurons were excited and exhibited an early burst of spikes with a mean latency of 16 +/- 1.2 ms. From a spontaneous discharge rate of 5.2 +/- 1.2 spikes/s, neuronal activity increased by 2.9 +/- 0.3 spikes/stimulus. In addition to an early peak, 15 neurons (25%) exhibited a late burst of spikes with a latency of 182 +/- 12.9 ms; neuronal activity increased by 5.0 +/- 1.3 spikes/stimulus. Duration of the late peak (130 +/- 18.5 ms) was longer than for the early peak (18 +/- 0.7 ms), but threshold voltages for eliciting each peak were comparable. Sixteen of 29 spontaneously active neurons exhibited a postexcitatory depression of activity that lasted for 163 +/- 19.1 ms. All but one tested neuron in RO responded to stimulation of sympathetic afferents, but 65% of neurons in RM responded to this stimulus. 3. In response to vagal afferent stimulation, 19% of 57 neurons exhibited inhibition only, 11% were only excited, and 9% were either excited or inhibited, depending on the stimulus paradigm used; the remaining 61% of neurons were unresponsive. From a spontaneous rate of 7.9 +/- 3.8 spikes/s, excited cells increased their discharge rate by 1.6 +/- 0.3 spikes/stimulus. Activity of inhibited cells was reduced from 21.3 +/- 5.8 to 7.8 +/- 3.1 spikes/s. The conditioning-test (CT) technique was used to assess 11 neurons' responses. Stellate ganglion stimulation was the test stimulus, and vagal stimulation the conditioning stimulus. Vagal stimulation reduced the neuronal responses to stellate ganglion stimulation by an average of 50% with a CT interval of 60-100 ms, and cell responses returned to control after 300 ms. With spontaneous cell activity, low frequencies of vagal stimulation were generally excitatory, and high frequencies (10-20 Hz) inhibitory.(ABSTRACT TRUNCATED AT 400 WORDS)


2003 ◽  
Vol 90 (4) ◽  
pp. 2240-2252 ◽  
Author(s):  
Ángel M. Pastor ◽  
David González-Forero

Abducens neurons undergo a dose-dependent synaptic blockade (either disinhibition or complete blockade) when tetanus neurotoxin (TeNT) is injected into the lateral rectus muscle at either a low (0.5) or a high dose (5 ng/kg). We studied the firing pattern and recruitment order in abducens neurons both in control and after TeNT injection. The eye position threshold for recruitment of control abducens neurons was exponentially related to the eye position and velocity sensitivities. We also found a constancy of recruitment threshold for different eye movement modalities (spontaneous, optokinetic, and vestibular). Exponential relationships were found, as well, for eye velocity sensitivity during saccades and for position and velocity sensitivities during the vestibulo-ocular reflex. Likewise, inverse relationships were found between recruitment threshold or position sensitivity with the antidromic latency in control abducens neurons. These relationships, however, did not apply following TeNT treatment. Neuronal firing after TeNT appeared either disinhibited (low dose) or depressed (high dose), but the relationships between neuronal sensitivities and recruitment still applied. However, the pattern of recruitment shifted toward the treated side as more inputs were blocked by the low- and high-dose treatments, respectively. Nonetheless, although the recruitment-to-sensitivity relationships persisted under the TeNT synaptic blockade, we conclude that synaptic inputs are determinant for establishing the recruitment threshold and recruitment spacing of abducens motoneurons and internuclear neurons.


1988 ◽  
Vol 60 (6) ◽  
pp. 1874-1895 ◽  
Author(s):  
A. F. Fuchs ◽  
C. A. Scudder ◽  
C. R. Kaneko

1. Single neurons in the abducens nucleus were recorded extracellularly in alert rhesus macaques trained to make a variety of eye movements. An abducens neurons was identified as a motoneuron (MN) if its action potentials triggered an averaged EMG potential in the lateral rectus muscle. Abducens internuclear neurons (INNs) that project to the oculomotor nucleus were identified by collision block of spontaneous with antidromic action potentials evoked with a stimulating electrode placed in the medial rectus subdivision of the contralateral oculomotor nucleus. 2. All abducens MNs and INNs had qualitatively similar discharge patterns consisting of a burst of spikes for lateral saccades and a steady firing whose rate increased with lateral eye position in excess of a certain threshold. 3. For both MNs and INNs the firing rates associated with different, constant eye positions could be described accurately by a straight line with slope, K (the eye position sensitivity in spikes.s-1.deg-1), and intercept, T (the eye position threshold for steady firing). For different MNs, K increased as T varied from more medial to more lateral values. In contrast, the majority of INNs already were active for values of T more medial than 20 degrees and showed little evidence of recruitment according to K. 4. During horizontal sinusoidal smooth-pursuit eye movements, both MNs and INNs exhibited a sinusoidal modulation in firing rate whose peak preceded eye position. From these firing rate patterns, the component of firing rate related to eye velocity, R (the eye velocity sensitivity in spikes.s-1.deg-1.s-1), was determined. The R for INNs was, on average, 78% larger than that for MNs. Furthermore, R increased with T for MNs, whereas INNs showed no evidence of recruitment according to R. If, as in the cat, the INNs of monkeys provide the major input to medial rectus MNs and if simian medial rectus MNs behave like our abducens MNs, then recruitment order, which is absent in INNs, must be established at the MN pool itself. 5. Unexpectedly, the R of MNs decreased with the frequency of the smooth-pursuit movement. Furthermore, the eye position sensitivity, K, obtained during steady fixations was usually less than that determined during smooth pursuit. Therefore, conclusions about the roles of MNs and premotor neurons based on how their R and K values differ must be viewed with caution if the data have been obtained under different tracking conditions.(ABSTRACT TRUNCATED AT 400 WORDS)


2015 ◽  
Vol 113 (10) ◽  
pp. 3866-3892 ◽  
Author(s):  
James O. Phillips ◽  
Leo Ling ◽  
Kaibao Nie ◽  
Elyse Jameyson ◽  
Christopher M. Phillips ◽  
...  

Animal experiments and limited data in humans suggest that electrical stimulation of the vestibular end organs could be used to treat loss of vestibular function. In this paper we demonstrate that canal-specific two-dimensionally (2D) measured eye velocities are elicited from intermittent brief 2 s biphasic pulse electrical stimulation in four human subjects implanted with a vestibular prosthesis. The 2D measured direction of the slow phase eye movements changed with the canal stimulated. Increasing pulse current over a 0–400 μA range typically produced a monotonic increase in slow phase eye velocity. The responses decremented or in some cases fluctuated over time in most implanted canals but could be partially restored by changing the return path of the stimulation current. Implantation of the device in Meniere's patients produced hearing and vestibular loss in the implanted ear. Electrical stimulation was well tolerated, producing no sensation of pain, nausea, or auditory percept with stimulation that elicited robust eye movements. There were changes in slow phase eye velocity with current and over time, and changes in electrically evoked compound action potentials produced by stimulation and recorded with the implanted device. Perceived rotation in subjects was consistent with the slow phase eye movements in direction and scaled with stimulation current in magnitude. These results suggest that electrical stimulation of the vestibular end organ in human subjects provided controlled vestibular inputs over time, but in Meniere's patients this apparently came at the cost of hearing and vestibular function in the implanted ear.


1992 ◽  
Vol 68 (1) ◽  
pp. 244-264 ◽  
Author(s):  
C. A. Scudder ◽  
A. F. Fuchs

1. To describe in detail the secondary neurons of the horizontal vestibuloocular reflex (VOR), we recorded the extracellular activity of neurons in the rostral medial vestibular nucleus of alert, trained rhesus monkeys. On the basis of their activity during horizontal head and eye movements, neurons were divided into several different types. Position-vestibular-pause (PVP) units discharged in relation to head velocity, eye velocity, eye position, and ceased firing during some saccades. Eye and head velocity (EHV) units discharged in relation to eye velocity and head velocity in the same direction so that the two signals partially canceled during the VOR. Two cell types discharged in relation to eye position and velocity but not head velocity; other types discharged in relation to head velocity only. 2. The position in the neural path from the primary vestibular afferents to abducens motoneurons was examined for each type. Direct input from the vestibular nerve was indicated if the cell could be activated by shocks to the nerve at latencies less than or equal to 1.4 ms. A projection to abducens motoneurons was indicated if spike-triggered averaging of lateral rectus electromyographic (EMG) activity yielded responses with a sharp onset at monosynaptic latencies. 3. PVP neurons were the principal interneuron in the VOR “three-neuron arc.” Eighty percent received primary afferent input, and 66% made excitatory connections with contralateral abducens motoneurons. Surprisingly few, approximately 11%, made inhibitory connections with ipsilateral abducens motoneurons. This imbalance in the ipsi- and contralateral projections was confirmed by measuring the EMG activity evoked by electrical microstimulation in regions where PVP neurons were located. 4. EHV neurons whose activity increased during contralaterally directed head or eye movements were also interneurons in the ipsilateral inhibitory pathway. Eighty-nine percent received ipsilateral primary afferent input, and 25% projected to ipsilateral abducens motoneurons. EHV neurons excited during ipsilateral movements received neither direct primary afferent input nor projected to either abducens nucleus. A small proportion of each of two other cell types having sensitivity to contralateral eye position made excitatory connections with contralateral abducens motoneurons. Other types rarely were activated from the eighth nerve or projected to the abducens nucleus. 5. The significance of the connections of VOR interneurons and the signals they convey is discussed for three situations: smooth pursuit of a moving target, suppression of the VOR, and the VOR itself. PVP neurons convey a signal with a ratio of eye position and velocity components that is inappropriate to drive motoneurons during pursuit or the VOR.(ABSTRACT TRUNCATED AT 400 WORDS)


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