Site of interaction between saccade signals and vestibular signals induced by head rotation in the alert cat: functional properties and afferent organization of burster-driving neurons

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)


1990 ◽  
Vol 63 (4) ◽  
pp. 902-917 ◽  
Author(s):  
Y. Iwamoto ◽  
T. Kitama ◽  
K. Yoshida

1. The firing characteristics and projection patterns of secondary vestibular nucleus neurons involved in the vertical vestibuloocular pathways were investigated in alert cats. Single-unit recordings were made in the medial longitudinal fasciculus (MLF) near the trochlear nucleus from axons that were monosynaptically activated after electrical stimulation of the vestibular nerve. In a total of 253 identified secondary neurons, 225 discharged in relation to vertical eye movements; 189 of these increased their firing rate for downward eye movements and 36 for upward movements. The activity of the remaining 28 axons was not related to eye movements when the head was still. 2. Virtually all of the secondary neurons with downward on-direction displayed tonic activity that was primarily related to steady eye position during fixation (DPV neurons). The slope of the relationship between firing rate and vertical eye position ranged from 1.2 to 9.1 (spikes/s)/deg with a mean of 3.2 (spikes/s)/deg. The regularity of firing was quantified by calculating the coefficient of variation (CV) of interspike intervals. A comparison of the CV in the population units indicated that DPV neurons could be classified as either regular or irregular neurons. There was a tendency for regular neurons to have higher firing rates and higher correlation coefficients for the rate-position relationships than irregular neurons. 3. During pitch rotation in the light, all the DPV neurons tested increased their firing rate with upward head rotation. Both the phase and the amplitude of the response indicated that DPV neurons discharged not only in relation to eye position but also in relation to head velocity, suggesting that they received monosynaptic input from the posterior semicircular canal. The gain and phase lag of the response relative to head velocity were measured at 0.5 Hz. The range of the gain was 1.1-5.1 (spikes/s)/(deg/s), and that of the phase lag was 18.3-62.4 degrees. There was a tendency for irregular DPV neurons to have a larger gain and smaller phase lag than regular DPV neurons. 4. Ascending and descending projection pathways were determined for 147 DPV axons. Of these, 69 ascended in the contralateral MLF with respect to their soma (crossed-DPV axons), and 78 in the ipsilateral MLF (uncrossed-DPV axons), as revealed by their monosynaptic activation from the contralateral or ipsilateral vestibular nerve. Stimulation of the caudal MLF at the level of the obex evoked direct responses caused by antidromic activation of descending collaterals in approximately 70% (49/69) of the crossed-DPV axons.(ABSTRACT TRUNCATED AT 400 WORDS)


1990 ◽  
Vol 64 (2) ◽  
pp. 413-422 ◽  
Author(s):  
J. M. Delgado-Garcia ◽  
C. Evinger ◽  
M. Escudero ◽  
R. Baker

1. The activity of both accessory abducens (Acc Abd) and abducens (Abd) motoneurons (Mns) was recorded in the alert cat during eye retraction and rotational eye movements. Cats were fitted with two scleral coils, one measured rotational eye movements directly and the other retraction by distinguishing the translational component. 2. Acc Abd and Abd Mns were identified following antidromic activation from electrical stimulation of the ipsilateral VIth nerve. 3. In response to corneal air puffs, bursts of spikes were produced in all (n = 30) Acc Abd Mns. The burst began 7.2 +/- 1.2 (SD) ms after onset of the air puff and 8.9 +/- 1.9 ms before eye retraction. 4. Acc Abd Mns were silent throughout all types of rotational eye movements, and tonic activity was not observed during intervals without air-puff stimulation. 5. In contrast, all (n = 50) identified Abd Mns exhibited a burst and/or pause in activity preceding and during horizontal saccades as well as a tonic activity proportional to eye position. 6. Only 10% of Abd Mns fired a weak burst of spikes in response to air-puff stimulation. 7. We conclude that Acc Abd Mns are exclusively involved in eye retraction in the cat and that only a few Abd Mns have an eye-retraction signal added to their eye position and velocity signals. Thus any rotational eye-movement response described in retractor bulbi muscle must result from innervation by Mns located in the Abd and/or the oculomotor nuclei. 8. The organization of the prenuclear circuitry and species variation are discussed in view of the nictiating membrane extension response measured in associative learning.


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 73 (4) ◽  
pp. 1396-1413 ◽  
Author(s):  
J. S. Stahl ◽  
J. I. Simpson

1. We recorded single vestibular nucleus neurons shown by electrical stimulation to receive floccular inhibition [flocculus receiving neurons (FRNs)] and/or to project toward midbrain motoneuronal pools [midbrain projecting neurons (MPNs)] in awake, head-fixed rabbits during compensatory eye movements. Stimuli included head rotation in the light, head rotation in the dark, and rotation of an optokinetic drum about the animal. We employed sinusoidal and triangular position profiles in the 0.05- to 0.8-Hz frequency band. We also examined transient responses to step changes in eye position. 2. We found identified vestibular nucleus cells (i.e., FRN/non-MPNs, FRN/MPNs, and non-FRN/MPNs) in the parvocellular and magnocellular portions of the medial vestibular nucleus, at the rostrocaudal level of the dorsal acoustic stria. 3. All identified vestibular nucleus neurons were excited during ipsilateral (relative to side of recording) head rotation and contralateral eye rotation. 4. The neuronal firing rates could be related to eye position and its time derivatives, and that relationship could be approximated by a two-pole, one-zero linear transfer function. As with abducens neurons, a more detailed approximation requires inclusion of two nonlinearities-a hysteresis and a variable sensitivity term that increases as eye movement amplitude decreases. 5. When the vestibuloocular reflex is suppressed by a conflicting full-field visual stimulus [visual vestibular conflict condition (VVC)], vestibular nucleus neuron modulation is largely suppressed. The remaining modulation is motoric in nature, because it can be related to the residual eye movements. Cells with "sensory vestibular signals," i.e., cells whose modulation during VVC correlates better with head rotation than eye movement, were not encountered. 6. We examined the dependence of firing rate parameters on stimulus modality. All neurons exhibited increased phase lead with respect to abducens nucleus neurons during stimuli involving head rotation. This finding could indicate that vestibular-derived inputs are inhomogeneously distributed on premotor neurons and that the studied premotor population receives a stronger vestibular input than another premotor group, not recorded in the current experiments. 7. FRNs and non-FRNs were similar in their qualitative response to the fast phases, the applicability of the two-pole, one-zero transfer function, hysteresis, and the amplitude nonlinearity. 8. FRNs differed from non-FRNs in having a phase advanced firing rate at all stimulus frequencies during visual and vestibular stimuli. The phase difference suggests that one role of the rabbit flocculus is to regulate phase of the net premotor signal.


1993 ◽  
Vol 69 (3) ◽  
pp. 965-979 ◽  
Author(s):  
K. Hepp ◽  
A. J. Van Opstal ◽  
D. Straumann ◽  
B. J. Hess ◽  
V. Henn

1. Although the eye has three rotational degrees of freedom, eye positions, during fixations, saccades, and smooth pursuit, with the head stationary and upright, are constrained to a plane by ListingR's law. We investigated whether Listing's law for rapid eye movements is implemented at the level of the deeper layers of the superior colliculus (SC). 2. In three alert rhesus monkeys we tested whether the saccadic motor map of the SC is two dimensional, representing oculocentric target vectors (the vector or V-model), or three dimensional, representing the coordinates of the rotation of the eye from initial to final position (the quaternion or Q-model). 3. Monkeys made spontaneous saccadic eye movements both in the light and in the dark. They were also rotated about various axes to evoke quick phases of vestibular nystagmus, which have three degrees of freedom. Eye positions were measured in three dimensions with the magnetic search coil technique. 4. While the monkey made spontaneous eye movements, we electrically stimulated the deeper layers of the SC and elicited saccades from a wide range of initial positions. According to the Q-model, the torsional component of eye position after stimulation should be uniquely related to saccade onset position. However, stimulation at 110 sites induced no eye torsion, in line with the prediction of the V-model. 5. Activity of saccade-related burst neurons in the deeper layers of the SC was analyzed during rapid eye movements in three dimensions. No systematic eye-position dependence of the movement fields, as predicted by the Q-model, could be detected for these cells. Instead, the data fitted closely the predictions made by the V-model. 6. In two monkeys, both SC were reversibly inactivated by symmetrical bilateral injections of muscimol. The frequency of spontaneous saccades in the light decreased dramatically. Although the remaining spontaneous saccades were slow, Listing's law was still obeyed, both during fixations and saccadic gaze shifts. In the dark, vestibularly elicited fast phases of nystagmus could still be generated in three dimensions. Although the fastest quick phases of horizontal and vertical nystagmus were slower by about a factor of 1.5, those of torsional quick phases were unaffected. 7. On the basis of the electrical stimulation data and the properties revealed by the movement field analysis, we conclude that the collicular motor map is two dimensional. The reversible inactivation results suggest that the SC is not the site where three-dimensional fast phases of vestibular nystagmus are generated.(ABSTRACT TRUNCATED AT 400 WORDS)


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)


2000 ◽  
Vol 83 (6) ◽  
pp. 3430-3452 ◽  
Author(s):  
H.H.L.M. Goossens ◽  
A. J. Van Opstal

Trigeminal reflex blinks evoked near the onset of a saccade cause profound spatial-temporal perturbations of the saccade that are typically compensated in mid-flight. This paper investigates the influence of reflex blinks on the discharge properties of saccade-related burst neurons (SRBNs) in intermediate and deep layers of the monkey superior colliculus (SC). Twenty-nine SRBNs, recorded in three monkeys, were tested in the blink-perturbation paradigm. We report that the air puff stimuli, used to elicit blinks, resulted in a short-latency (∼10 ms) transient suppression of saccade-related SRBN activity. Shortly after this suppression (within 10–30 ms), all neurons resumed their activity, and their burst discharge then continued until the perturbed saccade ended near the extinguished target. This was found regardless whether the compensatory movement was into the cell's movement field or not. In the limited number of trials where no compensation occurred, the neurons typically stopped firing well before the end of the eye movement. Several aspects of the saccade-related activity could be further quantified for 25 SRBNs. It appeared that 1) the increase in duration of the high-frequency burst was well correlated with the (two- to threefold) increase in duration of the perturbed movement. 2) The number of spikes in the burst for control and perturbed saccades was quite similar. On average, the number of spikes increased only 14%, whereas the mean firing rate in the burst decreased by 52%. 3) An identical number of spikes were obtained between control and perturbed responses when burst and postsaccadic activity were both included in the spike count. 4) The decrease of the mean firing rate in the burst was well correlated with the decrease in the velocity of perturbed saccades. 5) Monotonic relations between instantaneous firing rate and dynamic motor error were obtained for control responses but not for perturbed responses. And 6) the high-frequency burst of SRBNs with short-lead and long-lead presaccadic activity (also referred to as burst and buildup neurons, respectively) showed very similar features. Our findings show that blinking interacts with the saccade premotor system already at the level of the SC. The data also indicate that a neural mechanism, rather than passive elastic restoring forces within the oculomotor plant, underlies the compensation for blink-related perturbations. We propose that these interactions occur downstream from the motor SC and that the latter may encode the desired displacement vector of the eyes by sending an approximately fixed number of spikes to the brainstem saccadic burst generator.


1985 ◽  
Vol 53 (3) ◽  
pp. 726-745 ◽  
Author(s):  
J. A. Hirsch ◽  
J. C. Chan ◽  
T. C. Yin

Using extracellular electrodes we studied acoustic responses in the superior colliculus (SC) of the barbiturate-anesthetized cat. Pure tonal stimuli were delivered through sealed and calibrated earphones and were presented either monaurally or binaurally with interaural intensity differences (IIDs) and interaural time differences (ITDs). Acoustically sensitive cells were found in the intermediate and deep layers of the SC throughout its rostrocaudal and mediolateral extent. Most cells (80%) discharged only at stimulus onset; the rest had more complex firing patterns. For 88% of our sample the mean first-spike latency measured at 20 dB above threshold ranged between 6 and 16 ms. The sharpness and threshold intensity of the frequency tuning curves varied widely. In the SC, the average characteristic frequency and threshold intensity were higher than in other auditory brain stem nuclei. Neurons whose characteristic frequency was low were never sharply tuned. The probability of response decreased when the repetition rate at which the stimuli were delivered increased. The mean stimulus interval at which spike count reached 50% of maximum was 360 ms. Most (83%) of the cells discharged only to monaural stimulation of the contralateral ear, 7% responded to tones applied to either ear and only 1% to only ipsilateral input. The remaining cells responded only to stimulation of both ears. With binaural stimuli, most neurons (80%) could be shown to receive input from both ears. Seventy percent of the binaural cells showed predominant binaural inhibition (BI), 25% binaural facilitation (BF), and 5% a more complex mixture. Because the majority of SC neurons had high characteristic frequencies, we examined their responses to IIDs. The spike count vs. IID functions of BI cells were monotonic and sigmoidal, those of BF cells were nonmonotonic and bell-shaped. The slopes and horizontal positions of the curves varied among neurons. IIDs favoring the contralateral ear were the most effective. For a given cell, increasing the mean binaural level extended the range of IIDs that evoked maximal discharge. A small number of cells was sensitive to physiologically significant interaural time differences of low-frequency tones or the envelopes of amplitude-modulated, high-frequency tones.


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