Short-Latency Responses of Neurons in Dorsolateral Pontine Nucleus and Cortical Area MST of Alert Monkey to Movement of Large-Field Visual Stimulus

Author(s):  
Kenji Kawano ◽  
Munetaka Shidara ◽  
Yoshihiro Watanabe ◽  
Shigeru Yamane
1992 ◽  
Vol 67 (3) ◽  
pp. 680-703 ◽  
Author(s):  
K. Kawano ◽  
M. Shidara ◽  
S. Yamane

1. Movements of the visual scene evoke short-latency ocular following responses. To study the neural mediation of the ocular following responses, we investigated neurons in the dorsolateral pontine nucleus (DLPN) of behaving monkeys. The neurons discharged during brief, sudden movements of a large-field visual stimulus, eliciting ocular following. Most of them (100/112) responded to movements of a large-field visual stimulus with directional selectivity. 2. Response amplitude was measured in two components of the neural response: an initial transient component and a late sustained component. Most direction-selective DLPN neurons showed their strongest responses at high stimulus speeds (80-160 degrees/s), whether their response components were initial (63/87, 72%) or sustained (63/87, 72%). The average firing rates of 87 DLPN neurons increased as a linear function of the logarithm of stimulus speed up to 40 degrees/s for both initial and sustained responses. 3. Not only the magnitude but also the latency of the neural and ocular responses were dependent on stimulus speed. The latencies of both neural and ocular responses were inversely related to the stimulus speed. As a result, the time difference between the response latencies for neural and ocular responses did not vary much with changes of stimulus speed. 4. Response latency was measured when a large-field random dot pattern was moved in the preferred direction and at the preferred speed of each neuron. Seventy-three percent (56/77) of the neurons were activated less than 50 ms after the onset of the stimulus motion. In most cases (67/77, 87%), their increase of firing rate started before the eye movements, and 34% of them (26/77) started greater than 10 ms before the eye movements. 5. Blurring of the random dot pattern by interposing a sheet of ground glass increased the latency of both neural responses and eye movements. On the other hand, the blurred images did not change the timing of the effect of blanking the visual scene on the responses of the neurons or eye movements. 6. When a check pattern was used instead of random dots, both neural and ocular responses began to decrease rapidly when the temporal frequency of the visual stimulus exceeded 20 Hz. When the temporal frequency of the visual stimulus approached 40 Hz, the neurons showed a distinctive burst-and-pause firing pattern. The eye movements recorded at the same time showed signs of oscillation, and their temporal patterns were closely correlated to those of the firing rate.(ABSTRACT TRUNCATED AT 400 WORDS)


1990 ◽  
Vol 63 (1) ◽  
pp. 37-59 ◽  
Author(s):  
D. A. Suzuki ◽  
J. G. May ◽  
E. L. Keller ◽  
R. D. Yee

1. In this study we sought to characterize the visual motion processing that exists in the dorsolateral pontine nucleus (DLPN) and make a comparison with the reported visual responses of the middle temporal (MT) and medial superior temporal (MST) areas of the monkey cerebral cortex. The DLPN is implicated as a component of the visuomotor interface involved with the regulation of smooth-pursuit eye movements, because it is a major terminus for afferents from MT and MST and also the source of efferents to cerebellar regions involved with eye-movement control. 2. Some DLPN cells were preferentially responsive to discrete (spot and bar) visual stimuli, or to large-field, random-dot pattern motion, or to both discrete and large-field visual motion. The results suggest differential input from localized regions of MT and MST. 3. The visual-motion responses of DLPN neurons were direction selective for 86% of the discrete visual responses and 95% of the large-field responses. Direction tuning bandwidths (full-width at 50% maximum response amplitude) averaged 107 degrees and 120 degrees for discrete and large-field visual motion responses, respectively. For the two visual response types, the direction index averaged 0.95 and 1.02, indicating that responses to stimuli moving in preferred directions were, on average, 20 and 50 times greater than responses to discrete or large-field stimulus movement in the opposite directions, respectively. 4. Most of the DLPN visual responses to movements of discrete visual stimuli exhibited increases in amplitude up to preferred retinal image speeds between 20 and 80 degrees/s, with an average preferred speed of 39 degrees/s. At higher speeds, the response amplitude of most units decreased, although a few units exhibited a broad saturation in response amplitude that was maintained up to at least 150 degrees/s before the response decreased. Over the range of speeds up to the preferred speeds, the sensitivity of DLPN neurons to discrete stimulus-related, retinal-image speed averaged 3.0 spikes/s per deg/s. The responses to large-field visual motion were less sensitive to retinal image speed and exhibited an average sensitivity of 1.4 spikes/s per deg/s before the visual response saturated. 5. DLPN and MT were quantitatively comparable with respect to degree of direction selectivity, retinal image speed tuning, and distribution of preferred speeds. Many DLPN receptive fields contained the fovea and were larger than those of MT and more like MST receptive fields in size.(ABSTRACT TRUNCATED AT 400 WORDS)


1999 ◽  
Vol 82 (3) ◽  
pp. 1178-1186 ◽  
Author(s):  
David A. Suzuki ◽  
Tetsuto Yamada ◽  
Rebecca Hoedema ◽  
Robert D. Yee

Anatomic and neuronal recordings suggest that the nucleus reticularis tegmenti pontis (NRTP) of macaques may be a major pontine component of a cortico-ponto-cerebellar pathway that subserves the control of smooth-pursuit eye movements. The existence of such a pathway was implicated by the lack of permanent pursuit impairment after bilateral lesions in the dorsolateral pontine nucleus. To provide more direct evidence that NRTP is involved with regulating smooth-pursuit eye movements, chemical lesions were made in macaque NRTP by injecting either lidocaine or ibotenic acid. Injection sites first were identified by the recording of smooth-pursuit-related modulations in neuronal activity. The resulting lesions caused significant deficits in both the maintenance and the initiation of smooth-pursuit eye movements. After lesion formation, the gain of constant-velocity, maintained smooth-pursuit eye movements decreased, on the average, by 44%. Recovery of the ability to maintain smooth-pursuit eye movements occurred over ∼3 days when maintained pursuit gains attained normal values. The step-ramp, “Rashbass” task was used to investigate the effects of the lesions on the initiation of smooth-pursuit eye movements. Eye accelerations averaged over the initial 80 ms of pursuit initiation were determined and found to be decremented, on the average, by 48% after the administration of ibotenic acid. Impairments in the initiation and maintenance of smooth-pursuit eye movements were directional in nature. Upward pursuit seemed to be the most vulnerable and was impaired in all cases independent of lesioning agent and type of pursuit investigated. Downward smooth pursuit seemed more resistant to the effects of chemical lesions in NRTP. Impairments in horizontal tracking were observed with examples of deficits in ipsilaterally and contralaterally directed pursuit. The results provide behavioral support for the physiologically and anatomic-based conclusion that NRTP is a component of a cortico-ponto-cerebellar circuit that presumably involves the pursuit area of the frontal eye field (FEF) and projects to ocular motor-related areas of the cerebellum. This FEF-NRTP-cerebellum path would parallel a middle and medial superior temporal cerebral cortical area-dorsolateral pontine nucleus-cerebellum pathway also known to be involved with regulating smooth-pursuit eye movements.


2007 ◽  
Vol 98 (5) ◽  
pp. 2918-2932 ◽  
Author(s):  
Seiji Ono ◽  
Michael J. Mustari

The smooth pursuit (SP) system can adapt its response to developmental changes, injury, and behavioral context. Previous lesion and single-unit recording studies show that the macaque cerebellum plays a role in SP initiation, maintenance, and adaptation. The aim of this study was to determine the potential role of the DLPN in SP adaptation. The DLPN receives inputs from the cortical SP system and delivers eye and visual motion information to the dorsal/ventral paraflocculus and vermis of the cerebellum. We studied SP adaptation in two juvenile rhesus monkeys ( Macaca mulatta), using double steps of target speed that step- up (10–30°/s) or step-down (25–5°/s). We used microinjection of muscimol (≤2%; 0.15 μl) to reversibly inactivate the DLPN, unilaterally. After DLPN inactivation, initial ipsilesional SP acceleration (first 100 ms) was significantly reduced by 47–74% ( P < 0.01; unpaired t-test) of control values in the single-speed step-ramp paradigm. Similarly, ipsilesional steady-state SP velocity was also reduced by 59–78% ( P < 0.01; unpaired t-test) of control values. Contralesional SP was not impaired after DLPN inactivation. Control testing showed significant adaptive changes of initial SP eye acceleration after 100 trials in either step-up or step-down paradigms. After inactivation, during ipsilesional SP, adaptation was impaired in the step-up but not in the step-down paradigm. In contrast, during contralesional tracking, adaptive capability remained in the step-down but not in the step-up paradigm. Therefore SP adaptation could depend, in part, on direction sensitive eye/visual motion information provided by DLPN neurons to cerebellum.


1979 ◽  
Vol 42 (1) ◽  
pp. 1-15 ◽  
Author(s):  
G. Mower ◽  
A. Gibson ◽  
M. Glickstein

1. The superior colliculus projects to the dorsolateral nucleus of the pons. Retrograde transport of horseradish peroxidase (HRP) revealed that cells in the superior colliculus, which send their axons to the pons, lie in both superficial (III) and deep (IV--VII) layers. Superficial cells outnumbered deep cells. The inferior colliculus also projects heavily to the dorsolateral pontine nucleus. 2. Dorsolateral pontine visual cells were activated only by visual stimulation. Cells responsive to somatic or auditory stimulation were also found in the dorsolateral nucleus, and they too responded to only one sense modality. 3. Of the dorsolateral pontine visual cells, 69% were directionally selective. 4. Dorsolateral pontine visual cells were responsive to moving targets over a wide range of stimulus velocities. Velocities between 25 and 100 degrees/s were the most effective. No cells responded to a stationary stimulus. 5. Single-spot targets were the most effective stimuli. Stimulus size was a more important parameter than stimulus configuration. Many cells had inhibitory regions outside of their excitatory fields. 6. The excitatory receptive fields of dorsolateral pontine cells were very large (median, 1,100 deg2). 7. Nearly all receptive fields were centered in the contralateral visual hemifield, and 91% of the dorsolateral visual cells were activated from either eye. 8. We conclude that the visual cells in the dorsolateral nucleus have receptive-field properties that are similar to those of cells in the superior colliculus. The preference of dorsolateral cells for single-spot targets contrasts strongly with the multiple-spot preference of medial pontine cells, which receive their input from visual cortex.


2004 ◽  
Vol 91 (6) ◽  
pp. 2484-2500 ◽  
Author(s):  
Seiji Ono ◽  
Vallabh E. Das ◽  
Michael J. Mustari

The dorsolateral pontine nucleus (DLPN) and nucleus reticularis tegmenti pontis (NRTP) are basilar pontine nuclei important for control of eye movements. The aim of this study was to compare the response properties of neurons in DLPN and rostral NRTP (rNRTP) during visual, oculomotor, and vestibular testing. We tested 51 DLPN neurons that were modulated during smooth pursuit (23/51) or during motion of a large-field visual stimulus (28/51). Following vestibular testing, we found that the majority of smooth pursuit–related neurons in DLPN were best classified as gaze (13/23) or eye velocity (7/23) related. Only a small percentage (3/51) of DLPN neurons responded during vestibular ocular reflex in the dark (VORd). We tested rNRTP neurons as described above and found the majority of neurons (35/43) were modulated during smooth pursuit or during motion of a large-field stimulus only (4/43). A significant proportion of our rNRTP gaze velocity neurons (10/18) were also modulated during VORd. We found that the majority of smooth pursuit related neurons in rNRTP were best classified as gaze velocity (18/35) or gaze acceleration (11/35) sensitive. The remaining neurons were classified as eye position or eye/head related. We used multiple linear-regression modeling to determine the relative contributions of eye, head and visual inputs to the responses of DLPN and rNRTP neurons. Our results support the suggestion that both DLPN and rNRTP play significant roles not only in control of smooth pursuit but also in control of gaze.


2005 ◽  
Vol 93 (1) ◽  
pp. 108-116 ◽  
Author(s):  
Seiji Ono ◽  
Vallabh E. Das ◽  
John R. Economides ◽  
Michael J. Mustari

The dorsolateral pontine nucleus (DLPN) and nucleus reticularis tegmenti pontis (NRTP) comprise obligatory links in the cortico-ponto-cerebellar system supporting smooth pursuit eye movements. We examined the response properties of DLPN and rNRTP neurons during step-ramp smooth pursuit of a small target moving across a dark background. Our neurophysiological studies were conducted in awake, behaving juvenile macaques ( Macaca mulatta). We used multiple linear-regression modeling to estimate the relative sensitivities of neurons to eye parameters (position, velocity, and acceleration) and retinal-error parameters (position, velocity, and acceleration). We found that a large proportion of pursuit-related DLPN neurons primarily code eye-velocity information, whereas a large proportion of rNRTP neurons primarily code eye-acceleration information. We calculated the relative decrease in variance found when using a six-component model that included both eye- and retinal-error parameters compared with three-component models that include either eye or retinal error. These comparisons show that a majority of DLPN (14/20) and rNRTP (17/19) neurons have larger contributions from eye compared with retinal-error parameters ( P < 0.001, paired t-test). Even though eye-motion parameters provide the strongest contributions in a given model, a significant contribution from retinal error was often present (i.e., >20% reduction in variance in 6-component model compared with 3-component models). Thus our results indicate that the DLPN plays a larger role in maintaining steady-state smooth pursuit eye velocity, whereas rNRTP contributes to both the initiation and maintenance of smooth pursuit.


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