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Exp Brain Res (1984) 53:473-478 Brain Research 9 Springer-Verlag 1984 Research Note Visual Signals in the Dorsolateral Pontine Nueleus of the Alert Monkey: Their Relationship to Smooth-Pursuit Eye Movements* D.A. Suzuki and E.L. Keller Smith-Kettlewell[nstitule of Visual Sciences, 2232 Webster Strect, San Francisco,CA 94115, USA Summary. The visual properties of 77 dorsolateral pontine nucleus (DLPN) cells were studied in two alert monkeys. In 41 cells, presentation of a moving random dot background pattern, while the monkeys fixated a stationary spot, elicited modulations in discharge rate that were related either to (i) the velocity of background motion in a specific direction or to (ii) only the direction of background movement. Thirty-six DLPN cells exhibited responses to small, 0.6-1.7 deg, visual stimuli. Nine such ceils exhibited non-direction selective receptive fields that were eccentric from the fovea. During fixation of a stationary bluish spot, the visual responses of 27 DLPN cells to movement of a small, white "test" spot were characterized by two components: (1) as the test spot crossed the fovea in a specific direction, transient velocity-related increases in discharge rate occurred and (2) a maintained, smaller increase in activity was observed for the duration of test spot movement in the preferred direction. This DLPN activity associated with small visual stimuli was also observed during smooth-pursuit eye movements when, due to imperfect tracking, retinal image motion of the target produced slip in the same direction. These preliminary results suggest that the DLPN could supply the smooth-pursuit system with signals concerning the direction and velocity of target image motion on the retina. Key words: Dorsolateral pontine nucleus - Visual responses - Retinal slip velocity - Smooth-pursuit eye movements- Monkey * This study was supported by NSF Grant BNS-8107111, Nil! Grant R01 EY04552-01, and the Smith-KettlewellEye Research Foundation Offprint requests to: David Suzuki, Ph.D., at the Jules Stein Eye Institute, UCLA School of Medicine, Los Angeles, CA 90024, USA Introduction The elucidation of the neural substrates for sensory to motor signal transformations has been a prominent goal in motor physiology in general and in oculomotor studies in particular. Progress has been made in clarifying the role of vestibular and visionrelated single-cell activity in the generation of the vestibuloocular reflex, saccadic (fast) eye movements and optokinetically elicited slow eye movements. In contrast, knowledge of the sensorimotor transformations involved with the regulation of voluntary, smooth-pursuit eye movements remains limited. Anatomical results implicate the dorsolateral pontine nucleus (DLPN) both as a major terminus for converging, descending pathways from visionand visuomotor-related structures and as a major source of efferents to cerebellar regions involved with ocular motility. In the primate, tecto-pontine (I/arting 1977), cortico-pontine (Brodal 1978; Wiesendanger et al. 1979; Glickstein et al. 1980), and pretecto-pontine afferents (Weber and Harting 1980) to the DLPN have been demonstrated. Furthermore, horseradish peroxidase studies indicate that the DLPN projects to vermal lobules VI and VII (Brodal 1979) and to the flocculus (Langer et al. 1980; Brodal 1982) which are both cerebellar structures that figure prominently in oculomotor functions (Lisberger and Fuchs 1978; Noda and Suzuki 1979a, b; Kase et al. 1980; Miles et al. 1980; Suzuki et al. 1981; Suzuki and Keller 1982; Waespe and Henn 1981). While anatomical evidence implicates the DLPN in the pontocerebellar control of oculomotor behavior, knowledge of the physiological characteristics of DLPN cells is limited to an acute cat preparation (Mower et al. 1979) and is non-existent in the monkey. The present study sought to determine the vision-related properties of DLPN neurons in the alert monkey. Our results suggest that the DLPN could supply the 474 D.A. Suzuki and E.L. Keller: Visual Signals in the Dorsolateral Pontine Nucleus of the Alert Monkey 300- BG MOVEMENT co A. 200- C. (_9 < -rL.) tO a 3001 ~;~i~i!~iiii 100- 200 ] 0 R10 CNT L10 CNT R10 100- TS POSITION L10~ o_ o~ 3001 ~ RIO~ ~ ~ _ i..t.i 0- .-,,, B. 20o1 D. tY (.S. 150- 09 kl.I 100- r,." 100' e,,- < -i(,.) co c'., 0R10 50 CNT L10 CNT R10 TEST SPOT POSITION (DEG) , , , , 10 20 30 40 50 PEAK TEST SPOT VELOCITY (DEG/SEC) smooth-pursuit eye movement system with signals concerning the direction and velocity of target image motion on the retina. Methods Extracellular activity was recorded in the dorsolateral pontine nucleus of two macaques (Macaca fascicularis and M. radiata). Recording sites within the DLPN were verified by histological examination of focal electrolytic lesions. Eye movements were monitored with the magnetic search coil method (Robinson 1963; Judge et al. 1980). The monkeys' heads were immobilized with respect to the monkey chair and they were trained to fixate a 0.5 deg in diameter, back projected, bluish "fixation spot". Fixation was maintained whether the fixation spot was moving, thereby elicifing smooth-pursuit eye movements, or was stationary as during the presentation of visual stimuli. The visual stimuli were back projected onto a 90-deg square tangent screen and consisted of a random dot background pattern (which filled the screen) and a discrete "test SPOt" that was 1.7 or 0.6 deg in diameter. Results Vision related modulations in DLPN discharge rate were observed in a total of 77 DLPN cells. Although not extensively studied, two additional cells exhibited activity related to smooth-pursuit eye movements, but not to movements of visual stimuli. Of the 77 visually responsive cells, 41 were responsive to large field, random dot background movement, 27 were Fig. 1A-D. Responses of a DLPN cell to discrete spot and background movements. A 1.7 deg (A) or 0.6 deg (B) test spot (white spot) was oscillated at 0.4 Hz + 10 deg as the monkey fixated a reward-related fixation spot (denoted as a cross). The test spot moved across the fixation spot, though for clarity, the fixation spot (cross) is indicated below the line of test spot movement (white spot between arrows). The sinusoidal change in test spot position is illustrated between histograms A and B. Gaze was directed toward the fixation spot at the center of the screen, CNT. Fourteen and 18 cycles of test spot-related activity were sampled with 30 ms bins and averaged in the construction of the histograms in A and B, respectively. C A large field, random dot background pattern was oscillated at 0.4 Hz + 10 deg. Concurrent DLPN activity was sampled with 20 ms bins and averaged over 20 cycles. D Amplitude of the transient response to test spot (0.6 deg) movement at different velocities. Frequency of test spot movement was constant at 0.2 Hz. The spontaneous discharge rate was 20 spikes/s. Unit C21 activated with test spot movement, and 9 were responsive to movements of both large and discrete visual stimuli. The subpopuiations of DLPN cells responding to large field (41) or discrete (27) visual stimuli may' not b e mutually exclusive, since the majority of DLPN cells could not be tested for both responses before isolation was lost. When the monkey fixated a stationary spot during movements of a random dot background pattern, two types of visual responses were observed. In a majority of the DLPN cells responsive to movements of the background pattern, discharge rate increased with increases in the velocity of background motion in "preferred" directions. During sinusoidal movement of the background pattern, the response of this type of cell appeared half-wave rectified with sinusoidal modulation of discharge rate occurring only for background movement with a component in a specific, "preferred" direction. Other DLPN cells were only responsive to the direction of background motion and were not sensitive to the velocity of background generated retinal image motion over the range tested (10to 50 deg/s). Such units responded with a sustained, nonsinusoidal increase in discharge rate for sinusoidal background movement in the preferred direction (Fig. 1C). Responses to discrete visual stimuli were elicited when the monkeys, in an otherwise dark environment, were required to fixate a stationary, bluish D.A. Suzuki and E.L. Keller: Visual Signals in the Dorsolateral Pontine Nucleus of the Alert Monkey A I I III llllllllililllNtl IIif IIIIIUII spikes 475 § 2 T: target position E: eye position S: retinal image 20 ~ E ' 1 sec 20 slip velocity sec N down S; ~ down S, up up/no S, B c I IIULI IIIIIIIIIIIIImlLIIIIIINIIILIUIII IIIIIIIIIIIIIIIL I lilllltllllllllll LIII Nil lull I IIIIIllllllll IILIIINIIIIIIIIII 111111111111111 Ill IIIIIIIIlUlIlUlll IIII D E I I11 IIIILIIIllnllllll I I IIIIIIltlIUII IIIli It111tllI Ill pursuit down pursuit lll[I [ IIIIIIItlIIIIIIIItlIUIIII III I I IIIIIIIIIlUll II II{lllllUIIIIIInllll II IIIIInll I Pig. 2A-E. Responses of a DLPN cell during smooth-pursuit eye movements. A-C constant velocity, vertical smooth pursuit, 0.4 Hz + 10 deg. D and E sinusoidal vertical smooth pursuit, 0.4 Hz + 10 deg. Upper traces, discriminated spike occurrence divided by two. T, target position. E, vertical eye position. Upward target or eye position is up. Vertical 20 deg calibration bar is for T and E; one sec bar valid throughout figure. S, retinal image slip velocity with downward slip shaded in. Dotted line, zero retinal slip velocity. Filled arrow, denotes occurrence of downward retinal slip during upward pursuit. Open arrow, denotes occurrence of zero or upward retinal slip during downward smooth-pursuit eye movements. Unit L14B spot (shown as a cross in Fig. 1A and B) during movements of a white test spot. The test spot moved across the fixation spot, and consequently the fovea (though in Fig. 1A and B, the fixation spot is shown below the line of test spot movement for purposes of clarity. Both fixation and test spots were visible during cross-over). The responses of 9 of the 36 DLPN cells responsive to discrete visual stimuli were non-direction selective and had receptive fields that were eccentric from the fovea. For reasons of brevity, these cells will not be considered in this short communication. The test spot elicited responses of 27 DLPN cells appeared to have two components. Movement of the test spot in the preferred direction was associated with (i) a maintained increase in discharge rate and (ii) a transient burst of activity (Fig. 1A and B). The unit represented in Fig. 1 exhibited responses to movements of both large field and discrete visual stimuli. The maintained component of the test spot response (Fig. 1A and B) resembled the sustained response to background movement (Fig. 1C), since the direction of visual stimulus movement appeared to be the primary stimulus-related information conveyed. The transient component of the response to test spot movement appeared to be due to stimulation of a small, foveaUy centered receptive field. Movement of the retinal image was required, since firing rates were similar for intersaccadic periods in the dark and during fixation of the stationary fixation spot. In Fig. 1A and B, test spot position was plotted on the abscissas. Since gaze was continuously directed toward the fixation spot at the center of the screen (CNT), the position of the fovea 476 D.A. Suzuki and E.L. Keller: Visual Signals in the Dorsolateral Pontine Nucleus of the Alert Monkey corresponded to CNT. When the test spot crossed the fovea (CNT) in the preferred direction (right), a burst of discharges was observed with a 150 ms delay (Fig. 1A and B). The magnitude of the transient response was related to the size of the test spot stimulus. For a 1.7 deg test spot moving at about 0.4 Hz + 10 deg, the amplitude of the burst was 283 spikes/s (Fig. 1A). When a 0.6 deg test spot was moved at the same frequency and amplitude, the cell exhibited a peak discharge rate of 176 spikes/s (Fig. 1B). Within the limits tested, the amplitude of the transient, test spot elicited response was also related to the velocity of retinal image motion. Since the monkeys' heads were stationary and eye movements suppressed during fixation of a stationary fixation spot, the velocity of visual stimulus movement approximated retinal image or "slip" velocity. When the small, 0.6 deg diameter test spot was oscillated with different amplitudes at 0.2 Hz, the magnitude of the transient response generally increased with increases in peak stimulus velocity (Fig. 1D). The persistence of the direction selective DLPN activity was investigated during smooth-pursuit eye movements. For a unit exhibiting test spot-related responses similar to those of the cell in Fig. 1, the receptive field of the transient component, though not studied in detail, was found to be less than 5 deg in diameter, centered on the fovea, and selective for downward test spot movement. The discharges of this unit were also studied during smooth-pursuit eye liaovements and are illustrated in Fig. 2. As shown in Fig. 2A, as the target (T) started to move down and before the eyes (E) started to track, there was a resultant downward slip velocity (S, shaded region) which was associated with an increase in DLPN activity. With a latency on the order of 100 ms, the discharges were suppressed following the turn-about in target direction and the resultant upward slip velocity (non-shaded region above dotted line). During tracking in the non-preferred direction, there was a short period where upward eye velocity exceeded target velocity resulting in a relative downward slip velocity (filled arrow, Fig. 2A) and firing of the cell. Since the eye~ were moving i:n the non-preferred direction when the unit discharged, eye movements per se do not appear to be the cause for the modulations in discharge rate observed during smooth pursuit. Similar instances of the unit firing for relative downward slip during upward eye and target movements are shown in Fig. 2B and C (filled arrows). In Fig. 2C and E are shown examples where downward eye velocity equalled or exceeded target velocity resulting in zero or upward retinal slip velocity (open arrows) and decreases in the discharge rate. Out of the 27 cells responsive to test spot movement, nine were tested for activity during smooth pursuit. All nine exhibited responses similar to the unit in Fig. 2. Although more quantitative experiments are planned, the preliminary results indicate that the DLPN could supply the smoothpursuit eye movement system with information concerning retinal image slip velocity and direction during pursuit. Discussion The dorsolateral pontine nucleus (DLPN) may participate in a cortico-ponto-cerebellar system that is intimately involved with oculomotor functions. DLPN afferents from striate; prestriate, and temporal cortices (Brodal 1978; Fries 1981) suggest a role in visual signal processing, while inputs from the posterior parietal cortex (Glickstein et al. 1980; Wiesendanger et al. 1979) and area 19 suggest the availability of information concerning target selection (Mountcastle et al. 1975; Robinson et al. 1978; Fischer and Boch 1981). Some functional convergence is indicated if the convergence of inputs from different visual cortical areas onto single pontine neurons in the cat (Fries and Albus 1980) also occurs in the monkey. The observation of direction selective visual responses in the DLPN is consistent with the corticopontine connection from middle temporal cortex (Fries 1981), which contains a preponderance of direction selective cells (Zeki 1974; Van Essen et al. 1981; Baker et al. 1981). On the efferent side, it is notable that the DLPN responses to random dot background movements are similar to mossy fiber activity in vermis-VI, VII and the flocculus (Suzuki et al. 1981; Noda 1981), consistent with the anatomical evidence for DLPN projections to these two cerebellar structures (Brodal 1979, 1982; Langer et al. 1980). Possible contributions to the regulation of optokinetically elicited slow eye movements await further study. The character of the response to discrete spot movements suggests the convergence of inputs from two functionally different populations of afferent neurons. The maintained response could convey direction information from a large receptive field, while the stronger transient discharge could convey both direction and retinal slip velocity information from a more discrete receptive field centered on or near the fovea. Such information would be useful in the regulation of smooth-pursuit eye movements. The former, sustained response could be a saturated signal informing the oculomotor system that a target D.A. Suzuki and E.L. Keller: Visual Signals in the Dorsolateral Pontine Nucleus of the Alert Monkey is eccentric from the fovea and moving in a specific direction. Upon foveation and tracking of the moving target, slippage of the target image on the fovea would activate the transient component of the DLPN visual response. Consistent with this possibility was the target-elicited, retinal image slip-related, DLPN activity observed during smooth-pursuit eye movements (Fig. 2). The DLPN could provide the smoothpursuit system with the retinal slip velocity component of an internal neural correlate of target velocity in space. This target velocity signal plays an important role in models of the smooth-pursuit control system (Young 1971; Robinson 1976) and its existence has been implicated in a recipient of DLPN afferents, i.e., the cerebellar vermis, lobules V! and VII (Suzuki et al. 1981). Both background and test spot-related activities were observed in some DLPN cells (Fig. 1A and C), but interactions between these two classes of responses were not extensively tested in these initial experiments. A normal characteristic of the primate smooth pursuit system is, of course, the ability to track a small spot against a patterned background and studies of the interactions present in DLPN cells during such tracking will be conducted in the near future. Dedication. This paper is dedicated to Dr. Kitsuya Iwama, Emeritus Professor of Osaka University Medical School, on his retirement. The first author is grateful for the inspiration and guidance that Dr. Iwama provided during the early part of the author's education in neurophysiology. Acknowledgements. It is a pleasure to thank Drs. W. Crandall, M. Mackeben, and K. Nakayama for their valuable criticism during the preparation of this manuscript. References Baker JF, Petersen SE, Newsome WT, Allman JM (1981) Visual response properties of neurons in four extrastriate visual areas of the owl monkey (Aotus trivirgatus): a quantitative comparison of medial, dorsomedial, dorsolateral, and middle temporal areas. J Neurophysiol 45:397-416 Brodal P (1978) The cortico-pontine projection in the rhesus monkey. Origin and principles of organization. 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J Comp Ncurol 199:293-326 Waespe W, Henn V (1981) Visual-vestibular interaction in the flocculus of the alcrl monkey. II. Purkinje cell activity. Exp Brain Res 43:349-3(-,0 478 D. A, Suzuki and E.L. Keller: Visual Signals in the Dorsolateral Pontine Nucleus of the Alert Monkey Weber JT, Harting JK (1980) The efferent projections of the pretectal complex: an autoradiographic and horseradish peroxidase analysis. Brain Res 194:1-28 Wiesendanger R, Wiesendanger M, Ruegg DG (1979) An anatomical investigation of the corticopontine projection in the primate. (Macaca fascicularis and Saimiri sciureus). - II. The projection from frontal and parietal association areas. Neuroscience 4:747-765 Young LR (1971) Pursuit eye tracking movements. In: Bach-y- Rita P, Collins CC, Hyde JE (eds) The control of eye movements. Academic Press, New York, pp 42%444 Zeki SM (1974) Functional organization of a visual area in the posterior bank of the superior temporal sulcus of the rhesus monkey. J Physiol (Lond) 236:54%573 Received March 9, 1983 / Accepted September 22, 1983