Download Visual signals in the dorsolateral pontine nucleus of the alert

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
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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
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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.
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Received March 9, 1983 / Accepted September 22, 1983