CENTRAL MESENCEPHALIC RETICULAR FORMATION (cMRF) NEURONS DISCHARGING BEFORE
AND DURING EYE MOVEMENTS.
Waitzman, David M., Bernard Cohen and Valentine L. Silakov.
Department of Neurology, VA Connecticut, Newington Campus and The
University of Connecticut Medical Center, 555 Willard Ave, Newington, CT
06111, Mount Sinai School of Medicine, Department of Physiology and
Biophysics, Annenberg, Building, Rm 21-74, New York, NY 10029.
APStracts 2:0320N, 1995.
SUMMARY AND CONCLUSIONS
1) 120 neurons were recorded in the central Mesencephalic Reticular Formation
(cMRF) of four rhesus monkeys, trained to make visually guided and targeted
saccadic eye movements (EMs). EMs were recorded with the head fixed, using
electroculography (EOG) or subconjunctival scleral search coils. 76% (92/120)
of cells discharged before and during contraversive visually guided or
targeted rapid eye movements and 76% of these (70/92) responded during
contraversive spontaneous saccades in the dark. cMRF neurons had large
contraversive movement fields and either a high (> 10 spks/sec) or low
background level of spontaneous activity in the dark. The optimal movement
vectors (i.e., saccades with greatest response) were predominantly horizontal,
although many had a vertical component. Cells with optimal movement vectors
within +/- 25 degrees of pure vertical were more rostral in the MRF and were
excluded from the analysis. 2) A subgroup of cMRF neurons (31 of 92) which
discharged before and during visually guided saccades were examined for visual
sensitivity. Slightly less than half of these cells (42%, 13/32) were
visuomotor units, i.e., they responded to visual targets in the absence of eye
movement. The other 58% (N = 18) did not discharge during the visual probe
trial; they were movement-related cells. 3) Microstimulation (threshold 40 -
60 [mu] A at 333 Hz) at the sites of many of these cMRF neurons produced
contraversive saccadic eye movements at short latency (< 40 msec). The
amplitude and direction of the elicited saccades were similar to the optimal
movement vector determined from single unit recording. This suggested that
cMRF cells recorded at the same locus of electrical microstimulation
participated in the network responsible for the production and control of
rapid eye movements. 4) The 92 saccade-related neurons were divided into two
groups on the basis of their background discharge rate. Firing rates for both
low background (28%, N=26) and high background (72%, N=66) cells increased
about 30 msec before contraversive saccades and reached a peak discharge just
before saccade onset. The low background neurons had either no activity or
generated a few spikes just before the end of ipsiversive saccades. The steady
rate of discharge ( > 10 spikes/sec) of high background neurons was inhibited
from about 20 msec before ipsiversive saccades until just before saccade end.
5) Cells were also subdivided based on how their discharge rates fell at the
end of saccades. Clipped cells (38%, N=35) had activity which fell sharply
with saccade offset. Partially clipped cells (62%, N=57) had persistent firing
in the 100 msec following the saccade which was > 20% higher than the firing
during the 100 msec before the saccade. 6) Latencies between the 90% point on
the rising edge of the peak discharge and the start of the saccade were 5.3 ms
or less for eye movement related cells in two monkeys. Longer latencies (11 to
19 ms) were found when measured between the 10% point on the rising edge of
the peak discharge and saccade onset. These latencies were equal to or shorter
than those obtained for eye movement related burst neurons in the intermediate
and deep layers of the superior colliculus analyzed similarly. Delays between
the peak discharge and peak eye velocity were 13.6 - 15.1 ms for the same
group of cMRF EM related cells. These were significantly shorter than the
delays measured for EM neurons in the SC of one of the monkeys. These findings
suggest that the buildup discharge of cMRF neurons occurs early enough before
saccades may to contribute to saccade triggering. The peak discharge, however,
occurs coincidentally or after the burst in the SC suggesting that this
portion of the discharge serves a function other than saccade triggering. 7)
The number of spikes in bursts associated with eye movement was correlated
with saccade parameters. 23 of 31 cells had activity within the 22 ms interval
before saccade onset that was associated with the direction of the upcoming
saccade ( r 2 > 0.3). In 13 of these 31 neurons, the number of spikes was also
correlated with horizontal saccade amplitude. When the counting interval
included just the spikes during the saccade (8 ms before saccade onset to 8 ms
before saccade end), the number of cells associated with horizontal saccade
amplitude increased to 19. This suggests that activity before the saccade can
provide information about saccade direction and in some neurons, eye
displacement. In others a relationship to eye displacement became evident only
when spikes during the saccade were included. This analysis distinguished the
portion of the discharge which influenced saccade triggering and direction,
from that which modulated saccade displacement and velocity. The former could
proved feedforward activity to the PPRF or omnipause neurons, and the latter
feedback, probably via the superior colliculus. 8) Latency, saccade metric,
and phase plane analyses suggest that there are at least three different
groups of cMRF neurons. The temporal pattern of the cMRF discharge was related
to eye displacement (difference between current and desired eye position) in
8/29 cells, to eye velocity in 15/29 cells, and to both eye displacement and
velocity in the remaining 6 cells. An eye displacement signal has been
postulated to explain how the SC can remain aware of the current position of
the eyes during a saccade. Some cMRF cells (in the midbrain) may participate
in an ascending stream of activity from the PPRF (in the pons) to the SC (in
the midbrain) coding current horizontal eye displacement. cMRF neurons related
to eye velocity may also provide feedback of current eye velocity to the SC.
9) A model of the cMRF and the superior colliculus in the control of saccades
is presented. The model simulated the physiologic evidence for an almost
linear decline in discharge of some individual cMRF neurons with radial error
(difference between current and desired eye displacement). We propose that the
cMRF eye displacement neurons participate in a servo loop that provides a
current horizontal eye displacement signal to the SC. Feedback to the SC via
cMRF eye velocity neurons could also be important in the generation of
straight trajectories of oblique saccades.
Received 10 May 1995; accepted in final form 26 October 1995.
APS Manuscript Number J254-5.
Article publication pending J. Neurophysiol.
ISSN 1080-4757 Copyright 1995 The American Physiological Society.
Published in APStracts on 30 November 95