Pre-motor single unit activity in the monkey brain stem correlated with eye velocity during pursuit

210

Brain Research, 184 (1980) 210--214 © Elsevier/North-Holland Biomedical Press

Pre-motor single unit activity in the monkey brain stem correlated with eye velocity during pursuit

ROLF ECKMILLER* and MANFRED MACKEBEN Smith-Kettlewell Institute of Visual Sciences, 2232 Webster Street, San Francisco, Calif. 94115 (u.s.A.)

(Accepted October 25th, 1979) Key words: pre-motor unit activity - - brain stem oculomotor system - - eye velocity - - pursuit eye

movements

Among the various classes of supra-nuclear neurons in the oculomotor system of the monkey which have been associated with the generation of saccadic or vestibularly-induced eye movements (EM), a class specifically concerned with the control of pursuit eye movements (PEM) has not yet been described3-L In this paper we describe some features of single neurons, the activity of which is correlated with eye movements specifically during PEM in a way that one would expect of neurons linking the visual to the oculomotor system. The techniques used in this study are identical with the ones described recently 2. In brief: single unit recordings were performed by means of tungsten microelectrodes in 3 monkeys (2 male Macaca fascicularis and 1 female Macaca mulatta) of 3-4 kg weight. A head gear and lucite chamber were implanted over a trephine hole in the vertex of the skull. In one animal EM were measured as horizontal and vertical DCelectro-oculograms using surface electrodes (Hellige). The other two monkeys had Ag-AgC1 electrodes (In Vivo Metric Systems, Healdsburg, California) implanted into the bone of the outer canthi of the orbits and between both eyes, so that horizontal EM of either eye could be measured independently, with very small drift (typically less than l°/min) and a gain of about 17 #V/degree. All 3 monkeys were trained to pursue a light spot with a diameter of 4 min arc in the horizontal plane at a distance of 150 cm. All relevant signals were recorded on instrumentation tape and in parallel on a jet ink writer (Siemens Mingograf 800). Both recording systems, including the pre-amplifiers, had cut-off frequencies above 1 kHz. For further analysis the impulse trains of single neurons were converted into time function of the instantaneous impulse rate I R (t). The results are based on the analysis of 42 neurons 3. They appear to form a class which has not been described so far. These neurons were clearly distinguishable from motoneurons in that their I R was typically independent of the eye position. The * Present address: Institut ffJr Allgemeine Biologie, Abteilung Biokybernetik, UniversitAt Dfisseldorf, D-4000 D/isseldorf 1, G.F.R.

211 localization of these neurons was based entirely on stereotaxic measurements relative to the abducens nucleus during at least 20 electrode tracks per monkey. F o r this purpose the microelectrodes were always m o v e d vertically (perpendicular to the horizontal plane o f the stereotaxic coordinate system) t h r o u g h the brain stem o f the monkey, which sat upright in the primate chair with its head fixed. In order to find these neurons, the electrode had to pass first t h r o u g h the abducens nucleus which is clearly recognizable by its characteristic activity pattern. The neurons were encountered by advancing the electrode tip further d o w n into a region 0.5-1.5 m m inferior to the abducens nucleus. Correlating these stereotaxic measurements and the corresponding neural activity, there was a 'silent' region of about 0.5 m m just below the inferior border o f the abducens nucleus. The recordings were probably made from cell somata as inferred f r o m the frequent occurrence o f long trains o f injury potentials.

M12-145

I, I E I11 lllllll liiiiiiiiii

i

Illlllll ,1,I

.-, _

"t,__--~

_..

i~'rll,~l.

........

I~illllllll~lil

J

i

L_.._ M12-224

i

iii

iiiii II I

i

i ii iiii

iiiii L.--

M12-823

I

1I

I1111

IIlI

iiiili

M16-380

i i

_..s

i i

i i iiiiii

\

I

ii

i i iiiil k_

1 (sec)

Fig. 1. Neural activity patterns of 4 representative neurons during spontaneous saccadic eye movements together with the horizontal movement (right is up) of the ipsilateral eye. Remarkable features of the different neurons: M12 - 145, presentation of a new visual object into the right field of gaze (second half of the record) led to a loosely coupled increase of IR; M12 - 224, no clear correlation between IR and the spontaneous EM; M12 - 823, IR was loosely associated with ipsilateral saccades but continued well after the end of those saccades.

212 M12-145

iiiiiiiiiiiiiiiiii iiii iiii iiiiiiii+~iiiri+liiiiiiiiiiii ii

l l',liiiiii~iiiiii+~iiiIlllll

iiiiiiiiiiii~liiiiiiiiiii i

ii

1.0 Hz

M12-224

iiii!iiiiiijiliiiiiiiiJiii [

i[iiiiiiiiiiiiiiiiiiii+ilil

ItllllllllllllIll[

~11[[I ISTIMULUS

OFF

I I

...--- ..:

.~.. -'-'::

1.2 Hz

M12-823

iiiJjli ii i i

iihi ]Jill

iiiiiii iii[ii]

i iiiiiiiii

1.0 Hz

M16-380

i iiiiHiiiiJ

ii

J i jiiiiiiiiiflii iii;i

I1[!

!!11

tiiiiiiiiiii

ill

I

[[i[i[iii

I

I

0.85 Hz v e s t i b u l a r

Fig. 2. Activity pattern of the same 4 neurons as in Fig. 1 during pursuit eye movements together with the horizontal movement of the ipsilateral eye. M12 - 224: during and after an episode of stimulus disappearance of 800 msec (marked as 'stimulus off') slow eye movements were performed which gradually deviated from the time course of proper pursuit (interrupted curve) while the neuron still increased its IR during movement to the right. M16 - 380: upper pair of traces during PEM with head fixed, lower pair of traces during rotation of the monkey around the vertical axis while trying to keep the stationary light spot on the fovea. Note the seemingly uncorrelated activity in the latter case.

It was also a p p a r e n t from the b a c k g r o u n d activity that they were clustered i n a small region. The following characteristic features of these n e u r o n s (as exemplified i n Figs. 1 a n d 2), together with their c o m m o n location, seem to justify the suggestion that they indeed constitute one class: (1) Their activity patterns d u r i n g spontaneous E M are only loosely, if at all, coupled with E M parameters (Fig. 1), a n d they sometimes can be

213 activated by arousing stimuli, particularly by visual objects of interest. During sinusoidal PEM, however, the following features appear: (a) their IR increases and decreases during movements into one direction about in phase with the stimulus- and eye-velocity and goes to 0 during PEM in the opposite direction (Fig. 2); (b) the increases of IR always occur during ipsilateral PEM, i.e. neurons inferior to the right abducens nucleus reach their maximum IR during PEM to the right and vice versa; (c) the correlation between IR and PEM velocity is independent of the absolute eye position: the maximum IR at a given PEM frequency does not change, when the midposition of the sinusoidal movement ( ± 10°) is shifted from the usual zero to 10° right or to 10° left; (d) when the pursued light spot suddenly disappears and the monkey continues for a while to perform smooth EM (see ref. 2), the IR is still correlated with the movement of the eye (see neuron M12-224 in Fig. 2); (e) when the light spot is kept stationary, while the monkey is rotated sinusoidally around the vertical axis and performs compensatory smooth EM in order to keep the stimulus on the fovea, the correlation between IR and eye velocity seems to be disrupted. In this case of conflict between the visual and the vestibular input, some neurons are silent or generate a low irregular IR (see bottom traces of neuron M16 -

A tsol

,

B

IR max[Imp/sec]

1 ~ O(Stim'-IRmx)Ideal 15(

1! .......

12(

9(

6(

30'

6 6:3

0!s

. . . .

1~0 ....

,"s'("~

.

.

.

.

.

.

.

.

Fig. 3. A: relationship of the phase angle o (extreme stimulus position minus maximum impulse rate) and stimulus frequency during PEM for 11 representative neurons. Phase angles were measured using the graphically determined maxima of IR (t). Each dot is the mean of 5 values. Hatched band in the lower part of the diagram: range of phase angles of oculomotor motoneurons. Dashed horizontal line at 90 °: ideal values for o if the maximum IR were always in phase with maximum velocity. B: relationship between maximum impulse rate IRmax and stimulus frequency during PEM for the same 11 neurons as in A. Each dot represents the mean of 5 values. The numbers 1-4 refer to the 4 neurons in Fig~. 1 and 2 in the order in which they are shown there from top to bottom.

214 380 in Fig. 2); others are even slightly activated during contralateral smooth EM (ipsilateral head rotation). The dependence of maximum I R and of its phase angle relative to the extreme stimulus position on the PEM frequency shows considerable variation among different neurons. Fig. 3A demonstrates for a set of 11 neurons that some of them lead or lag the maximum stimulus velocity by up to 50 ° . For comparison, the range of phase angles for oculomotor motoneurons during PEM under similar experimental conditions was added to this diagram 2. As shown in Fig. 3B, for some neurons the maximum I R increases, for others it stays constant, or even decreases, with increasing frequency of stimulus movement. The described neurons were found to be specifically correlated with horizontal PEM in the phase range of eye velocity in one direction, but only loosely coupled during spontaneous EM. Their location corresponds to those regions in the vicinity of the abducens nucleus, where smooth EM have been elicited by electrical stimulation in the monkey 1. Since eye and head movements are usually superimposed during pursuit of a slowly moving visual object 6, the corresponding neural input to the oculomotor system presumably also controls neck muscles, even if the head movement can only be intended rather than executed. We observed in a few cases that the monkey with fixed head moved its shoulders slightly during PEM, as if it wanted to turn its body into the direction of the moving light spot. The activity of these neurons could, however, not be modulated by actively turning the trunk of the monkey (by about ± 20 °) around the vertical axis relative to its fixed head. This work was supported in part by Grant Ec 43/5 awarded by the Deutsche Forschungsgemeinschaft, by Grants 5 R01 EYO1474 and 5 P30 EYO1186, awarded by the National Institute of Health, and by the Smith-Kettlewell Eye Research Foundation. The authors are grateful to Dr. P. Bach-Y-Rita, who kindly invited them to continue and complete this project at the Smith-Kettlewell Institute of Visual Science and provided extensive support. The assistance of Ms. K.-U. Florian with the data analysis is also gratefully acknowledged.

1 Cohen, B. and Komatsuzaki, A., Eye movements induced by stimulation of the pontine reticular formation: evidence for integration in oculomotor pathways, Exp. NeuroL, 36 (1972) 101-117. 2 Eckmiller, R. and Mackeben, M., Pursuit eye movements and their neural control in the monkey, Pfliigers Arch. ges. PhysioL, 377 (1978) 15-23. 3 Eckmiller, R. and Mackeben, M., Velocity coded neurons: a new class of pre-motor neurons in the primate oculomotor system during pursuit, Neurosci. Abstr., 4 (1978) 162. 4 Fuchs, A. F. and Luschei, E. S., Unit activity in the brainstem related to eye movement, Bibl. OphthaL, 82 (1972) 17-27. 5 Keller, E. L., Participation of medial pontine reticular formation in eye movement generation in monkey, J. NeurophysioL, 37 (1974) 316-332. 6 Lanman, J., Bizzi, E. and Allum, J., The coordination of eye and head movement during smooth pursuit, Brain Research, 153 (1978) 39-53.