The Convergence of Vestibular and Visual Information Onto Neurons of the Vestibular Nuclei in Alert Monkeys (Macaca Mulatta)

THE CONVERGh'NCE OF VESTIBULAR AND VISUAL INFORMATION ONTO NEURONS OF THE VESTIBULAR NUCLEI IN ALERT MONKBYS (MACACA MULATTA) W. Waespe, V. Henn Neurologische Klin1k, Universi tilt ZUrich, 8091 ZUrich, Switzerland

SWIIIII8.ry: Single neuron recordings were taken from the vestibular nuclei of alert monkeys. Neurons were tested during vestibular stimulation (ro~ation about a vertical axis in the dark); visual stimulation (rotation of a !Striped cylinder around the stationary monkey in the light); and combined visual-vestibular stimulation (rotation of the monkey in the light). If vision is allowed, all vestibular neurona exh.i bi t activation even during constant velocity rotation, thus greatly extending the working range of the central vestibular system.

Introduction:

The peripheral vestibular system and the eye mus-

cles are basically interconnected by a three neuron arc. The first neuron transmits information from the end organ, the semicircular canals and otoliths, to neurona in the vestibular nuclei. These second order neurons project to the motoneurone of extraocular muscles, which move the e7es. The vestibular end organs can only me..ur8 acoeleration. Motoneurone need not onl7 1ntoruUOIl iUIoIlt ho" to move the e7", but the7 need cOIltiDuoua input to hold the eyes in the ne" peei Uon. !hi. requ1ree a double in~t1OD

of the acceleration 8ignal to 71eld a poeition 8ignal

for the ocular motoneurone. A continuous vestibW.ar stilllul.ation leads to nystagmus: slow phase eye movements, the velocities of which are proportional to the vestibular signal, and a fast resetting phase, the velocities of which are a parameter of the

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intercalated neuronal network. If an animal or human being is rotated about a vertical axis in the dark, nystagmus is elicited only during the acceleration ' and deceleration periods. However, for nystagmus to be compensatory, its slow phase should be proportional to velocity of rotation rather than acceleration. If a subject is rotated in the light, nystagmus ' is compensatory, i.e. the addition of vision has the result that the oculomotor system nov receives an input which is proportional to the velocity of motion. Another integration which is necessary to convert the velocity signal in'to a position signal :will not be discussed in this context. We vill focus on how the visual and vestibular signal combine at the level of the vestibular nuclei to yield a signal which

.

is proportional to velOCity of, motion (Waespe & Henn, 1977; BUttner et al., 1977).

Methods:

Single neuron recordings were taken from the vestibular

nuclei of chronically prepared Rhesus monkeys. A head holder, a stereotactically placed ring which could accept a micromanipulator :with the aicroelectrode, and DC electrodes to monitor eye posiUon :were all. iaplaDted UDder anaesthesia. The monkeys eat on a ..no-Gontrollecl

turn~bl.e

aDd . . re rotated in cOllplete darkness

(...Ubular st1aJJ.aUon). Den tu l1pts :were nitched on, striped cyliDder :which totall1 ~ble,

enc~osed

&Dd

a

the an1aa1 on the turn-

:w.. rotated by another seno-controlled IIOtor aroUDd the

s~tionary

IIOnkey (.isual stt.ulation). Combined visual-vestibular

stimulation :w.. performed by rotating the animal within the stationary cylinder. Conflicting visual-vestibular stimuli consisted

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of rotating the animal together with the cylinder, so that inspite of the vestibular acceleration there was no relative movement of the visual surround.

Results :

Neurons in the vestibular nuclei are conveniently olas-

sified as type I cells, which are activated during angular acceleration to the ipsilateral side, and type 11 cells, which are acti- ' vated during acceleration to the contralateral side (Duensing & Schaefer, 1958). Type I cells receive their main input from the semicircular canals on the same side. Type, II cells receive a powerful input from type I cells from the opposite side of the brain stem (Shimazu & Precht, 1966). During vestibular stimulation type I and type 11 cells exhibit a mirror-like activity pattern. A central vestibular neuron which receives its input from the horizontal canal is shown in fig. 1. It exemplifies the typical behavior: During vestibular stimulation in the dark, time constants are always longer than those in the peripheral nerve (longer than 10 sec), visual stimulation leads to a consistent frequency change in every neuron, and visual-vestibular stimulation leads to a combined response. More than 200 neurons from the vestibular nuolei were investigated, and all of them exhibited essentially the s ... behavior. It should be pOinted, out very clearly that none of these nsurons have visual receptive fields. The.. neurons are onl.1 activated, ,when large parts of the visual field are acving, eo that optokinetic D7etasaua can be elioited. Theee neurons see. to carry the rather abstract intoraation ".otion of the vieual surround-. The anatomical pathway fro. the visual e1ste. 'i e unII:nown.

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Fig. 1 A tjpe I neuron during different stimulus conditions. The d01ll reflect instantaneous frequency .of neuron. Spontaneous activity is about 35 imp/sec. The turntable or cylinder velocity for the stimulation period is indicated at the bottom of each column. A: Vestibular stimulation: Rotatiog of the an1JIal in the dark to the right at an end-velocity of 60 /sec on the left and end. velocity of 1200 /sec on the right. Bote the IIJIIIIIl8try of excitation and inhibition during acceleration and deceleration. C: Visual stimulation: Cylinder rotation to the left around the lltationary an1IIal in tlle light. Aa long as the cylinder rotatell, there ill a steady state response of the neuron without ' a rebo~ a~ the end of st1llul.ation. The response ill already saturated at 60 /lIec; there ill nO f~her increase in nsuronal activity at cylinder velooity of 120 /sec. During deceleration of cylinder neuronal activity star~s declining only atter velocity of visual stimulus fell below 60 /sec. B: Visual-vestibular st1llul.ation: Rotation of an1Ml. in the light to the right within stationsry cylinder. During the aoceleratio~ period response is identical to the one seeD during vestibular IItimulation in the dark. Dur~ the Constant velocity period rellponse ill identical to thet seen during visual stimulation. Bote the small rebound during deceleratioD.

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Vestibular stimulation:

The adequate stimulus for the vestibular

system is acceleration. The threshold for reliable activity changes in single vestibular neurons is most often between 0,5 and 20 /sec 2 , although the threshold for the vestibular system as a whole is much lower. In our experiments the fastest acceleration was 10 0 / sec 2 • Some neurons did not show a continuous frequency increase during the whole period of acceleration when it lasted more than 8 sec (fig. 3 B).

Visual stimulation:

The adequate stimulus for the visually media-

ted response in vestibular neurons is velocity. The activating direction for the visual stimulus is always in the opposite direction to that for the vestibular stimulus. All neurons exhibited a reliable response if velocities were higher than 50 /sec. Most neurons became saturated, if velocities were increased beyond 60 0 /sec (fig. 2). This is far below the saturation level of optokinetic nystagmus, which can reach velocities of more than 180 0 /sec in monkeys (Cohen et al. 1977). Most neurons can follow velocity changes of the visual stimulus, if they do not exceed 50 /sec 2 • In conelusion, the visually mediated response to motion enables the vestibular neurons to respond to constant velocities and extends their working range to accelerations from high values down to very low accelerations.

VisUal-vestibular stimulation:

During the period of constant ve-

locity stimulation there is no difference whether the cylinder is

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6-frequency (Hz)

deg/sec

•

•

120

30

n=8 20

60

36 10

18

o" o

18

36

60

120

deg/sec

Fig. 2 Frequency increase of vestibular neuron and nystagmus response during different velocities of visual stimulus. Abscissa is velocity of cylinder, which is rotated around the stationary monkey. Left ordinate is frequency increase (dots) above levels of spontaneous activity. Right ordinate is nystagmus slow-phase velocity (squares)" which is recorded simultaneously. N refers to number of tria!s, from which average values were taken. Note that from 18 to 120 /sec there is a linear increase in slow-phase nystagmus velocity, whereas neuro~ activity shows a linear increase up to a stimulus velocity of 60 /sec and then remains constant. This is the typical behavior found in all neurons: OVer a wide range there is a linear relation between nystagmus velocity and neuronal activity, which always dissociates at high stimulus velocities. .

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A

B

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'21'1_

10,J-_ _ _ __

a-_IHQ

I .,-, -

80·'-.:

20

~

21

40

Frequency increase in a type I neuron (A) and type II neu-

r
averages from 6 trials for each stimulus condition. The velocity 0 the stimulus is the same for eacg display, i.e. acc81era~ion of 5 /sec 2 up to an end-velogity of 90 /sec in A, and 7.5 /sec up to an end-velocity of 128 /sec in B. The horizontal bar at the top indicates the duration of the acceleration, after which stimulus continues to move at constant veloCity. Vestibular stimulation: heavy line. Note the decline of activity after the end of acceleration. Visual stimulation: dotted line. In A, notice the slow increase of activity and the plateau reached at the end of the acceleration period. In B there is the same rise in activity &8 dur~ vestibular stimulation, but the plateau (and also Aevel of saturation) is reached early at a velOCity of about ,50 /sec. Visualvestibular stimUlation: light line, monkey is rotated in the light within the stationary cylinder. In A neuronal activity first follows the same course &8 during vestibular stimulation, then after the end "switches over" to level of aotivity seen in pure visual 8timulation. In B activity first follows the same course seen in vi8ual or vestibular stimulation alone. Whereas both the vestibmlar and the visual response alone seem to saturate during the long aoceleration stimulus, under the coUlii tion of combined st1JauJ.ation activity continues to rise until the end of the acoeleration period. During constant velocity rotation activity 'is the same &8 that seen during visual stimulation.

8

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rotated around the stationary monkey, or the monkey is r.otated within the stationary cylinder. Only the relative velocity between monkey and visual surround ' determines the level of neuronal activity. During the acceleration period the combined rasponse usually follows the same course as during vestibular stimulation alone (figs. 1 and 3 A). For low

accelera~~ons,

which are below

threshold for the vestibular system, the combined response follows the course of the visual stimulus as velocity is the adequate signal for the visual input. The figures display the typical respo~se

pattern found in the majority of neurons. Only in those

neurons, which saturate or adapt during long acceleration periods, could the activity during combined stimulation be greater than the activity during visual or vestibular stimulation alone (fig. 3Br. Suoh a dissociation, however, is only observed, if acceleration periods last longer than 6 - 8 sec. During deceleration after oonstant velOCity rotation in the light, neuronal activity returns to baseline levels. Only if the previous rotation velocity was higher than the level of visual saturation for the respective neuron, is some rebound in neuronal aotivity seen during deoeleration (fig. 1, right side).

Oonolusions:

The phenomenon that vestibular neurons can be in-

fluenced by optokinetiC stimuli has been found by several authors (n1nke " SChmidt, 1970; Dichgane et al., 1972, 1973; Henn et al., 1974). In the monkey such an interaction is also found in the vestibular projection area in the thalamus (BUttner" Henn, 1976).

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'lie speculate that the functional significance of this interaction is to provide central vestibular neurons with information about actual velocity instead of only acceleration, and thus to extend the working range of the vestibular system to include constant velocities and a very wide range of acceleration values. This leads to question of how the two inputs from the visual and the peripheral vestibular organ should combine. In agreement with that idea it appears that the two inputs complement each other, the visual input dominates the response in the low acceleration range (below 20/sec 2 ) and during periods of constant velocity, while the vestibular input dominates the response in the high acceleration range. There is also a middle range, where both inputs overlap. In order to have a linear response over the whole range of stimulation, one should not expect a summation of the two inputs. Responses seem to switch from the one input mode to the other, e.g. from the vestibular input to the visual input at the end of acceleration periods. On the basis of results from

psychophysical experiments a

model which incorporates such a switch was proposed by Young (1973) , Our results very much favor such a ' hypothesis. Recently, similar experiments have been done in t.mobllised goldfish (.lllua et al.,

1976). These authors come to the conclusion that the visual

&Dd

vestibular input are summated with weighted ,factors. ApplyinB such a model to our HSul ts would require that all veightinB factors chanBe continuously with time and thus i8 unsuitable. , In summary it could be shown that at the level of the vestibular nuclei information about movement is not only received from the

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peripheral vestibular organ, but also from the visual system. This extends the working range of movement detection from high to low acceleration and constant velocities. This single neuron recording in the alert monkey permits the investigation of the convergence of information from two different sensory systems and their respective influence on the oculomotor system.

Supported in part by Swiss National Foundation for Scientific Research 3.044.77 and Emi1 Bare11-Foundation of Hoffman-La Roche, Base1, Switzerland.

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