Interactions between extraocular myotatic and ascending vestibular activities

EXPERIMENTAL

NEUROLOGY

20,

120-134

(1968)

Interactions Between Extraocular Myotatic and Ascending Vestibular Activities Bo E. GERNANDT Naval Nnval

Aerospace Medical Institute, Aerospace Medical Center, Pensacola, Florida 32512

Received

September

22, 1967

The effect of bisensory convergence and interaction between extraocular myotatic and ascending vestibular activities, as reflected by recording from oculomotor nerves, the brain-stem reticular formation, or from single cells within that structure, was studied in cats. As revealed by extraocular stretch receptor and vestibular nerve stimulation in a controlled temporal sequence, the vestibular responses were markedly inhibited by conditioning stretch-receptor volleys, but interference with extraocular stretch response by preceding vestibular activity was weak or absent at the same recording site. In the competition for access to the cells within the reticular formation the impulses evoked by extraocular muscle stretch-receptor activation dominated. Only the vestibulo-ocular impulses funneled through neurons within the brain-stem reticular formation are under the inhibitory control of extraocular muscle stretch activation. vestibular activity conducted through the vestibular nuclei and along the

longitudinal

fasciculus to the oculomotor

The medial

nuclei was uninfluenced by this inhibitory

control, and no modification of the spontaneous in response to passive stretch applied to the observed.

activity extrinsic

in the oculomotor nuclei ocular muscles could be

Introduction

It is well known that impulses from the labyrinths are able to act on the different extraocular muscles in an extremely rapid and precise manner. Clearly, a complex neuronal circuitry is required for the autonomic achievement of conjugate ocular adjustments appropriate for head movements in any direction, In addition, the well-established existence of extraocular muscle receptors in man and mammals makes it reasonable to search for some peripheral event in the muscles themselves that is able to subserve. by feedback control, the precision and coordination of vestibulo-ocular reflex activity. However, the pertinent literature does not give much support to the assumption that proprioceptors in the eye muscles play au 120

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important part in eye movements or that they even give rise to myotatic stretch reflexes (18, 21). The present study concerns the functional significance of extraocular muscle receptor activation in governing the ascending flow of vestibular impulses and in providing the central nervous system with discriminative sensory information about muscle length and tension in the control of eye movements. In studying the effect of interaction upon spinal Motor pool activity in response to vestibular and proprioceptive stimulation it became evident how strongly and dominatingly the vestibular discharge was under proprioceptive control (2). Stretch receptors are found in the cat, a species that lacks extraocular muscle spindles (3, 7-9, 19, 27). Some insight into the complex interaction between impulses evoked by vestibular and extraocular stretch receptor activation can be obtained by stimulating these organs in a controlled temporal sequencewhile recording the average discharge activity from peripheral oculomotor nerves, the central core of the brain stem, or single cells within this structure. Not only do these evoked afferent impulses present themselvesto the samegeneral parts of the brainstem reticular formation, but also the impulses initiated from these two sourcesinteract with each other within the brain stem. The impulses elicited by stretch receptor activation have predominantly an inhibitory effect upon ascending vestibular activity. However, the characteristics, magnitude and duration of the alterations imposed upon vestibular activity vary according to the ascending vestibulofugal pathway involved. Only the vestibulo-ocular impulses routed through the multisynaptic connections of the reticular formation are influenced and not those conducted via the medial longitudinal fasciculus (MLF) . Methods The experiments were performed on cats anesthetized with intravenously administered alpha chloralose (35-50 mg/kg) or sodium pentobarbitone. They were kept fully immobilized by iterative dosesof gallamine triethiodide and were maintained on artificial respiration. The peripheral branches of the left vestibular nerve were exposed and equipped with stimulating electrodes according to the technique previously described ( 1). The stimuli, square wave pulses of 0.3 msec duration, were obtained from a Grass stimulator and applied through a stimulus-isolation unit. The soft tissues and bone of the frontal sinus over the left orbit were removed and the globe exposed. After emptying and remoX@ the globe the peripheral branches of the oculomotor nerve supplying the superior or medial rectus muscles were transected distally and placed on silver bipolar recording or stimulating electrodes. The nerves and muscles were protected by a pool of continuously warmed mineral oil. In certain of the cats

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(identified in Results) the tendon of the superior or medial rectus muscle together with a portion of the sclera containing the muscle insertion was attached to a puller by a fine thread. The puller consisted of a RCA 5733 mechanoelectronic transducer mounted on a pivot arm driven through a mechanical linkage by a Grass model III EEG machine pen motor (Fig 1) . The transducer could be calibrated in terms of grams versus volts. One channel of the oscilloscope recorded muscle stretch. The initial tension applied to the muscle was approximately 1 g. For brain stem recording, the posterior fossa was approached through an occipital craniotomy and, following exposure of the floor of the fourth ventricle by cerebellectomy, the medulla was penetrated by stereotaxically

PIVOTING LINKAGE ADJUSTMENT PIVOTING LINKAGE ATTACHMENT

\ 4mm DISTANCE OF TRAVEL

PULL bIRECTION

\

HOLLOW POLYSTYRENE ROD I

INSULATING NYLON CLAMP N/YLON SET SCREW

\ / ,r

MOTOR 3 SHAFT

/TEFLON

“I

PASS PEN MOTOR

ROD

‘RCA

PLATE

SHAFT

TUBE

SHELL

EVENT OUT

TRANSDUCER CIRCUIT PEN FIG. 1. to extrinsic

MOTOR

CONTROL

Diagram of experimental eye muscles. See text.

arrangement

and

equipment

for

applying

stretch

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oriented coaxial electrodes or by tungsten microelectrodes for single-unit extracellular analysis of the activity. The electrode-tip position was obtained by lateral, rostrocaudal and vertical measurements from surface landmarks. The electrode, mounted on a micromanipulator fixed to the stereotaxic instrument, was connected by a cathode follower to an a-ccoupled amplifier feeding a multibeam cathode-ray tube. A loudspeaker unit in parallel with the appropriate channel of the oscilloscope was used to monitor the activity recorded by the microelectrode. An electric intensifier circuit was used to brighten the oscilloscope traces of the spike potentials. Results

Interactions in Brain-Stem Rcyiolts Between Evoked Vest&&r and Oculomotov Nerve Activity. Neuronal convergence of different sensory modalities was first found in the reticular formation of the brain stem, and it is well established that vestibular stimulation evokes large bilateral responsesfrom both medial and lateral reticular formation (15, 16). Figure 2A (left insert) shows the ipsilateral response to single-shock vestibular stimulation recorded with a coaxial electrode from the caudal edge of the left inferior colliculus at a depth of 3 mm. Figure 2B shows this response preceded by activity evoked by a shock applied to the central end of the cut

0 IO

20

30

40

50

60

0 IO

20

30

40

50

60

MSEC 2. Left insert depicts control response (A) to single-shock vestibular stimulation recorded from brain-stem reticular formation when preceded by activity evoked by shock applied to central end of oculomotor nerve (B). Response to 20 pulse/xc vestibular stimulation (C). Right insert shows control response (D) to single-shock oculomotor nerve stimulation and when preceded by activity evoked by single-shock vestibular stimulation (E). Response to 20 pulse/set oculomotor nerve stimulation (F). Time scale in msec. Graphs demonstrate amplitude variations of vestibular and oculomotor nerve test responses relative to control responses = 1.0 plotted against conditioning-testing intervals in msec. FIG.

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oculomotor nerve supplying the left superior rectus muscle. At this interval between conditioning and test shocks the vestibular response was obliterated. Graphic representation of temporal interaction patterns permits some assessment of the changes of excitability which occur in a given brain-stem region. The powerful interference between the responses evoked by oculomotor nerve and vestibular nerve stimulation is depicted in the left graph of Fig. 2. Because of some spo’ntaneous variations in size of the two responses the subtraction method was not used for intervals at which conditioning and test responses overlapped in time. The preceding response to oculomotor nerve stimulation abolished the vestibular evoked response over an interval of IO-30 msec, measured between artifacts. At an interval of approximately 60 msec the test response had regained control size. Another way of influencing the amplitude of the vestibular response is by increasing the frequency of stimulation. As shown in Fig. 2C, the rate of stimulation was increased from one pulse every 2 set (A) to 20/set, and at this latter frequency the response was almost immediately abolished. When the sequence of stimulation was reversed, i.e., the vestibular response preceding the activity evoked by oculomotor nerve stimulation, a weak and sometimes questionable interaction could be observed (Fig. 2D and E, and the right graph). Thus, in the competition for access to the cells within the reticular formation the impulses evoked by oculomotor nerve stimulation dominate. In addition, this activity was less frequencysensitive, as demonstrated in Fig. 2D, showing the control response to one pulse applied every other set, and in F when the frequency of stimulation was increased to 20 pulse/set. Functional Diferences Between Reticular Formation and Medial Longitudinal

Fasciculus

in Conducting

Vestibular

Iw$wl.ses

to the Oculomotor

Nuclei. It was observed that high-frequency electrical stimulation of the vestibular nerve (200-250 pulse/set) evoked strong contractions of the extraocular muscles, as displayed by differently patterned eye movements. However, the present results indicate that the reticular formation does not transmit vestibular impulses above a certain repetition rate (Fig. 2C). Thus, the conduction of vestibulo-ocular impulses above a certain frequency must be handled by another route, i.e., the MLF, a pathway of almost point-to-point projection and with appropriate kinds of linear synaptic contacts with high-safety factor of transmission. In order to obtain some insight into this question, one coaxial electrode was placed with the tip just underneath the floor of the fourth ventricle and among the fibers of the ascending branch of the MLF, midway between the levels of eighth nerve entrance and inferior colliculus and ipsilateral or contralateral to the side of vestibular stimulation. A deep electrode, at the same level, was placed inside the reticular formation. In Fig. 3A is depicted the responses

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FIG. 3. Vestibular evoked responses recorded from medial longitudinal fasciculus (upper beam) and brain-stem reticular formation (lower beam) at 1 (A), 10 (B), 50 (C), and 200 pulse/set (D), respectively. Time scale in msec.

to single-shock vestibular stimulation recorded from MLF (upper beam) and reticular formation (lower beam), and B, C, and D show the responses when the frequency of vestibular stimulation was increased. At 10 pulse/ set (Fig. ZB), the MLF activity did not show any change, but the response recorded from the reticular formation was clearly diminished in size. At 50 and 200 pulse/set stimulation (C and D) , respectively, the MLF response started to decline in amplitude, particularly the early component, while a visible responsewas not obtained from the reticular formation. Oculomotor Nerve Recording. Figure 4,4 shows the ipsilateral response to single-shock vestibular stimulation recorded from the peripheral end of the oculomotor nerve branch supplying the medial rectus muscle. The nerve was cut and split into thin fasciculi after the connective sheath had been removed. At this frequency of stimulation of one shock every other set, the response recorded from a fasciculus appeared after a latency of about 5 msec and had a duration of approximately 8 msec. It was not unusual to distinguish two clusters of impulses, separated by a gap of about 1 msec, to single-shock vestibular stimulation in this kind of recording; the first volley of impulsespresumably was conducted through MLF and the second one through the reticular formation. However, most often there existed a slight overlap between the two sets of impulses, making a separation impossible without surgical interference of one of the available pathways (MLF). When the rate of stimulation was increased to 20 pulse/set, the duration of the response shortened considerably, but the latency was unchanged (Fig. 4B). Since the previous seriesof experiments demonstrated that only impulses evoked by vestibular stimulation and conducted via

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FIG. 4. Responses to single-shock (A) and 20 pulse/set (B) vestibular stimulation recorded from ipsilateral oculomotor nerve. Single-shock vestibular responses during stretch applied to superior rectus muscle at two different conditioning-testing intervals (C and D). Control vestibular response (E) and during gradually increasing muscle stretch (F-I). Single shock vestibular response after cerebellectomy (J) and during extraocular muscle stretch (I( and L). Vestibular response recorded from same animal but after sectioning of MLF (M) and during applied stretch to extraocular muscle (N). For further details see text. Time scale (lower beam) in msec.

ascending fibers of the MLF were able to follow high-frequency stimulation, it is reasonable to assumethat the initial part of the responseshown in Fig. 4B was due to activity transmitted along this trajectory. The rest of the response is postulated to be conducted via the reticular formation and thus unable to follow higher frequency stimulation. Another way of influencing the response was by applying gentle passive stretch to the superior rectus muscle while recording the efferent impulses. Compared to the control response (A), a pull of 69 g strongly reduced the duration (C). A still stronger pull, 88 g, permitted only the initial component of the response to appear without any noticeable change in latency (D). In this latter recording, the interval between the pull and the shock applied to the ear was shortened. In Fig. 4 (E-I), the effect of gradually

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increasing the strength of muscle stretch receptor stimulation upon the vestibular evoked activity is demonstrated. Compared to the control response (E) the duration of the evoked activity gradually became shorter when the strength of pull was increased from 16 (F) to 32 (G), and to 51 g (II), respectively. As shown in Fig. 41, a further increase to 59 gr did not influence the response, thus d~onstrating that a maximal effect was reached while a clearly visible initial part of the response was still present. In order to expose the floor of the fourth ventricle for a subsequent section of the ascending portion of the MLF, a complete cerebellectomy was performed. Figure 4f (as compared to A) illustrates the release of the response immediately following the elimination of this source of tonic control exerted upon vestibuIar activity (12, 14, 24). The inhibitor effect of eye muscle stretch receptor stimulation, however, was still demonstrable (K L). In Fig. 4M, the MLF had been eliminated bilaterally by section at a level 6 mm above the entrance of the eighth nerve. Because of the difficulties confining the MLF, particularly in the ventral direction, the section across the midline was made 3-mm wide and 3-mm deep (28). This gave rise to an increased latency of several msec ; the remai~ng response is looked upon as being conducted through the reticular formation. Support for this assumption was obtained by applying either high-frequency vestibular stimulation or extraocular muscle stretch. The latter is demonstrated in Fig. 4N, where a gentle pull of the muscle was able to obliterate the response completely. Interactions Between Evok‘ed Stretch Receptor and Vestibular Nerve ~cti~.t~ u.s ~~s~la~ed by Single-unit recording Within the Brown-Stem ~e~~c~~a~ ~o~rna~~o~. It seemed desirable to supplement the data presented so far with information provided by single-unit recordings. In order to carry out this kind of study, the units must be shared by the two input sources and both the stretch receptors and the vestibular organ must have connections projecting onto them. A change in the discharge rate of the isolated units in response to afferent activation was the sole criterion for establishing such a projection. With this biased method of selection in mind, a11neurons yielding stable patterns of discharge and spike amplitudes of at least 150 PV were investigated. As the microelectrode was advanced into the brain stem, numerous units were encountered along the line of penetration ; however, only a fourth of the units met the criterion. Since vestibular stimulation led to gross activation of the bulbar reticular formation, it was not hard to find single units whose activity could be influenced by this kind of peripheral stimulation. It was more difficult to isofate units onto which the stretch receptors of one of the extraocular muscles project,

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and finding cells whose activity is influenced by both peripheral sources, called for some searching. During microelectrode penetrations of the brain stem, the presence of a unit was usually first discovered by its spontaneous discharge. A small proportion of units might respond to appropriate peripheral stimuli when there was no spontaneous discharge at all, Such units were identified only by continuous stimulation of the two inputs during microelectrode penetration. The great majority of the extracellular focal potentials observed were diphasic, initially negative, spikes which lasted about 1 msec, thus making it probable that the recorded discharges were derived from cell bodies rather than from axons. The response types of each neuron to the two modalities of stimulation were repeatable and consistent, although the excitability varied. The usual response of a unit to a brief muscle stretch or to an electrical shock applied to the peripheral vestibular nerve branches consisted of a short repetitive train of impulses at high frequency. This is illustrated in Fig. 5A and G. In A the strength of pull applied to the medial rectus muscle was 44 g, and in G the response to vestibular stimulation, recorded from another unit, was evoked by a shock of 4 V and 0.3 msec duration. In some units the responses to a series of slowly repeated peripheral stimuli of constant parameters had a certain and stable,,distribution with relation to the number of impulses per response. while other units displayed multiple responses intermingled with failures. Sometimes, stimulation at low frequency produced initially a single action potential following each stimulus, but as the stimulation continued the response built up to a continuous high-frequency firing. In Fig. 5B-L are shown the effects of activity in extraocular muscle afferent fibers and vesfibular fibers as evidenced by changes of excitability of a unit in the reticular core of the brain stem. Figure 5B shows the most common type of response to a single-stretch stimulation of the eye muscle at an intensity of approximately three times threshold. Since the impulse frequency for a given muscle length was higher when the stretch was applied suddenly rather than slowly, it is likely that the tension of the muscle bundle rather than its length was the critical parameter which determined the impulse frequency. When the stimuli were repeated slowly, at rates up to 5/set, the unit was able to respond to each stimulus (Fig. SC and D). Wh en trains of higher frequency stimulation (20-30 pulse/set) were delivered, some units; commonly encountered, responded to the first few stimuli and then became inhibited during the
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FIG. 5. Unit recordings from bulbar reticular formation of responses to medial rectus muscle stretch (A) and to single-shock vestibular stimulation (G). Responses to medial rectus muscle stretch during gradually increasingfrequency (B to E).

Extraocular musclestretch stimulationprecedingvestibular stimulation(F, marked by dot). Vestibularcontrol respotiseto single-shock stimulation(H) andat gradually increasing

frequency

(I-K).

Vestibular

stimulation

preceding

extraocular

muscle

stretchactivation (L). Time scalein IO-msecintervals. at the usual rate of stimulation (one pull every other set). Following this inhibition, the units discharged at increased rates for some time, finally returning to their initial “resting” level. However, the presence of an inhibitory influence in normal, unimpared units could not be excluded. Figure 5F depicts the interaction between activity evoked by muscle stretch receptor stimulation and vestibular stimulation. The vestibular responsewas completely abolished when preceded by a pull of an extraocular muscle. The unconditioned vestibular control response obtained by an electrical shock of approximately three times threshold strength is shown in Fig. 5H. The blocking of this responsewhen preceded by activity evoked by stretch receptor activation was complete and lasted over an interval of about 300 msec, measured from artifact to artifact. When the interval between conditioning and testing stimuli was constant, changes in intensity

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relations clearly influenced the inhibitory interaction. Regularly, more intense and prolonged inhibition followed decrease in testing intensity relative to conditioning intensity, especially with strong conditioning stimuli. Decreasing the strength of the conditioning stimulus while keeping the testing intensity constant resulted in a gradual decrease of inhibitory action. Thus, it became evident how strongly and dominatingly the vestibular discharge is under proprioceptive control. Figure 5H illustrates the control response to low-frequency (one pulse every other set) vestibular stimulation, and Fig. 51-K demonstrates how rapidly the firing rate declined when the stimulation frequency increased. This occurred at a frequency when the unit was still able to fire in response to muscle stretch receptor stimulation (compare E and Ii). When the vestibular response preceded the response evoked by stretch receptor activation, an occlusive interaction was in most cases weak or absent (L) . Discussion

Vestibule-ocular movements, like countertorsion and nystagmus, are highly intricate reflexes designed to maintain the retinal image in the same position. Two principal pathways connect the vestibular organ with the extraocular muscles. One is the rather simple, rapidly conducting bisynaptic tract consisting of three ‘neurons : (a) the primary vestibular neuron ; (b) the secondary neuron ascending from the vestibular nuclei in the MLF to the oculomotor nuclei ; and (c) the motoneurons innervating the extrinsic eye muscles. The other fundamental link or important relay station in the vestibule-ocular reflex arc is more complex and includes the multisynaptic connections of the reticular formation (4, 5, 20). The convergence of impulses from a multitude of different receptors and central structures onto the reticular formation through abundant collaterals is well established. In accordance with Fillenz (9), it has now been possible to record activity evoked by passive stretch of the cat’s extraocular muscles from cell bodies within the brain-stem reticular formation. These impulses enter the brain stem through the trigeminal nerve (7, 9, 30) and reach the trigeminal nucleus, from which collaterals are given off to the reticular formation (6, 23). Since impulses from both the vestibular and extraocular muscle receptors impinge upon the same cells within the formation, the question arises whether the resulting interaction is of any functional importance in the regulation of these image-stabilizing reflexes. The literature, however, favors the governing of extraocular muscle activity exclusively by motor outflow without the support of kinesthetic feedback control (18). Previous studies on vestibular motor control carried out on the cat’s hind limb have shown that proprioceptive reflexes have both facilitatory and inhibitory effects upon vestibular activity; only the Golgi tendon organs

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were looked upon as being responsible for pure inhibition (2, 11, 13, 17). Although the extraocular muscles of the cat lack muscle spindles, they obviously possess receptors that are activated by passive stretch. These impulses impinge upon neurons within the brain-stem reticular formation and inhibit the vestibular activity that is funneled through the same neurons. In no instance has the interaction between activities evoked from the two sources shown facilitation. However, the vestibular activity which is conducted through the vestibular nuclei and along the MLF to the oculomotor nuclei seems to be uninfluenced by this inhibitory control. In addition, the ability of this anatomically rigidly organized pathway to transmit vestibular impulses of high frequency seems to be well above the limit at which impulses are generated in the vestibular receptor cells (10, 26). Modification of the spontaneous activity in the oculomotor nuclei in response to pulling on eye muscles was not observed (7). Since vestibular activity conducted through the MLF is not influenced by these two factors, feedback control and frequency limitation, it is of interest to know the proportion of activity routed through the reticular formation where these inhibitory influences are demonstrabIe. Some insight into this question can be obtained by functional separation or surgical interference. Thus, when increasing the frequency of vestibular stimulation to about 20 pulse/set, the response recorded from the reticular formation was abolished while the response obtained from the medial longitudinal fasciculus remained unchanged. When applying peripheral recording from an oculomotor nerve during single-shock vestibular stimulation, the response consisted of activity funneled through the two available routes. Then when higher frequency stimulation was applied, the original response to 1 pulse/ set showed a reduction of duration from 8 msec to 2 msec, but without a change in latency. As judged by the small response remaining, most of the vestibular impulses to the oculomotor nuclei must be conducted through the reticular formation, and only about one-fourth reaches the nuclei via MLF, although this tract, due to its relative simplicity, transmits impulses at a higher frequency and shorter latency. These results obtained by functional separation were supported by those achieved by surgical interference. The section through the MLF eliminated the early part of the response, increasing the latency by about 2 msec, but the greater portion of the response did not seem to be influenced. This demonstrated that the volleys of impulses conducted along the two principal pathways do not overlap to any considerable extent. When recording the average discharge activity with a coaxial electrode placed inside the bulbar reticular formation, stretch receptor activation always had a strong inhibitory effect upon a succeeding volley of vestibular impulses. This was not necessarily the case when recording from single

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cells within the same structure. Although the strength of stimulation could be regulated so that stretch and vestibular activation gave rise to an equal number of spikes, the interaction still varied widely from a very powerful, long-lasting inhibition to a weak or questionable effect. Admittedly, it called for some searching with the microelectrode tip before finding neurons within the reticular formation onto which both sets of peripheral receptors projected, but there was never any difficulty in isolating a sufficient number of cells in most experiments to carry out the present analysis. Whenever there was a failure, it was due to deterioration of the receptor organs or the peripheral nerves. Thus, the percentage of neurons with this dual projection is probably high, and, in spite of the abundance of vestibuloocular connections available, an inhibitory feedback control regulating the activity of these particular neurons ought to he reff ected in the performance of the effector organs-the extraocular muscles. Every extraocular muscle contraction must he accompanied by stretch of the antagonistic muscle whose receptors signal its state of tension. As shown, vestibulo-ocular motor responses recorded from a nerve sectioned before it enters an extraocular muscle can be strongly influenced by stimulating the stretch receptors of an intact neighboring muscle. It is difficult. however, to form a clear picture of the functional significance of the inhibitory control exerted by the stretch receptors upon that part of the vestibular activity which is transmitted through the reticular formation. One possible role of these impulses may be to dampen and correct overshooting and oscillations of the eye muscles with a self-regulating system operating on the feedback principle. The slow properties of the muscles, owing to the viscosity of the muscle tissue, are another supporting factor. However. it is difficult to believe that the stretch receptors contribute to the control of saccadic eye movements or vestihular and optokinetic nystagmus since neither the vestibular nuclei nor the oculomotor nuclei is under the influence of this inhibitory mechanism. In addition, we know that only the midbrain is necessary for nystagmus since it persists after section of the brain stem at the level of the oculomotor nuclei, and that the motor discharge during nystagmus is unaffected by section of the nerves to the extraocular muscles (21, 22, 29). Since cocainization of the receptors, for example, does not influence nystagmus (25) one may suspect either that the method of recording nystagmus externally is not delicate enough in detecting minute changes in rhythmic eye movements or that the vestibuloocular impulses funneled through connections that are not controlled by inhibitory feedback are enough for evoking the highly intricate imagestabilizing reflexes exclusively by motor outflow.

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2. 3. 4.

5. 6.

7.

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ANDERSON,

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8. COOPER,S., and M. FILLENZ. 1955. Afferent discharges in response to stretch from the extraocular muscles of the cat and monkey and the innervation of those muscles. J. Physiol. London 127: 400-413. 9. FILLENZ, M. 1955. Responses in the brain stem of the cat to stretch of extrinsic ocular muscles. J. Physiol. London 128: 182-199. 10. GERNANDT, B. E. 1949. Response of mammalian vestibular neurons to horizontal rotation and caloric stimulation. J. Neurophysiol. 12: 173-184. 11. GERNANDT, B. E. 1964. Somatic and autonomic motor outflow to vestibular stimulation, pp. 194-211. In “Neurological Aspects of Auditory and Vestibular Disorders,” W. S. Fields and B. R. Alford reds.]. Thomas, Springfield, Illinois. 12. GERNANDT, B. E. 1967a. Central regulation of the vestibular system. Arch. Otolavyngol. 85: 521-528. 13. GERNANDT, B. E. 1967b. Vestibular influence upon spinal reflex activity, pp. 17O383. 1~ “Myotatic, Kinesthetic and Vestibular Mechanisms,” A. V. S. de Reuck and J. Knight [eds.]. Churchill, London. 14. GERNANDT, B. E., and S. GILMAN. 1959. Descending vestibular activity and its modulation by proprioceptive, cerebellar, and reticular influences. Exptl. Neurol. 15.

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