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Canal-Otolith Convergence on Cat Ocular Motoneurons
Canal-Otolith Convergence on Cat Ocular Motoneurons W. PRECHT, J.H. ANDERSON and R.H.I. BLANKS
Max-Planck-Institutf i r Hirnforschung, Neurobiologische Abteilung, 6000 Frankfurt M.-Niederrad (F.R.G.)
In the last decade, considerable progress has been made in our understanding of the response dynamics of vestibulo-ocular reflexes and the central neural systems involved, in particular, for the canal-ocular reflexes (for review, see Schmid and Jeannerod, this volume, chapter IVC6). Relatively little work has been done with the dynamics and neural organization of otolith-ocular reflexes and the importance of canal-otolith convergence for the control of -eye movements. In these studies the relationship between acceleratory stimuli excitatory for the otolith receptors, and eye position was studied during ocular-counterrolling under static (Van der Hoeve and De Kleijn, 1917; Fleisch, 1922a) and dynamic (Fleisch, 1922b) lateral tilting of the head. Furthermore, eye movements have been studied during horizontal linear acceleration in the rabbit (Reisch, 192213; Baarsma and Collewijn, 1975; Kleinschmidt and Collewijn, 1975), cat (Kohut, 1974) and man (Jongkees and Philipszoon, 1964). The contributions made by the different extraocular muscles to these movements (Lorente de Nb, 1932; Suzuki et al., 1968) as well as the receptor groups likely to contribute to activation of the corresponding motoneuron pools (Fluur and Mellstrom, 1971) have been investigated in a qualitative manner. Of particular interest are the quantitative studies in the rabbit (Baarsma and Collewijn, 1975) which demonstrate a considerable phase lag of eye position relative to linear acceleration at higher frequencies suggesting that the otolith-ocular system performs poorly under dynamic load conditions. Since the responses of otolith afferents in frog, monkey and cat do not show this phase lag (Blanks and Precht, 1976; Fernhndez and Goldberg, 1976a, b; Anderson et al., 1978), the dynamic characteristics of the otolith-ocular reflexes must be due to either visco-elastic properties of the eyeball-orbit system and/or result from central processing. One part of this paper will be devoted to the demonstration of central processing of otolithic information, by comparing motoneuron output with primary otolith input. A second part will deal with the importance of canal-otolith convergence for extending the frequency response characteristics of motoneurons involved primarily, but not exclusively, in vertical/rotatory eye movements. METHODS Experiments were carried out in cats anesthetized with ketamine. Details of the experimental procedures for natural stimulation and data analysis have been fully
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described previously and will not be repeated here (Anderson et al., 1978; Blanks et al., 1978; Anderson and Precht, 1979). In short, single identified motoneurons were recorded with glass micropipettes from the abducens and trochlear nuclei during natural stimulation of canal only, otolith only and during combined canal-otolith stimulation. Similar stimuli were applied while recording the EMG activity of the superior and inferior obliques, and medial and lateral recti with flexible wires inserted into the muscles. RESULTS AND DISCUSSION As a first step we recorded the responses of trochlear motoneurons to canal and otolith stimulation. These neurons were chosen for the investigation because of their importance for the control of vertical-rotatory eye movements in response to gravitational (static and dynamic) and angular accelerations (Suzuki et al., 1969; Fluur and Mellstrom, 1971). Secondly, the responses of abducens motoneurons, which are mainly responsible for canal-evoked horizontal eye movements, were studied during gravitational stimuli as well. Finally, to confirm and expand the data obtained from single motoneurons of the vertical-rotatory and horizontal eye muscle systems, we recorded simultaneously multi-unit EMGs from the antagonistic muscle pairs, the superior and inferior obliques and the medial and lateral rectus muscles, during angular and gravitational stimulation. The responses of trochlear and abducens motoneurons to vestibular stimuli will be described first.
Responses of trochlear and abducens motoneurons to canal and otolith stimulation Determination of inputs. Natural vestibular stimuli were applied to determine which receptors projected to motoneurons. For the canal projection this was done by a null-point technique (Blanks et al., 1978). This technique implies systematic changes of the animal's head position until the unit no longer responds to horizontal rotation. With this spatial orientation of the head, the canals providing excitatory inputs are perpendicular t o the plane of rotation and yield no response. By comparing the null-points obtained from motoneurons with those determined for the peripheral canal afferents (Estes et al., 1975), it was concluded that trochlear motoneurons received their major excitatory input from the cantralateral posterior canal and, based on studies in hemilabyrinthectomid cats, an inhibitory input from the ipsilateral anterior canal (Blanks et al., 1978). These data are in full agreement with results obtained from electrical stimulation of individual vestibular nerve branches (Precht and Baker, 1972; Baker et al., 1973)Abducerzs motoneurons received their excitatory and inhibitory inputs from the contra- and ipsilateral horizontal canals, respectively (Richter and Prexht, 1968; Baker et al., 1969; Precht et al., 1969; Schwindt et al., 1973; Anderson and Precht, 1979). It is important to note that the motoneurons showed a very stereotyped input from these coplanar canal pairs and little orthogonal canal-canal convergence when studied with electrical and natural stimuli. Only a few units had n o null-point, a fact that is indicative of orthogonal convergence (Blanks et al., 1978). Otolith projections to motoneurons were studied by measuring the firing frequency in various static positions. Fig. 1 exemplifies this procedure in showing the responses
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Fig. 1. Responses of trochlear motoneurons (TMns) as a function of static tilt in roll. The discharge for each of 5 different TMns was determined at the different head positions as the average discharge rate over a 30 sec interval, 20 sec after arrival at the new position. Note that all units show a &otolith response. (From Blanks et al., 1978.)
of five trochlear motoneurons in various roll angles. As the head was tilted laterally towards the recording side the resting rate decreased, whereas the opposite movement caused an increase in firing @-response). Almost all trochlear motoneurons showed this response and only few responded exclusively to canal stimulation. The sensitivity of the response was high (ca. 1 spike/degree/sec), and there was no upper saturation up to 30" of tilt angle. Abducens motoneurons also showed responses to static lateral tilt which consisted of increases and decreases in firing with the recording side down and up, respectively, i.e., an a-otolith response (Anderson and Precht, 1979). Gravity responses were less frequently observed in abducens motoneurons when compared with trochlear motoneurons and, when present, the sensitivity was generally low. The canal and otolith inputs to trochlear and abducens neurons, determined with natural stimulation, are in perfect agreement with electrophysiological studies showing short-latency utricular inputs to ipsilateral abducens (Schwindt et al., 1973) and contralateral trochlear motoneurons (Baker et al., 1973). It is interesting to note that electrical stimulation of the utricular nerve did not reveal any short-latency inhibitory reflexes to antagonistic motoneurons, as in the case for reference, Precht, 1978). When trochlear motoneurons of canal-ocular reflexes (6. of hemilabyrinthectomized cats were studied during static tilt, responses were found that could only be explained by assuming an inhibitory otolith-ocular reflex as well (Blanks et al., 1978). Since they had escaped electrophysiological studies it must be assumed that they are polysynaptic in nature and were therefore depressed in anesthetized preparations. In summary, trochlear and abducens motoneurons receive very specific canal and otolith inputs and show very little orthogonal canal convergence. Contrary to the disynaptic inhibitory and excitatory canal-ocular reflexes, otolith-ocular reflexes appear to be disynaptic only when excitatory. To corroborate and extend the findings obtained with single motoneurons, simultaneous EMG recordings were obtained from i) the two lateral recti muscles, iij the medial (MR) and lateral (LR) recti muscles of the same eye, and iii) the superior (SO) and inferior oblique (10) muscles, during static and/or low frequency sinusoidal roll stimulation. At the low frequency of 0.025 Hz (Fig. 2A-D) the modulation of EMG activity is displacement related and at higher frequencies of
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Fig. 2. Reciprocal organization of the oblique and horizontal recti muscles during roll rotations. The response to low frequency rotations shown here demonstrates the pattern of responses to otolith inputs: on side down the EMG of the ipsilateral SO and LR and contralateral I 0 and MR increase while the contralaterat SO and LR decrease, e.g., SO,(A) and LR,(E) increase on left side down (i.e., acceleration right). The rotations used were 0.025 Hz,%20" in A-C and 0.25 Hz, %20"in D-F. The pulse trains corresponding to the EMG recordings were binned and averaged over 5-10 periods to give the cycle histograms shown. (From Anderson and Precht, 1979.)
rotation (Fig. 2E, F) the horizontal recti show a significant phase lag. Quantitative analysis is presented in Fig. 5 . As these records show, both the oblique (Fig. 2A-C) and horizontal (Fig. 2D-F) systems have a reciprocal organization of otolith inputs during roll, i.e., the SO and 10, SO, and SO,, LR, and LR, are synergistic pairs which can subserve the coordinated eye movements caused by otolith-ocular reflexes. A similar reciprocal relationship was noted in the muscle pairs: MR, and MR,1 0 , and 10, (not shown).
Responses of motoneurons to ramp changes in head position In the preceding section it has been shown that most trochlear and some abducens motoneurons respond to both canal and static otolithic stimuli. In this and the following sections we shall describe the behavior of motoneurons during stimuli such as ramp changes in head position and sinusoidal rotations (next section) about the longitudinal body axis (roll). Non-periodic ramp changes in roll-position produce angular acceleration pulses at the beginning and termination of the ramp which can activate the canals. In addition, otolith inputs are present due to the changing orientation of the animal's head with respect to gravity. The latter input predominates with slow changes in head positions whereas canals are recruited as the slopes of the ramps become greater. Typical examples of responses of a trochlear motoneuron to ramp changes in head position in roll are shown in Fig. 3. Slow transients of head position (Fig. 3A) produce changes in
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Fig. 3 . Response of trochlear motoneurons to ramp changes in roll position. The instantaneous frequency of the discharge of a single motoneuron is shown for changes in angular position from -2” (ipsi side down) to +25” (ipsi side up) with constant velocities of 3.3 (A) and 16.2 degrees/sec (B). (From Anderson et al., 1977.)
instantaneous firing rate which were nearly proportional or slightly lagging head displacement. The maximum discharge level is achieved only after arrival of the final displacement and then adapts, as in this neuron, to a new steady state level. With greater slopes of the ramp stimuli (Fig. 3B) and hence greater acceleration pulses at the onset and termination, the threshold for a canal response is exceeded, thereby producing a transient increase in discharge at the onset of the ramp and a decrease of firing following its termination. Following the canal transient, the firing continues to increase due to otolithic stimuli and finally adapts to a new level. Adaptation was observed in about 30% of the neurons. Ramps of the same magnitude but in the opposite direction yielded a slow decrease in firing, along with the fast canal transients. It should be pointed out that the canal induced transients had the same polarity as the otolith-evoked responses at the onset of ipsilateral side-up movements but were of opposite polarity at the termination of the ramp. The opposite pattern of activation was noted with transients from ipsilateral-up to ipsilateral-down. Abducens motoneurons showed a similar combination of canal and otolithic responses to ramp displacements in roll only when the animal’s head was oriented in such a way as to cause costimulation of the horizontal canals. When the latter were brought into a null-plane with respect to roll rotation, only otolith modulation of discharge rate was noted. However, it is important to emphasize that both the sensitivity and the number of otolith responses were smaller than in the trochlear neuron. The importance of this fact will be further discussed iri the next section. In short, the responses of motoneurons to ramp changes have shown that whenever canals are in the stimulating plane and the slope of the ramp is large enough to reach canal threshold, motoneurons are subjected to a combined canal-otolithic input. Gravity responses resulting from ramp changes lag head displacement more than primary otolith afferents (Anderson et al., 1978) indicating central processing of otolith afferent input. Further details of the dynamics of otolith processing will be given in the next section. Responses of motoneurons to sinusoidal stimulation The phase-gain response properties of single trochlear and abducens motoneurons as well as the EMGs of the corresponding muscles were recorded during sinusoidal rotation (Anderson et al., 1977; Blanks et al., 1978; Anderson and Precht, 1979). As already shown in the preceding section, roll stimulation activates both canal and otolith inputs to trochlear motoneurons, whereas rotation in yaw leads to canal activation only provided the contralateral posterior and ipsilateral anterior canals
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have some component in the plane of horizontal rotation. The otolith component of the combined canal-otolith response may then be obtained by vectorially subtracting the yaw (canal only) from the roll (canal and otolith) responses. To test the validity of the subtraction method we have then compared the calculated frequency responses of the otolith input to trochlear motoneurons with that obtained for abducens motoneurons and lateral rectus muscle in roll (an otolith input only, provided the horizontal canals are perpendicular to roll plane). The averaged responses of trochlear motoneurons during rotation in both yaw and roll are shown in Fig. 4. In yaw, the motoneuron's phase lags increase as the frequency of rotation increases (0,Fig. 4). Also, the phase lags of motoneurons are larger at all frequencies as compared to those of the primary canal afferents (A, Fig. 4); the upper-left shaded area in Fig. 4 indicates the central processing (integration) of canal inputs. It should be noted that these experiments were done under light ketamine anesthesia which influences the central integration process resulting in smaller phase values. When the same population of motoneurons were studied in roll (0, Fig. 4), the phase lag decreases as the frequency of rotation increases. Since the phase in both cases was measured with respect to the acceleration excitatory for the contralateral posterior canal, the yaw and roll phase behavior would have been identical if there were only canal input. Therefore, the phase differences between yaw and roll responses can only be due to the otolith input present in roll. It is apparent that at low frequencies, where the canal input is small relative to otolith input, the phase of trochlear motoneurons in roll is largely determined by the otolith input which, from previous sections, have a DC response maximum with ipsilateral side-up position (-6) in Fig. 4). At higher frequencies, the phase of the roll response is largely determined by the canal input, which increases as the frequency squared. Carefully considering the various problems of the vectorial subtraction procedure (Blanks et al., 1978) the yaw, response vector (gain,, phase,) was subtracted from the roll(r) vector (gain,, phase,) for each frequency. An example of one such calculation is shown by the insert in Fig. 4. The results of this procedure are shown by the lowest dashed line and X ' S in Fig. 4. It can be seen that the phases of the otolith response show a lag of 10"-90"over the frequency range, 0.025-0.5 Hz. These are relative to angular displacement which is proportional to the gravity input to otoliths. The difference between these calculated values for trochlear neurons and those obtained from primary otolith fibers (A, Fig. 4) (Anderson et al., 1978) are given by the shaded zone in the lower part of Fig. 4. Obviously, the signal in the otolith-ocular pathway undergoes central transformations similar to those in the canal-ocular path, i.e., phases and gains increase and decrease, respectively, with increasing frequency indicating central integration. The lag dynamics noted in the ramp studies (Fig. 3) are consistent with the results obtained in the frequency domain. The phase values relative to displacement for the abducens motoneuron response and the EMG activity of lateral and medial recti muscles during sinusoidal stimulation in roll (otolith only) are shown in Fig. 5 (Anderson and Precht, 1979). These values are, indeed, very similar to those calculated for trochlear motoneurons. This similarity indicates that the subtraction method is valid for calculation of otolith input during roll, and that otolith processing is similar for the horizontal and vertical eye movement systems. The central structures necessary for this processing of the afferent activities are still unknown. However, some data obtained from the vestibular nuclei (Melvill Jones and
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Fig. 4. Canal and otolith contributions to the motor output of trochlear motoneurons (TMns). The responses of 10 TMns during both yaw and roll (mean values shown by 0,0 , resp.) were used to calculate the otolith contribution (Y,) to the motor output. This entailed a vectorial subtraction of the yaw (Yc, canal only input) from the roll (Tcmrcanal plus macular input) response, as indicated in the insert. The mean 51 SD of these calculations are shown by the symbol X and the vertical bars. For comparison, the mean phases and gains for the canal (A) and otolith (A) afferents (Anderson et al., 1978) are shown. The vertical bars include ?1 SD. Note that the stippled areas represent the difference between the afferent inputs and the motoneuron outputs. Thus it is evident that for both the canal and otolith systems there is extensive central processing of the afferent activities. (From Blanks et al., 1978.)
Milsum, 1969) indicates that responses of secondary vestibular neurons already differ significantly from those of vestibular afferents. During the course of our experiments we often recorded from axons of vestibular neurons within the trochlear nucleus which were monosynaptically driven by ipsilateral (Vi) or contralateral (Vc) vestibular nerve stimulation. Since it may be assumed that some of these axons terminate in the trochlear nucleus their response characteristics are of some interest. About half of the Vi and Vc axons showed responses to otolithic in addition to canal stimulation. The polarity of these responses was such that the excitatory Vc and inhibitory Vi axons could modulate the motoneuron discharge as described above. Thus, Vc axons were driven by the contralateral posterior canal and showed a @-otolithresponse; whereas Vi axons were exclusively activated by the ipsilateral anterior canal, and, when present, showed a-otolith responses. Also, the frequency response of these convergent units during yaw and roll sinusoidal rotations was very similar to those of trochlear motoneurons (Fig. 4) except that their phase lags were somewhat smaller. This finding also supports the notion that secondary vestibular axons projecting to motoneurons carry an otolithic signal that is already different from that of otolith afferents. Interestingly, we did not find any axons that carried a pure otolithic signal without canal components whereas the opposite, i.e., a canal response only, was seen in about half of the cases. Of course, these negative findings do not exclude the possible
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005 01 025 05 10 FREQUENCY (Hz1 Fig. 5. Phase behavior of otolith afferent and extraocular motor outputs during sinusoidal roll rotations. The calculated otolith-dependent responses of trochlear motoneurons (0,mean of 10 units) are shown together with the measured responses of abducens neurons (V, mean of 5 units) and the EMGs of the medial and lateral recti ( 0 ,mean of 3 animals). The hatched area encompassesthe mean 2 1SD for the responses of the otolith afferents. For all cases, the input reference is angular displacement: ipsilateral side up for the trochlear neurons and medial rectus EMGs and side down for abducens neurons and the lateral rectus EMGs. The stippled region shows the phases of a simple first order system, l / s + a, which approximates the motor outputs with time constants, l / a of 0.8-1.6 sec. (From Anderson and Precht, 1979.) 0 01
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existence of pure otolithic projections. If they were to terminate, for example, as thin fibers on dendritic ramifications of the motoneuron pool they may easily have escaped microelectrode search.
CONCLUSION AND SUMMARY In the present paper it has been shown that ocular motoneurons of the horizontal and vertical/oblique systems receive both canal and otolithic inputs and that these inputs are reciprocally organized. The functional importance of canal-otolithic convergence in vertical/oblique motoneurons, and probably also in horizontal motoneurons, is to extend the working range over a much wider frequency band than is provided by the simple canal VOR. This is particularly evident in trochlear motoneurons during roll rotation where the canal and otolith responses have the same polarity. At high frequencies, the canal system may, therefore, serve to compensate for the lag present in the otolith system in addition to its compensation for the visco-elastic properties of the eye. When the roll movement is stopped the responses of canal and otolith are of opposite polarities and may cancel one another. In this case, the canal response may serve to prevent the eye from overshooting its final position. On the other hand, the otolith input serves to compensate for the poor canal performance in the low frequency range and, of course, during static head displacement. It is interesting to note that the responses of vertical/rotatory motoneurons in roll, measured in the dark, are comparable to those found in the horizontal system in the presence of vision. Thus, whereas vision improves the insufficiencies of the canal-ocular response in yaw at low frequencies, the otolith
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contribution in roll may be important for extending the lower frequency range of the vertical/rotatory vestibulo-ocular reflexes. The otolith responses found in the horizontal eye movers may also be important in roll and pitch rotation, because a contraction of the lateral and medial recti muscles, due to their insertions, can facilitate the vertical or rotatory eye movements. However, it should be noted that the otolith signal in the horizontal system was much weaker than that in vertical/rotatory muscles. When the dynamics of the central otolith signal were compared with those of peripheral afferents, a large difference was apparent suggesting that, as for the canal input, a leaky neural integrator is processing the otolithic afferent input. Pertinent to the present results is the work of Baarsma and Collewijn (1975), who have studied the phase and gain behavior of eye movements in the alert rabbit during horizontal linear accelerations. They found phase lags for the motor output very similar to those shown above for frequencies from 0.023 to 0.5 Hz.They report greater phase lags at the higher frequencies (180" at 1.2 Hz) which suggest that other factors (e.g., eyeballorbit visco-elastic properties) may be involved.
REFERENCES Anderson, J.H. and Precht, W. (1979) Otolith responses of extraocular muscles during sinusoidal roll rotations. Bruin Res., 160: 150-154. Anderson, J.H., Precht, W. and Blanks, R.H.I. (1977) Central processing in otolith-ocular reflex pathways. In Control of Gaze by Bruin Stem Neurons, R. Baker and A. Berthoz (Eds.), Elsevier, Amsterdam, pp. 253-260. Anderson, J.H., Blanks, R.H.I. and Precht, W. (1978) Response characteristics of semicircular canal and otolith systems in cat. I. Dynamic responses of primary vestibular fibers. Exp. Brain Res., 32: 491-507. Baarsma, E.A. and Collewijn, H. (1975) Eye movements due to linear accelerations in the rabbit. J. Physiol. (Lond.), 245: 227-247. Baker, R., Precht, W. and Berthoz, A. (1973) Synaptic connections to trochlear motoneurons determined by individual vestibular nerve branch stimulation in the cat. Bruin Res., 64: 402406. Blanks, R.H.I. and Precht, W. (1976) Functional characterization of primary vestibular afferents in the frog. Exp. Bruin Res., 25: 369-390. Blanks, R.H.I., Anderson, J.H. and Precht, W. (1978) Response characteristics of semicircular canal and otolith systems in cat. 11. Responses of trochlear motoneurons. Exp. Brain Res., 32: 509-528. Estes, M.S., Blanks, R.H.I. and Markham, C.H. (1975) Physiologic characteristics of vestibular first-order canal neurons in the cat. I. Response plane determination and resting discharge characteristics. J. Neurophysiol., 38: 1232-1 249. Fernhdez, C. and Goldberg, J.M. (1976a) Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. I. Response to static tilts and to long-duration centrifugal force. J. Neurophysiol., 39: 970-984. Fernhndez, C. and Goldberg, J.M. (1976b) Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. 111. Response dynamics. J. Neurophysiol., 39: 996-1008. Fleisch, A. (1922a) Tonische Labyrinthreflexe auf die Augenstellung. Pjliigers Arch., 194: 554-573. Reisch, A. (1922b) Das Labyrinth als beschleunigungsempfindendes Organ. Pfligers Arch ., 195: 499-5 15. Fluur, E. and Mellstrom, A. (1971) The otolith organs and their influence on oculomotor movements. Exp. Neurol., 30: 13%147. Jongkees, L.B.W. and Philipszoon, A.J. (1964) Electronystagmography. Actu oto-luryngol. (Stockh.), SUPPI.189: 1-111. Kleinschmidt, H.J. and Collewijn, H. (1975) A search for habituation of vestibulo-ocular reactions to rotatory and linear sinusoidal accelerations in the rabbit. Exp. Neurol., 45: 257-267.
468 Kohut, R.I. (1974) Vertical linear acceleration (otolithic-ocularresponses). Laryngoscope, 84: 1627-1662. Lorente de N6, R. (1932) The regulation of eye positions and movements induced by the labyrinth. Laryngoscope, 42: 233-332. Melvill Jones, G. and Milsum, J.H. (1969) Neural response of the vestibular system to translational acceleration. In Conference on Systems Analysis Approach to Neurophyswlogical Problems, Brainerd, Minnesota. Precht, W. (1978) Neuronal operations in the vestibular system. In Studies ofBrain Function, Vol. 2 , V. Braitenberg (Ed.), Springer-Verlag, Berlin-Heidelberg-New York, p. 226. Precht, W. and Baker, R. (1972) Synapticorganization of the vestibulo-trochlearpathway. Exp, Brain Res., 14: 158-184. Precht, W., Richter, A. and Grippo, J. (1969) Responses of neurones in cat’s abducens nuclei to horizontal angular acceleration. Pfliigers Arch., 309: 285-309. Richter, A. and Precht, W. (1968) Inhibition of abducens motoneurones by vestibular nerve stimulation. Brain Res., 11: 701-705. Schwindt, P.C., Richter, A. and Precht, W. (1973) Short latency utricular and canal input to ipsilateral abducens motoneurons. Brain Res., 60: 259-262. Suzuki, J.I., Tokumasu, K. and Goto, K. (1969) Eye movements from single utricular nerve stimulation in the cat. Acta oto-laryngol. (Stockh.), 68: 350-392. Van der Hoeve, J. and De Kliijn, A. (1917) Tonische Labyrinthreflexe auf die Augen. Pflugers Arch., 169: 241-262.
Max-Planck-Institutf i r Hirnforschung, Neurobiologische Abteilung, 6000 Frankfurt M.-Niederrad (F.R.G.)
In the last decade, considerable progress has been made in our understanding of the response dynamics of vestibulo-ocular reflexes and the central neural systems involved, in particular, for the canal-ocular reflexes (for review, see Schmid and Jeannerod, this volume, chapter IVC6). Relatively little work has been done with the dynamics and neural organization of otolith-ocular reflexes and the importance of canal-otolith convergence for the control of -eye movements. In these studies the relationship between acceleratory stimuli excitatory for the otolith receptors, and eye position was studied during ocular-counterrolling under static (Van der Hoeve and De Kleijn, 1917; Fleisch, 1922a) and dynamic (Fleisch, 1922b) lateral tilting of the head. Furthermore, eye movements have been studied during horizontal linear acceleration in the rabbit (Reisch, 192213; Baarsma and Collewijn, 1975; Kleinschmidt and Collewijn, 1975), cat (Kohut, 1974) and man (Jongkees and Philipszoon, 1964). The contributions made by the different extraocular muscles to these movements (Lorente de Nb, 1932; Suzuki et al., 1968) as well as the receptor groups likely to contribute to activation of the corresponding motoneuron pools (Fluur and Mellstrom, 1971) have been investigated in a qualitative manner. Of particular interest are the quantitative studies in the rabbit (Baarsma and Collewijn, 1975) which demonstrate a considerable phase lag of eye position relative to linear acceleration at higher frequencies suggesting that the otolith-ocular system performs poorly under dynamic load conditions. Since the responses of otolith afferents in frog, monkey and cat do not show this phase lag (Blanks and Precht, 1976; Fernhndez and Goldberg, 1976a, b; Anderson et al., 1978), the dynamic characteristics of the otolith-ocular reflexes must be due to either visco-elastic properties of the eyeball-orbit system and/or result from central processing. One part of this paper will be devoted to the demonstration of central processing of otolithic information, by comparing motoneuron output with primary otolith input. A second part will deal with the importance of canal-otolith convergence for extending the frequency response characteristics of motoneurons involved primarily, but not exclusively, in vertical/rotatory eye movements. METHODS Experiments were carried out in cats anesthetized with ketamine. Details of the experimental procedures for natural stimulation and data analysis have been fully
460
described previously and will not be repeated here (Anderson et al., 1978; Blanks et al., 1978; Anderson and Precht, 1979). In short, single identified motoneurons were recorded with glass micropipettes from the abducens and trochlear nuclei during natural stimulation of canal only, otolith only and during combined canal-otolith stimulation. Similar stimuli were applied while recording the EMG activity of the superior and inferior obliques, and medial and lateral recti with flexible wires inserted into the muscles. RESULTS AND DISCUSSION As a first step we recorded the responses of trochlear motoneurons to canal and otolith stimulation. These neurons were chosen for the investigation because of their importance for the control of vertical-rotatory eye movements in response to gravitational (static and dynamic) and angular accelerations (Suzuki et al., 1969; Fluur and Mellstrom, 1971). Secondly, the responses of abducens motoneurons, which are mainly responsible for canal-evoked horizontal eye movements, were studied during gravitational stimuli as well. Finally, to confirm and expand the data obtained from single motoneurons of the vertical-rotatory and horizontal eye muscle systems, we recorded simultaneously multi-unit EMGs from the antagonistic muscle pairs, the superior and inferior obliques and the medial and lateral rectus muscles, during angular and gravitational stimulation. The responses of trochlear and abducens motoneurons to vestibular stimuli will be described first.
Responses of trochlear and abducens motoneurons to canal and otolith stimulation Determination of inputs. Natural vestibular stimuli were applied to determine which receptors projected to motoneurons. For the canal projection this was done by a null-point technique (Blanks et al., 1978). This technique implies systematic changes of the animal's head position until the unit no longer responds to horizontal rotation. With this spatial orientation of the head, the canals providing excitatory inputs are perpendicular t o the plane of rotation and yield no response. By comparing the null-points obtained from motoneurons with those determined for the peripheral canal afferents (Estes et al., 1975), it was concluded that trochlear motoneurons received their major excitatory input from the cantralateral posterior canal and, based on studies in hemilabyrinthectomid cats, an inhibitory input from the ipsilateral anterior canal (Blanks et al., 1978). These data are in full agreement with results obtained from electrical stimulation of individual vestibular nerve branches (Precht and Baker, 1972; Baker et al., 1973)Abducerzs motoneurons received their excitatory and inhibitory inputs from the contra- and ipsilateral horizontal canals, respectively (Richter and Prexht, 1968; Baker et al., 1969; Precht et al., 1969; Schwindt et al., 1973; Anderson and Precht, 1979). It is important to note that the motoneurons showed a very stereotyped input from these coplanar canal pairs and little orthogonal canal-canal convergence when studied with electrical and natural stimuli. Only a few units had n o null-point, a fact that is indicative of orthogonal convergence (Blanks et al., 1978). Otolith projections to motoneurons were studied by measuring the firing frequency in various static positions. Fig. 1 exemplifies this procedure in showing the responses
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Fig. 1. Responses of trochlear motoneurons (TMns) as a function of static tilt in roll. The discharge for each of 5 different TMns was determined at the different head positions as the average discharge rate over a 30 sec interval, 20 sec after arrival at the new position. Note that all units show a &otolith response. (From Blanks et al., 1978.)
of five trochlear motoneurons in various roll angles. As the head was tilted laterally towards the recording side the resting rate decreased, whereas the opposite movement caused an increase in firing @-response). Almost all trochlear motoneurons showed this response and only few responded exclusively to canal stimulation. The sensitivity of the response was high (ca. 1 spike/degree/sec), and there was no upper saturation up to 30" of tilt angle. Abducens motoneurons also showed responses to static lateral tilt which consisted of increases and decreases in firing with the recording side down and up, respectively, i.e., an a-otolith response (Anderson and Precht, 1979). Gravity responses were less frequently observed in abducens motoneurons when compared with trochlear motoneurons and, when present, the sensitivity was generally low. The canal and otolith inputs to trochlear and abducens neurons, determined with natural stimulation, are in perfect agreement with electrophysiological studies showing short-latency utricular inputs to ipsilateral abducens (Schwindt et al., 1973) and contralateral trochlear motoneurons (Baker et al., 1973). It is interesting to note that electrical stimulation of the utricular nerve did not reveal any short-latency inhibitory reflexes to antagonistic motoneurons, as in the case for reference, Precht, 1978). When trochlear motoneurons of canal-ocular reflexes (6. of hemilabyrinthectomized cats were studied during static tilt, responses were found that could only be explained by assuming an inhibitory otolith-ocular reflex as well (Blanks et al., 1978). Since they had escaped electrophysiological studies it must be assumed that they are polysynaptic in nature and were therefore depressed in anesthetized preparations. In summary, trochlear and abducens motoneurons receive very specific canal and otolith inputs and show very little orthogonal canal convergence. Contrary to the disynaptic inhibitory and excitatory canal-ocular reflexes, otolith-ocular reflexes appear to be disynaptic only when excitatory. To corroborate and extend the findings obtained with single motoneurons, simultaneous EMG recordings were obtained from i) the two lateral recti muscles, iij the medial (MR) and lateral (LR) recti muscles of the same eye, and iii) the superior (SO) and inferior oblique (10) muscles, during static and/or low frequency sinusoidal roll stimulation. At the low frequency of 0.025 Hz (Fig. 2A-D) the modulation of EMG activity is displacement related and at higher frequencies of
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Fig. 2. Reciprocal organization of the oblique and horizontal recti muscles during roll rotations. The response to low frequency rotations shown here demonstrates the pattern of responses to otolith inputs: on side down the EMG of the ipsilateral SO and LR and contralateral I 0 and MR increase while the contralaterat SO and LR decrease, e.g., SO,(A) and LR,(E) increase on left side down (i.e., acceleration right). The rotations used were 0.025 Hz,%20" in A-C and 0.25 Hz, %20"in D-F. The pulse trains corresponding to the EMG recordings were binned and averaged over 5-10 periods to give the cycle histograms shown. (From Anderson and Precht, 1979.)
rotation (Fig. 2E, F) the horizontal recti show a significant phase lag. Quantitative analysis is presented in Fig. 5 . As these records show, both the oblique (Fig. 2A-C) and horizontal (Fig. 2D-F) systems have a reciprocal organization of otolith inputs during roll, i.e., the SO and 10, SO, and SO,, LR, and LR, are synergistic pairs which can subserve the coordinated eye movements caused by otolith-ocular reflexes. A similar reciprocal relationship was noted in the muscle pairs: MR, and MR,1 0 , and 10, (not shown).
Responses of motoneurons to ramp changes in head position In the preceding section it has been shown that most trochlear and some abducens motoneurons respond to both canal and static otolithic stimuli. In this and the following sections we shall describe the behavior of motoneurons during stimuli such as ramp changes in head position and sinusoidal rotations (next section) about the longitudinal body axis (roll). Non-periodic ramp changes in roll-position produce angular acceleration pulses at the beginning and termination of the ramp which can activate the canals. In addition, otolith inputs are present due to the changing orientation of the animal's head with respect to gravity. The latter input predominates with slow changes in head positions whereas canals are recruited as the slopes of the ramps become greater. Typical examples of responses of a trochlear motoneuron to ramp changes in head position in roll are shown in Fig. 3. Slow transients of head position (Fig. 3A) produce changes in
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Fig. 3 . Response of trochlear motoneurons to ramp changes in roll position. The instantaneous frequency of the discharge of a single motoneuron is shown for changes in angular position from -2” (ipsi side down) to +25” (ipsi side up) with constant velocities of 3.3 (A) and 16.2 degrees/sec (B). (From Anderson et al., 1977.)
instantaneous firing rate which were nearly proportional or slightly lagging head displacement. The maximum discharge level is achieved only after arrival of the final displacement and then adapts, as in this neuron, to a new steady state level. With greater slopes of the ramp stimuli (Fig. 3B) and hence greater acceleration pulses at the onset and termination, the threshold for a canal response is exceeded, thereby producing a transient increase in discharge at the onset of the ramp and a decrease of firing following its termination. Following the canal transient, the firing continues to increase due to otolithic stimuli and finally adapts to a new level. Adaptation was observed in about 30% of the neurons. Ramps of the same magnitude but in the opposite direction yielded a slow decrease in firing, along with the fast canal transients. It should be pointed out that the canal induced transients had the same polarity as the otolith-evoked responses at the onset of ipsilateral side-up movements but were of opposite polarity at the termination of the ramp. The opposite pattern of activation was noted with transients from ipsilateral-up to ipsilateral-down. Abducens motoneurons showed a similar combination of canal and otolithic responses to ramp displacements in roll only when the animal’s head was oriented in such a way as to cause costimulation of the horizontal canals. When the latter were brought into a null-plane with respect to roll rotation, only otolith modulation of discharge rate was noted. However, it is important to emphasize that both the sensitivity and the number of otolith responses were smaller than in the trochlear neuron. The importance of this fact will be further discussed iri the next section. In short, the responses of motoneurons to ramp changes have shown that whenever canals are in the stimulating plane and the slope of the ramp is large enough to reach canal threshold, motoneurons are subjected to a combined canal-otolithic input. Gravity responses resulting from ramp changes lag head displacement more than primary otolith afferents (Anderson et al., 1978) indicating central processing of otolith afferent input. Further details of the dynamics of otolith processing will be given in the next section. Responses of motoneurons to sinusoidal stimulation The phase-gain response properties of single trochlear and abducens motoneurons as well as the EMGs of the corresponding muscles were recorded during sinusoidal rotation (Anderson et al., 1977; Blanks et al., 1978; Anderson and Precht, 1979). As already shown in the preceding section, roll stimulation activates both canal and otolith inputs to trochlear motoneurons, whereas rotation in yaw leads to canal activation only provided the contralateral posterior and ipsilateral anterior canals
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have some component in the plane of horizontal rotation. The otolith component of the combined canal-otolith response may then be obtained by vectorially subtracting the yaw (canal only) from the roll (canal and otolith) responses. To test the validity of the subtraction method we have then compared the calculated frequency responses of the otolith input to trochlear motoneurons with that obtained for abducens motoneurons and lateral rectus muscle in roll (an otolith input only, provided the horizontal canals are perpendicular to roll plane). The averaged responses of trochlear motoneurons during rotation in both yaw and roll are shown in Fig. 4. In yaw, the motoneuron's phase lags increase as the frequency of rotation increases (0,Fig. 4). Also, the phase lags of motoneurons are larger at all frequencies as compared to those of the primary canal afferents (A, Fig. 4); the upper-left shaded area in Fig. 4 indicates the central processing (integration) of canal inputs. It should be noted that these experiments were done under light ketamine anesthesia which influences the central integration process resulting in smaller phase values. When the same population of motoneurons were studied in roll (0, Fig. 4), the phase lag decreases as the frequency of rotation increases. Since the phase in both cases was measured with respect to the acceleration excitatory for the contralateral posterior canal, the yaw and roll phase behavior would have been identical if there were only canal input. Therefore, the phase differences between yaw and roll responses can only be due to the otolith input present in roll. It is apparent that at low frequencies, where the canal input is small relative to otolith input, the phase of trochlear motoneurons in roll is largely determined by the otolith input which, from previous sections, have a DC response maximum with ipsilateral side-up position (-6) in Fig. 4). At higher frequencies, the phase of the roll response is largely determined by the canal input, which increases as the frequency squared. Carefully considering the various problems of the vectorial subtraction procedure (Blanks et al., 1978) the yaw, response vector (gain,, phase,) was subtracted from the roll(r) vector (gain,, phase,) for each frequency. An example of one such calculation is shown by the insert in Fig. 4. The results of this procedure are shown by the lowest dashed line and X ' S in Fig. 4. It can be seen that the phases of the otolith response show a lag of 10"-90"over the frequency range, 0.025-0.5 Hz. These are relative to angular displacement which is proportional to the gravity input to otoliths. The difference between these calculated values for trochlear neurons and those obtained from primary otolith fibers (A, Fig. 4) (Anderson et al., 1978) are given by the shaded zone in the lower part of Fig. 4. Obviously, the signal in the otolith-ocular pathway undergoes central transformations similar to those in the canal-ocular path, i.e., phases and gains increase and decrease, respectively, with increasing frequency indicating central integration. The lag dynamics noted in the ramp studies (Fig. 3) are consistent with the results obtained in the frequency domain. The phase values relative to displacement for the abducens motoneuron response and the EMG activity of lateral and medial recti muscles during sinusoidal stimulation in roll (otolith only) are shown in Fig. 5 (Anderson and Precht, 1979). These values are, indeed, very similar to those calculated for trochlear motoneurons. This similarity indicates that the subtraction method is valid for calculation of otolith input during roll, and that otolith processing is similar for the horizontal and vertical eye movement systems. The central structures necessary for this processing of the afferent activities are still unknown. However, some data obtained from the vestibular nuclei (Melvill Jones and
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Fig. 4. Canal and otolith contributions to the motor output of trochlear motoneurons (TMns). The responses of 10 TMns during both yaw and roll (mean values shown by 0,0 , resp.) were used to calculate the otolith contribution (Y,) to the motor output. This entailed a vectorial subtraction of the yaw (Yc, canal only input) from the roll (Tcmrcanal plus macular input) response, as indicated in the insert. The mean 51 SD of these calculations are shown by the symbol X and the vertical bars. For comparison, the mean phases and gains for the canal (A) and otolith (A) afferents (Anderson et al., 1978) are shown. The vertical bars include ?1 SD. Note that the stippled areas represent the difference between the afferent inputs and the motoneuron outputs. Thus it is evident that for both the canal and otolith systems there is extensive central processing of the afferent activities. (From Blanks et al., 1978.)
Milsum, 1969) indicates that responses of secondary vestibular neurons already differ significantly from those of vestibular afferents. During the course of our experiments we often recorded from axons of vestibular neurons within the trochlear nucleus which were monosynaptically driven by ipsilateral (Vi) or contralateral (Vc) vestibular nerve stimulation. Since it may be assumed that some of these axons terminate in the trochlear nucleus their response characteristics are of some interest. About half of the Vi and Vc axons showed responses to otolithic in addition to canal stimulation. The polarity of these responses was such that the excitatory Vc and inhibitory Vi axons could modulate the motoneuron discharge as described above. Thus, Vc axons were driven by the contralateral posterior canal and showed a @-otolithresponse; whereas Vi axons were exclusively activated by the ipsilateral anterior canal, and, when present, showed a-otolith responses. Also, the frequency response of these convergent units during yaw and roll sinusoidal rotations was very similar to those of trochlear motoneurons (Fig. 4) except that their phase lags were somewhat smaller. This finding also supports the notion that secondary vestibular axons projecting to motoneurons carry an otolithic signal that is already different from that of otolith afferents. Interestingly, we did not find any axons that carried a pure otolithic signal without canal components whereas the opposite, i.e., a canal response only, was seen in about half of the cases. Of course, these negative findings do not exclude the possible
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005 01 025 05 10 FREQUENCY (Hz1 Fig. 5. Phase behavior of otolith afferent and extraocular motor outputs during sinusoidal roll rotations. The calculated otolith-dependent responses of trochlear motoneurons (0,mean of 10 units) are shown together with the measured responses of abducens neurons (V, mean of 5 units) and the EMGs of the medial and lateral recti ( 0 ,mean of 3 animals). The hatched area encompassesthe mean 2 1SD for the responses of the otolith afferents. For all cases, the input reference is angular displacement: ipsilateral side up for the trochlear neurons and medial rectus EMGs and side down for abducens neurons and the lateral rectus EMGs. The stippled region shows the phases of a simple first order system, l / s + a, which approximates the motor outputs with time constants, l / a of 0.8-1.6 sec. (From Anderson and Precht, 1979.) 0 01
0025
existence of pure otolithic projections. If they were to terminate, for example, as thin fibers on dendritic ramifications of the motoneuron pool they may easily have escaped microelectrode search.
CONCLUSION AND SUMMARY In the present paper it has been shown that ocular motoneurons of the horizontal and vertical/oblique systems receive both canal and otolithic inputs and that these inputs are reciprocally organized. The functional importance of canal-otolithic convergence in vertical/oblique motoneurons, and probably also in horizontal motoneurons, is to extend the working range over a much wider frequency band than is provided by the simple canal VOR. This is particularly evident in trochlear motoneurons during roll rotation where the canal and otolith responses have the same polarity. At high frequencies, the canal system may, therefore, serve to compensate for the lag present in the otolith system in addition to its compensation for the visco-elastic properties of the eye. When the roll movement is stopped the responses of canal and otolith are of opposite polarities and may cancel one another. In this case, the canal response may serve to prevent the eye from overshooting its final position. On the other hand, the otolith input serves to compensate for the poor canal performance in the low frequency range and, of course, during static head displacement. It is interesting to note that the responses of vertical/rotatory motoneurons in roll, measured in the dark, are comparable to those found in the horizontal system in the presence of vision. Thus, whereas vision improves the insufficiencies of the canal-ocular response in yaw at low frequencies, the otolith
467
contribution in roll may be important for extending the lower frequency range of the vertical/rotatory vestibulo-ocular reflexes. The otolith responses found in the horizontal eye movers may also be important in roll and pitch rotation, because a contraction of the lateral and medial recti muscles, due to their insertions, can facilitate the vertical or rotatory eye movements. However, it should be noted that the otolith signal in the horizontal system was much weaker than that in vertical/rotatory muscles. When the dynamics of the central otolith signal were compared with those of peripheral afferents, a large difference was apparent suggesting that, as for the canal input, a leaky neural integrator is processing the otolithic afferent input. Pertinent to the present results is the work of Baarsma and Collewijn (1975), who have studied the phase and gain behavior of eye movements in the alert rabbit during horizontal linear accelerations. They found phase lags for the motor output very similar to those shown above for frequencies from 0.023 to 0.5 Hz.They report greater phase lags at the higher frequencies (180" at 1.2 Hz) which suggest that other factors (e.g., eyeballorbit visco-elastic properties) may be involved.
REFERENCES Anderson, J.H. and Precht, W. (1979) Otolith responses of extraocular muscles during sinusoidal roll rotations. Bruin Res., 160: 150-154. Anderson, J.H., Precht, W. and Blanks, R.H.I. (1977) Central processing in otolith-ocular reflex pathways. In Control of Gaze by Bruin Stem Neurons, R. Baker and A. Berthoz (Eds.), Elsevier, Amsterdam, pp. 253-260. Anderson, J.H., Blanks, R.H.I. and Precht, W. (1978) Response characteristics of semicircular canal and otolith systems in cat. I. Dynamic responses of primary vestibular fibers. Exp. Brain Res., 32: 491-507. Baarsma, E.A. and Collewijn, H. (1975) Eye movements due to linear accelerations in the rabbit. J. Physiol. (Lond.), 245: 227-247. Baker, R., Precht, W. and Berthoz, A. (1973) Synaptic connections to trochlear motoneurons determined by individual vestibular nerve branch stimulation in the cat. Bruin Res., 64: 402406. Blanks, R.H.I. and Precht, W. (1976) Functional characterization of primary vestibular afferents in the frog. Exp. Bruin Res., 25: 369-390. Blanks, R.H.I., Anderson, J.H. and Precht, W. (1978) Response characteristics of semicircular canal and otolith systems in cat. 11. Responses of trochlear motoneurons. Exp. Brain Res., 32: 509-528. Estes, M.S., Blanks, R.H.I. and Markham, C.H. (1975) Physiologic characteristics of vestibular first-order canal neurons in the cat. I. Response plane determination and resting discharge characteristics. J. Neurophysiol., 38: 1232-1 249. Fernhdez, C. and Goldberg, J.M. (1976a) Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. I. Response to static tilts and to long-duration centrifugal force. J. Neurophysiol., 39: 970-984. Fernhndez, C. and Goldberg, J.M. (1976b) Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. 111. Response dynamics. J. Neurophysiol., 39: 996-1008. Fleisch, A. (1922a) Tonische Labyrinthreflexe auf die Augenstellung. Pjliigers Arch., 194: 554-573. Reisch, A. (1922b) Das Labyrinth als beschleunigungsempfindendes Organ. Pfligers Arch ., 195: 499-5 15. Fluur, E. and Mellstrom, A. (1971) The otolith organs and their influence on oculomotor movements. Exp. Neurol., 30: 13%147. Jongkees, L.B.W. and Philipszoon, A.J. (1964) Electronystagmography. Actu oto-luryngol. (Stockh.), SUPPI.189: 1-111. Kleinschmidt, H.J. and Collewijn, H. (1975) A search for habituation of vestibulo-ocular reactions to rotatory and linear sinusoidal accelerations in the rabbit. Exp. Neurol., 45: 257-267.
468 Kohut, R.I. (1974) Vertical linear acceleration (otolithic-ocularresponses). Laryngoscope, 84: 1627-1662. Lorente de N6, R. (1932) The regulation of eye positions and movements induced by the labyrinth. Laryngoscope, 42: 233-332. Melvill Jones, G. and Milsum, J.H. (1969) Neural response of the vestibular system to translational acceleration. In Conference on Systems Analysis Approach to Neurophyswlogical Problems, Brainerd, Minnesota. Precht, W. (1978) Neuronal operations in the vestibular system. In Studies ofBrain Function, Vol. 2 , V. Braitenberg (Ed.), Springer-Verlag, Berlin-Heidelberg-New York, p. 226. Precht, W. and Baker, R. (1972) Synapticorganization of the vestibulo-trochlearpathway. Exp, Brain Res., 14: 158-184. Precht, W., Richter, A. and Grippo, J. (1969) Responses of neurones in cat’s abducens nuclei to horizontal angular acceleration. Pfliigers Arch., 309: 285-309. Richter, A. and Precht, W. (1968) Inhibition of abducens motoneurones by vestibular nerve stimulation. Brain Res., 11: 701-705. Schwindt, P.C., Richter, A. and Precht, W. (1973) Short latency utricular and canal input to ipsilateral abducens motoneurons. Brain Res., 60: 259-262. Suzuki, J.I., Tokumasu, K. and Goto, K. (1969) Eye movements from single utricular nerve stimulation in the cat. Acta oto-laryngol. (Stockh.), 68: 350-392. Van der Hoeve, J. and De Kliijn, A. (1917) Tonische Labyrinthreflexe auf die Augen. Pflugers Arch., 169: 241-262.