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Direction-Specific Vestibular and Visual Modulation of Fore- and Hindlimb Reflexes in Cats*
Direction-Specific Vestibular and Visual Modulation of Fore- and Hindlimb Reflexes in Cats* U. THODEN, J. DICHGANS, M. DOERR and Th. SAVIDES Neurologische Klinik, Abteilung f i r Neurophysiologie, Universitat Freiburg i. Br., 7800 Freiburg i. Br. (F.R.G.)
INTRODUCTION Modulation of spinal reflexes by neck and vestibular inputs is known since the original work by Magnus (1924). Large field visual motion information, mainly from the periphery of the visual field also exerts influence on posture (Dichgans et al., 1972, 1976). More specifically electrical stimulation of the frog’s optic nerve bilaterally yields short latency responses in neck, forelimb and hindlimb motoneurons (Maeda et al., 1977). With quasi physiological motion stimulation it was shown in a previous paper that a large visual stimulus rotating about the animals line of sight tonically modulates the excitability of hindlimb extensor and flexor motoneurons (Thoden et al., 1977). This reflex modulation in terms of directional specificity and amplitude was similar to that induced by body tilt. Since in the cat vestibular second order neurons are influenced by optokinetic stimuli (Bauer, 1976; Keller and Precht, 1978) a common pathway for both inputs from the brain stem to the spinal cord was assumed (Thoden e t al., 1977). The data of Maeda et al. (1977), however, suggest a separate tectospinal and vestibulospinal route in the frog. A decreasing vestibulospinal influence was found by Gernandt and Gilman (1959) and Thoden et al. (1978) for the forelimb as compared to the hindlimb. Similar results were obtained for the neck-to-spinal input (Wenzel et al., 1978). In this paper the craniocaudal organization of visuospinal influences was investigated and compared to vestibulospinal effects during body tilt.
METHODS The experiments were performed in 27 adult cats weighing between 2 and 3.5 kg, anesthetized with a mixture of oxygen, nitrogen and Fluothane during surgery. After surgery animals were immobilized for recording by repeated injections of gallamine triethiodide (FlaxediP) and artificially respirated after tracheal cannulation. During the recording the animals were under slight halothane anesthesia. *Supported by SonderforschungsbereichHirnforschung (SFB 70) der Deutschen Forschungsgemeinschaft (DFG).
212 In order to study monosynaptic reflexes afferents were electrically stimulated and mass potentials recorded from the efferent motoneuron. For anatomical reasons two different techniques were used for the fore- and hindlimb. 1. For forelimb repexes the cervical spinal cord was exposed by laminectomy from C4 to Thl in 15 cats. The dura was opened and the dorsal roots C&C8 were cut. The. proximal stump was then put on bipolar stimulation electrodes. Ventral roots were left intact. For recording the following nerves were prepared: the right deep radial nerve (DR) to the lateral head of the triceps, paradigmatic for an extensor muscle, and the right mixed ulnar nerve (ULN) to the flexor carpi ulnaris and the ulnar head of the flexor profundus digitorum as flexor muscles. These nerves were then mounted on bipolar silver-silverchloride recording electrodes (interpolar distance 3 mm). 2. For hindlimb reflexes the branch of the tibia1 nerve to the gastrocnemius-soleus muscle (GS) and the deep peroneal nerve (DP) to the tibialis anterior and the extensor digitorum longus muscles were prepared in the right popliteal fossa in another 12 cats. This time the peripheral nerve served for electrical stimulation by bipolar silversilverchloride electrodes and not for recording. Recordings were obtained from the ventral root after the spinal segments W S 2 were exposed by laminectomy. The dura was opened and ventral roots of the segments L 6 4 2 were filamented at their exit from the dura, then severed and the proximal stump attached to a silver-silverchloride recording electrode. The cord and the nerves were covered by a pool of warmed liquid paraffin at constant body temperature. Animals were placed in a modified Horsley-Clark headholder on a tilt table (Fa. Tonnies) with the body fixed at spinal processes. For steady state positional stimulation of the vestibular otoliths the animal was tilted 45" either to the left or to the right around its longitudinal body axis. For optokinetic stimulation, a large visual display rotated about the animals line of sight, 25 cm in front of the eyes at a speed ranging between 2-14 degreedsec. The surface of the disk was painted with randomly distributed large colored dots that covered 32% of its total surface. The disk subtended 130" of visual angle viewed binocularly. Both stimuli were combined in physiological and non-physiological directional combinations. Control experiments were performed in an upright position without display motion before each test trial. For evaluation, 32 reflex responses induced either by stimulation of the hindlimb nerves or the dorsal roots C4-Thl were averaged. For stimulation, single rectangular 0.2 msec impulses were applied every 3-5 sec. Stimulus intensities were tested at the reflex threshold and 1.3, 1.6, 2, 3 and 5 times the threshold value (T). Stimulation always started 30 sec after the animal was placed in the test position or 30 sec after onset of optokinetic stimulation. The modulation of the average response amplitudes produced by the different head and body tilts and optokinetic stimuli was expressed as a percentage of the average response amplitude in the upright position. RESULTS Tonic reflex modulation during animal tilt Ipsilatetal tilt produces an enhancement of monosynaptic extensor reflexes, whereas contralateral tilt produces an enhancement of monosynaptic flexor reflexes (Figs. 1 and 2, on the right).
213 opt o k i net ic
vesti bulor
r‘
L
TT
L-d L
a,
g’OII C
1 1
3
L
I
XI
+ - - a x 1
a, C
a,
Fig. 1 . Reflex modulation of flexor muscles in relation to relative intensity of electrical stimulation (threshold = 1) for pure optokinetic (left) and vestibular (right) stimulation. Average values of 5 cats with SD.
The reverse procedure causes inhibition. The maximal amount of modulation varies between 15 and 50%. It is usually reached at roughly 1.6 T. The amount of reflex modulation induced by vestibular stimuli falls off at higher stimulus intensities, although some modulation can still be detected at up to 5 T. The strongest reflex modulation is found during ipsilateral tilt in monosynaptic extensor reflexes. The vestibular modulation of monosynaptic flexor and extensor reflexes is generally stronger in the forelimb as compared to the hindlimb. This difference is more pronounced during ipsilateral tilt. Optokinetic reflex modulation As described elsewhere, optokinetic stimuli in the erect animal also produce a direction specific reflex modulation (Thoden et al., 1977). In agreement with its behavioral significance an enhancement is caused by contralateral display rotation for extensor reflexes and ipsilateral rotation for monosynaptic flexor reflexes. Standard deviations are similar to the ones observed with stimulation by exclusive body tilt stimulation (Figs. 1 and 2, on the left).
214 optokinetic
1
vest ibular
u 'C--
-
30'-
20"
! ! L
z
10.-
W
c d
0 .-
V
e
I
I1
Q
2 W C
-.l
d
.-0 0 Y
XI
Fig. 2. Reflex modulation of extensor muscles in relation to relative intensity of electrical stimulation (threshold = 1) for roll motion (left) and animal tilt (right). Average values of 5 cats with SD.
Similar amounts of optokinetic reflex modulation are found in the fore- and hindlimb. This contrasts to the craniocaudally decreasing vestibulospinal influence. The directional anisotropy of vestibular reflex modulation through body tilt is not observed with the exclusive application of large field motion of the visual scene.
Reflex modulation by different body tilt angles and different velocities of display rotation Vestibular modulation of monosynaptic reflexes at 1.6 T starts at tilt angles of about 10"to both sides and increases with larger tilt angles. For the hindlimb the slope of the curve relating body tilt to reflex modulation is steeper for extensor than for monosynaptic flexor reflexes (Fig. 3B,D). Tilt angles exceeding 45"could not be applied for technical reasons. The optokinetic modulation of monosynaptic reflexes depends on the angular velocity of roll motion. It reaches its maximum between 3.5-7 degrees/sec and falls off at velocities exceeding 10 degrees/sec. It seems that in both extensor and flexor monosynaptic reflexes the optokinetic reflex enhancement is larger than the inhibition (Fig. 3A,C).
215 optokinetic
vestibular X’
A
B
1/
C
r-=
20
5
lot
L
“3
L
20-
30r
D
/---
L
K
Z
Fig. 3. Reflex modulation by different body tilt angles (right) and different velocities of display rotation (left) for reflexes of 1.6 x the threshold intensity.
Simultaneous optokinetic and vestibular stimulation For the hindlimb, the physiological combination of both stimuli, e.g. body tilt to the right combined with counterclockwise display rotation results in modulation curves similar to the one obtained with exclusive body tilt (Fig. 4). With the stimulus parameters used summation of optokinetic and vestibular effects, if at all present, could only be detected near the threshold intensity of electrical stimulation as defined by control experiments. But this difference was not significant with the sample taken. With a non-physiological combination of stimulus directions again no interaction could be demonstrated. It seemed as if the reflex modulation whenever using combined optokinetic and vestibular stimulation was exclusively determined by the vestibular signal. DISCUSSION The demonstration of an optokinetically induced spinal reflex modulation fits behavioral experiments in man (Dichgans et al., 1972,1976; Lee and Aronson, 1974; Lestienne et al., 1977). These demonstrate that the body’s center of gravity in upright stance may be displaced towards the direction of motion of an ample visual stimulus. By comparing postural sway with eyes open vs. eyes closed it can be shown that physiologically vision stabilizes posture. A frequency analysis of the visual effect
216 optokinetic
combined with vestibular
T
9
'"
L
I
XI
C al
D
30
.
-.1
10
XI
Fig. 4. Simultaneous optokinetic and vestibular stimulation. On the right physiological combination, e.g., body tilt to one side combined with counterclockwise display rotation, compared with the non-physiological combination on the left.
suggests that the domain of visual influences upon body posture is below 1 Hz, whereas that of the vestibulospinal effects covers higher frequencies (Dichgans et al., 1976; Mauritz et al., 1975; Lestienne et al., 1977). These behavioral data fit the results presented in Fig. 3, where the optokinetic modulation reaches saturation at very low velocities. The underlying mechanism is behaviorally adaptive. An animal inadvertently swaying or falling towards one side is not only protected by vestibulospinal reflexes but also by external visuospinal feedback. The modulation of spinal reflexes by tilt reflects vestibulospinal connections as previously described (Anderson and Gernandt, 1956; Lund and Pompeiano, 1968; Roberts, 1970; Wilson and Yoshida, 1968). Gernandt investigated the cranio-caudal organization of the decending connections using single shock vestibular nerve stimulation. This results in an early large bilateral response spike, which is immediately followed by a smaller double wave in the forelimb. At the lumbar level only the late response is seen. This indicates more direct, stronger and denser connections influencing the cervical than lumbar segments (Gernandt and Gilman, 1959; Erulkar et al., 1966). The quantification of response modulations by vestibulospinal mechanisms presented above substantiates this finding and allows for a comparison with effects of other postural control mechanisms. The neck input to spinal reflexes is also known to
217 decrease in craniocaudal direction (Wenzel et al., 1978). In so far the craniocaudal distribution of both systems seems similar, but the neck afferents counteract the described vestibulospinal effects (Erhard and Wagner, 1970; Rosenberg and Lindsay, 1973). Finally, a prevalence of descending connections to the forelimb is also known for the tectospinal tract (Nyberg-Hansen, 1964). The fact that the difference in modulation curves for fore- and hindlimbs cannot be demonstrated for visuospinal mechanisms at first glance suggests a different pathway, as proposed by Maeda et al. (1977). A bias of vestibulospinal information flow by optokinetic stimuli, however, would be expected, since it was shown for semicircular canal dependent neurons in the vestibular nuclei of goldfish (Dichgans et al., 1973), cat (Bauer, 1976; Keller and Precht, 1978) and monkey (Henn et al., 1974) and also for otolith dependent neurons of the cat (Daunton and Thomsen, 1976). Similar conclusions may be drawn from our experiments with combined stimulation of both input channels. They show neither summation nor mutual inhibition, but rather a predominance of vestibular effects. Similar results have been obtained in recording from the vestibular nuclei for canal stimulation in the monkey (Waespe and Henn, 1977). Our data are not sufficient to definitely answer this question. The visuospinal pathway remains unknown until visual effects are directly recorded from identified neurons. SUMMARY The influence of large visual stimuli rotating about the animals' line of sight on electrically elicited monosynaptic fore- and hindlimb reflexes was compared with the effect of a 45" static body tilt. Both extensor and flexor reflexes were tested in the forelimb (branch to lateral head of m. triceps and ulnar nerve) and the hindlimb (tibia1 and peroneal nerve). Static body tilt enhances ipsilateral monosynaptic extensor reflexes up to 30% and inhibits flexor reflexes to a lesser degree. Contralateral reflexes show reversed effects. Vestibular reflex modulation is stronger in the fore- than in the hindlimb. Optokinetic roll motion stimuli also produce direction-specific reflex modulations, but with the reverse directional characteristic: equal effects of body tilt, e.g., to the right and pattern motion to the left. The amount of optokinetic modulation is very similar in fore- and hindlimb reflexes. Whereas it is largely identical to vestibular modulation in hindlimb reflexes, the latter is stronger in forelimb reflexes. If combined, the effects of both stimuli do not summate. The results are interpreted as being due to a vestibulospinal biasing of alpha motoneurons. It is not clear whether optokinetic effects exclusively use these pathways. REFERENCES Anderson, S. and Gernandt, B.E. (1956) Ventral root discharge in response to vestibular and propnoceptive stimulation.J. Neurophysiol., 19: 524-543. Bauer, R. (1976) Optisch-vestibuliire Znteraktion an Einzel-neuronen der Vestibdariskerne und des Vestibulo-cerebellum bei der Katze. Biol. Diss., Freiburg. Berthoz, A. and Anderson, J.A. (1971) Frequency analysis of vestibular influence on extensor motoneurons. 11. Relationship between neck and forelimb extensors. Brain Res., 34: 376-380.
218 Daunton. N.G. and Thomsen, D.D. (1976) Otolith-visual interactions in single units of cat vestibular nuclei. Neurosci. Abstr., 11: 1057, no. 1526. Dichgans, J., Schmidt, C.L. and Graf, W. (1973) Visual input improves the speedometer function of the vestibular nuclei in the goldfish. Exp. Brain Res., 18: 319-322. Dichgans. J., Held, R., Young, L. and Brandt, Th. (1972) Moving visual scenes influence the apparent direction of gravity. Scierice, 178: 1217-1219. Dichgans, J.. Mauritz, K.H., Allum, J.H.H. and Brandt, Th. (1976) Postural sway in normals and atactic patients: analysis of the stabilizing and destabilizing effects of vision. Agressologie, 17C: 15-24. Ehrhardt. K.J. and Wagner, A. (1970) Labyrinthine and neck reflexes recorded from spinal single motoneurons in the cat. Brain Res.. 19: 87-104. Erulkar. S.D.. Sprague. J.M., Whitsel, B.L., Dogan, S. and Janetta, P.J. (1966) Organization of the vestibular projection to the spinal cord of the cat. J. Neurophysiol., 29: 626-664. Gernandt. B.E. and Gilman, S. (1959) Descending vestibular activity and its modulation by proprioceptive, cerebellar and reticular influences. Exp. Neurol., 1: 274-304. Henn. V., Young, R.L. and Finley, C. (1974) Vestibular nucleus units in alert monkeys are also influenced by moving visual fields. Brairi Res., 71: 144-149. Keller. E.L. and Precht, W. (1978) Persistence of visual response in vestibular nucleus neurons in cerebellectoniized cat. Exp. Brain Rex. 32: 591-594. Lee. D.L. and Aronson, E. (1974) Visual proprioceptive control of standing in human infants. Percept. P s ~ c h o p ~ ~ y15: s . . 529-532. Lestienne. F., Soechting, J. and Berthoz, A. (1977) Postural readjustments induced by linear motion of visual scenes. Exp. Brain Res., 28: 363-384. Lund. S. and Ponipeiano, 0. (1968) Monosynaptic excitation of alpha motoneurons from supraspinal structures in the cat. Acra physiol. scatid., 73: 1-21. Maeda. M.. Magherini, P.C. and Precht, W. (1977) Functional organization of vestibular and visual inputs to neck and forelimb motoneurons in the frog. J. Neurophysiol., 40: 225-243. Magnus, R. (1 924) Kiirpersrellurig. Julius Springer, Berlin. Mauritz. K.H.. Dichgans. J., Allum, J.H.J. and Brandt, Th. (1975) Frequency characteristics of postural sway in response to self-induced and conflicting visual stimulation. Pflugers Arch., 355: R 95, no. 189. Nyberg-Hansen, R. (1964) The location and termination of tectospinal fibres in the cat. Exp. Neurol., 9: Z 12-22 7. Roberts, T.D.M. (1970) Changes in stretch reflexes in limb extensor muscles during position reflexes from the labyrinth in the cat. J. Physiol (Lorid.), 211: 5P-6P. Rosenberg, J.R. and Lindsay, K.W. (1973) Asymmetric tonic labyrinthine reflexes. Brain Res., 63: 347-350. Thoden, U., Dichgans, J. and Savidis, Th. (1977) Direction specific optokinetic modulation of monosynaptic hindlimb reflexes in cats. Exp. Brain Res., 30: 155-160. Thoden, U., Dichgans, J., Doerr, M. and Savidis, Th. (1978) Direction specific vestibular and visual modulation of monosynaptic fore- and hindlimb reflexes in cats. Pfliigers Arch., Suppl. 373: R 86. Waespe, W.and H e m , V. (1977) Neuronal activity in the vestibular nuclei of the alert monkey during vestibular and optokinetic stimulation. Exp. Brain Res., 27: 523-538. Wenzel, D., Thoden, U. and Frank, A. (1978) Forelimb reflexes modulated by tonic neck positions in cats. PPiigers Arch., 374: 107-113. Wilson, V.J. and Yoshida, M. (1968) Vestibulospinal and reticulospinal effects on hindlimb, forelimb and neck alpha motoneurons of the cat. Proc. Nut. Acad. Sci. (Wash.), 60: 836-840.
INTRODUCTION Modulation of spinal reflexes by neck and vestibular inputs is known since the original work by Magnus (1924). Large field visual motion information, mainly from the periphery of the visual field also exerts influence on posture (Dichgans et al., 1972, 1976). More specifically electrical stimulation of the frog’s optic nerve bilaterally yields short latency responses in neck, forelimb and hindlimb motoneurons (Maeda et al., 1977). With quasi physiological motion stimulation it was shown in a previous paper that a large visual stimulus rotating about the animals line of sight tonically modulates the excitability of hindlimb extensor and flexor motoneurons (Thoden et al., 1977). This reflex modulation in terms of directional specificity and amplitude was similar to that induced by body tilt. Since in the cat vestibular second order neurons are influenced by optokinetic stimuli (Bauer, 1976; Keller and Precht, 1978) a common pathway for both inputs from the brain stem to the spinal cord was assumed (Thoden e t al., 1977). The data of Maeda et al. (1977), however, suggest a separate tectospinal and vestibulospinal route in the frog. A decreasing vestibulospinal influence was found by Gernandt and Gilman (1959) and Thoden et al. (1978) for the forelimb as compared to the hindlimb. Similar results were obtained for the neck-to-spinal input (Wenzel et al., 1978). In this paper the craniocaudal organization of visuospinal influences was investigated and compared to vestibulospinal effects during body tilt.
METHODS The experiments were performed in 27 adult cats weighing between 2 and 3.5 kg, anesthetized with a mixture of oxygen, nitrogen and Fluothane during surgery. After surgery animals were immobilized for recording by repeated injections of gallamine triethiodide (FlaxediP) and artificially respirated after tracheal cannulation. During the recording the animals were under slight halothane anesthesia. *Supported by SonderforschungsbereichHirnforschung (SFB 70) der Deutschen Forschungsgemeinschaft (DFG).
212 In order to study monosynaptic reflexes afferents were electrically stimulated and mass potentials recorded from the efferent motoneuron. For anatomical reasons two different techniques were used for the fore- and hindlimb. 1. For forelimb repexes the cervical spinal cord was exposed by laminectomy from C4 to Thl in 15 cats. The dura was opened and the dorsal roots C&C8 were cut. The. proximal stump was then put on bipolar stimulation electrodes. Ventral roots were left intact. For recording the following nerves were prepared: the right deep radial nerve (DR) to the lateral head of the triceps, paradigmatic for an extensor muscle, and the right mixed ulnar nerve (ULN) to the flexor carpi ulnaris and the ulnar head of the flexor profundus digitorum as flexor muscles. These nerves were then mounted on bipolar silver-silverchloride recording electrodes (interpolar distance 3 mm). 2. For hindlimb reflexes the branch of the tibia1 nerve to the gastrocnemius-soleus muscle (GS) and the deep peroneal nerve (DP) to the tibialis anterior and the extensor digitorum longus muscles were prepared in the right popliteal fossa in another 12 cats. This time the peripheral nerve served for electrical stimulation by bipolar silversilverchloride electrodes and not for recording. Recordings were obtained from the ventral root after the spinal segments W S 2 were exposed by laminectomy. The dura was opened and ventral roots of the segments L 6 4 2 were filamented at their exit from the dura, then severed and the proximal stump attached to a silver-silverchloride recording electrode. The cord and the nerves were covered by a pool of warmed liquid paraffin at constant body temperature. Animals were placed in a modified Horsley-Clark headholder on a tilt table (Fa. Tonnies) with the body fixed at spinal processes. For steady state positional stimulation of the vestibular otoliths the animal was tilted 45" either to the left or to the right around its longitudinal body axis. For optokinetic stimulation, a large visual display rotated about the animals line of sight, 25 cm in front of the eyes at a speed ranging between 2-14 degreedsec. The surface of the disk was painted with randomly distributed large colored dots that covered 32% of its total surface. The disk subtended 130" of visual angle viewed binocularly. Both stimuli were combined in physiological and non-physiological directional combinations. Control experiments were performed in an upright position without display motion before each test trial. For evaluation, 32 reflex responses induced either by stimulation of the hindlimb nerves or the dorsal roots C4-Thl were averaged. For stimulation, single rectangular 0.2 msec impulses were applied every 3-5 sec. Stimulus intensities were tested at the reflex threshold and 1.3, 1.6, 2, 3 and 5 times the threshold value (T). Stimulation always started 30 sec after the animal was placed in the test position or 30 sec after onset of optokinetic stimulation. The modulation of the average response amplitudes produced by the different head and body tilts and optokinetic stimuli was expressed as a percentage of the average response amplitude in the upright position. RESULTS Tonic reflex modulation during animal tilt Ipsilatetal tilt produces an enhancement of monosynaptic extensor reflexes, whereas contralateral tilt produces an enhancement of monosynaptic flexor reflexes (Figs. 1 and 2, on the right).
213 opt o k i net ic
vesti bulor
r‘
L
TT
L-d L
a,
g’OII C
1 1
3
L
I
XI
+ - - a x 1
a, C
a,
Fig. 1 . Reflex modulation of flexor muscles in relation to relative intensity of electrical stimulation (threshold = 1) for pure optokinetic (left) and vestibular (right) stimulation. Average values of 5 cats with SD.
The reverse procedure causes inhibition. The maximal amount of modulation varies between 15 and 50%. It is usually reached at roughly 1.6 T. The amount of reflex modulation induced by vestibular stimuli falls off at higher stimulus intensities, although some modulation can still be detected at up to 5 T. The strongest reflex modulation is found during ipsilateral tilt in monosynaptic extensor reflexes. The vestibular modulation of monosynaptic flexor and extensor reflexes is generally stronger in the forelimb as compared to the hindlimb. This difference is more pronounced during ipsilateral tilt. Optokinetic reflex modulation As described elsewhere, optokinetic stimuli in the erect animal also produce a direction specific reflex modulation (Thoden et al., 1977). In agreement with its behavioral significance an enhancement is caused by contralateral display rotation for extensor reflexes and ipsilateral rotation for monosynaptic flexor reflexes. Standard deviations are similar to the ones observed with stimulation by exclusive body tilt stimulation (Figs. 1 and 2, on the left).
214 optokinetic
1
vest ibular
u 'C--
-
30'-
20"
! ! L
z
10.-
W
c d
0 .-
V
e
I
I1
Q
2 W C
-.l
d
.-0 0 Y
XI
Fig. 2. Reflex modulation of extensor muscles in relation to relative intensity of electrical stimulation (threshold = 1) for roll motion (left) and animal tilt (right). Average values of 5 cats with SD.
Similar amounts of optokinetic reflex modulation are found in the fore- and hindlimb. This contrasts to the craniocaudally decreasing vestibulospinal influence. The directional anisotropy of vestibular reflex modulation through body tilt is not observed with the exclusive application of large field motion of the visual scene.
Reflex modulation by different body tilt angles and different velocities of display rotation Vestibular modulation of monosynaptic reflexes at 1.6 T starts at tilt angles of about 10"to both sides and increases with larger tilt angles. For the hindlimb the slope of the curve relating body tilt to reflex modulation is steeper for extensor than for monosynaptic flexor reflexes (Fig. 3B,D). Tilt angles exceeding 45"could not be applied for technical reasons. The optokinetic modulation of monosynaptic reflexes depends on the angular velocity of roll motion. It reaches its maximum between 3.5-7 degrees/sec and falls off at velocities exceeding 10 degrees/sec. It seems that in both extensor and flexor monosynaptic reflexes the optokinetic reflex enhancement is larger than the inhibition (Fig. 3A,C).
215 optokinetic
vestibular X’
A
B
1/
C
r-=
20
5
lot
L
“3
L
20-
30r
D
/---
L
K
Z
Fig. 3. Reflex modulation by different body tilt angles (right) and different velocities of display rotation (left) for reflexes of 1.6 x the threshold intensity.
Simultaneous optokinetic and vestibular stimulation For the hindlimb, the physiological combination of both stimuli, e.g. body tilt to the right combined with counterclockwise display rotation results in modulation curves similar to the one obtained with exclusive body tilt (Fig. 4). With the stimulus parameters used summation of optokinetic and vestibular effects, if at all present, could only be detected near the threshold intensity of electrical stimulation as defined by control experiments. But this difference was not significant with the sample taken. With a non-physiological combination of stimulus directions again no interaction could be demonstrated. It seemed as if the reflex modulation whenever using combined optokinetic and vestibular stimulation was exclusively determined by the vestibular signal. DISCUSSION The demonstration of an optokinetically induced spinal reflex modulation fits behavioral experiments in man (Dichgans et al., 1972,1976; Lee and Aronson, 1974; Lestienne et al., 1977). These demonstrate that the body’s center of gravity in upright stance may be displaced towards the direction of motion of an ample visual stimulus. By comparing postural sway with eyes open vs. eyes closed it can be shown that physiologically vision stabilizes posture. A frequency analysis of the visual effect
216 optokinetic
combined with vestibular
T
9
'"
L
I
XI
C al
D
30
.
-.1
10
XI
Fig. 4. Simultaneous optokinetic and vestibular stimulation. On the right physiological combination, e.g., body tilt to one side combined with counterclockwise display rotation, compared with the non-physiological combination on the left.
suggests that the domain of visual influences upon body posture is below 1 Hz, whereas that of the vestibulospinal effects covers higher frequencies (Dichgans et al., 1976; Mauritz et al., 1975; Lestienne et al., 1977). These behavioral data fit the results presented in Fig. 3, where the optokinetic modulation reaches saturation at very low velocities. The underlying mechanism is behaviorally adaptive. An animal inadvertently swaying or falling towards one side is not only protected by vestibulospinal reflexes but also by external visuospinal feedback. The modulation of spinal reflexes by tilt reflects vestibulospinal connections as previously described (Anderson and Gernandt, 1956; Lund and Pompeiano, 1968; Roberts, 1970; Wilson and Yoshida, 1968). Gernandt investigated the cranio-caudal organization of the decending connections using single shock vestibular nerve stimulation. This results in an early large bilateral response spike, which is immediately followed by a smaller double wave in the forelimb. At the lumbar level only the late response is seen. This indicates more direct, stronger and denser connections influencing the cervical than lumbar segments (Gernandt and Gilman, 1959; Erulkar et al., 1966). The quantification of response modulations by vestibulospinal mechanisms presented above substantiates this finding and allows for a comparison with effects of other postural control mechanisms. The neck input to spinal reflexes is also known to
217 decrease in craniocaudal direction (Wenzel et al., 1978). In so far the craniocaudal distribution of both systems seems similar, but the neck afferents counteract the described vestibulospinal effects (Erhard and Wagner, 1970; Rosenberg and Lindsay, 1973). Finally, a prevalence of descending connections to the forelimb is also known for the tectospinal tract (Nyberg-Hansen, 1964). The fact that the difference in modulation curves for fore- and hindlimbs cannot be demonstrated for visuospinal mechanisms at first glance suggests a different pathway, as proposed by Maeda et al. (1977). A bias of vestibulospinal information flow by optokinetic stimuli, however, would be expected, since it was shown for semicircular canal dependent neurons in the vestibular nuclei of goldfish (Dichgans et al., 1973), cat (Bauer, 1976; Keller and Precht, 1978) and monkey (Henn et al., 1974) and also for otolith dependent neurons of the cat (Daunton and Thomsen, 1976). Similar conclusions may be drawn from our experiments with combined stimulation of both input channels. They show neither summation nor mutual inhibition, but rather a predominance of vestibular effects. Similar results have been obtained in recording from the vestibular nuclei for canal stimulation in the monkey (Waespe and Henn, 1977). Our data are not sufficient to definitely answer this question. The visuospinal pathway remains unknown until visual effects are directly recorded from identified neurons. SUMMARY The influence of large visual stimuli rotating about the animals' line of sight on electrically elicited monosynaptic fore- and hindlimb reflexes was compared with the effect of a 45" static body tilt. Both extensor and flexor reflexes were tested in the forelimb (branch to lateral head of m. triceps and ulnar nerve) and the hindlimb (tibia1 and peroneal nerve). Static body tilt enhances ipsilateral monosynaptic extensor reflexes up to 30% and inhibits flexor reflexes to a lesser degree. Contralateral reflexes show reversed effects. Vestibular reflex modulation is stronger in the fore- than in the hindlimb. Optokinetic roll motion stimuli also produce direction-specific reflex modulations, but with the reverse directional characteristic: equal effects of body tilt, e.g., to the right and pattern motion to the left. The amount of optokinetic modulation is very similar in fore- and hindlimb reflexes. Whereas it is largely identical to vestibular modulation in hindlimb reflexes, the latter is stronger in forelimb reflexes. If combined, the effects of both stimuli do not summate. The results are interpreted as being due to a vestibulospinal biasing of alpha motoneurons. It is not clear whether optokinetic effects exclusively use these pathways. REFERENCES Anderson, S. and Gernandt, B.E. (1956) Ventral root discharge in response to vestibular and propnoceptive stimulation.J. Neurophysiol., 19: 524-543. Bauer, R. (1976) Optisch-vestibuliire Znteraktion an Einzel-neuronen der Vestibdariskerne und des Vestibulo-cerebellum bei der Katze. Biol. Diss., Freiburg. Berthoz, A. and Anderson, J.A. (1971) Frequency analysis of vestibular influence on extensor motoneurons. 11. Relationship between neck and forelimb extensors. Brain Res., 34: 376-380.
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