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Symposium on the Role of the Vestibular Organs in Space Exploration (1970)

Chapter: VESTIBULAR ACTIVITY IN THE DESCENDING MEDIAL LONGITUDINAL FASCICULUS

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Suggested Citation:"VESTIBULAR ACTIVITY IN THE DESCENDING MEDIAL LONGITUDINAL FASCICULUS." National Research Council. 1970. Symposium on the Role of the Vestibular Organs in Space Exploration. Washington, DC: The National Academies Press. doi: 10.17226/18593.
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Suggested Citation:"VESTIBULAR ACTIVITY IN THE DESCENDING MEDIAL LONGITUDINAL FASCICULUS." National Research Council. 1970. Symposium on the Role of the Vestibular Organs in Space Exploration. Washington, DC: The National Academies Press. doi: 10.17226/18593.
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Page 238
Suggested Citation:"VESTIBULAR ACTIVITY IN THE DESCENDING MEDIAL LONGITUDINAL FASCICULUS." National Research Council. 1970. Symposium on the Role of the Vestibular Organs in Space Exploration. Washington, DC: The National Academies Press. doi: 10.17226/18593.
×
Page 239
Suggested Citation:"VESTIBULAR ACTIVITY IN THE DESCENDING MEDIAL LONGITUDINAL FASCICULUS." National Research Council. 1970. Symposium on the Role of the Vestibular Organs in Space Exploration. Washington, DC: The National Academies Press. doi: 10.17226/18593.
×
Page 240
Suggested Citation:"VESTIBULAR ACTIVITY IN THE DESCENDING MEDIAL LONGITUDINAL FASCICULUS." National Research Council. 1970. Symposium on the Role of the Vestibular Organs in Space Exploration. Washington, DC: The National Academies Press. doi: 10.17226/18593.
×
Page 241
Suggested Citation:"VESTIBULAR ACTIVITY IN THE DESCENDING MEDIAL LONGITUDINAL FASCICULUS." National Research Council. 1970. Symposium on the Role of the Vestibular Organs in Space Exploration. Washington, DC: The National Academies Press. doi: 10.17226/18593.
×
Page 242
Suggested Citation:"VESTIBULAR ACTIVITY IN THE DESCENDING MEDIAL LONGITUDINAL FASCICULUS." National Research Council. 1970. Symposium on the Role of the Vestibular Organs in Space Exploration. Washington, DC: The National Academies Press. doi: 10.17226/18593.
×
Page 243
Suggested Citation:"VESTIBULAR ACTIVITY IN THE DESCENDING MEDIAL LONGITUDINAL FASCICULUS." National Research Council. 1970. Symposium on the Role of the Vestibular Organs in Space Exploration. Washington, DC: The National Academies Press. doi: 10.17226/18593.
×
Page 244

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Vestibular Activity in the Descending Medial Longitudinal Fasciculus *'2 Bo E. GERNANDT Naval Aerospace Medical Institute SUMMARY The functional importance of the medial longitudinal fasciculus (MLF) in carrying vestibular impulses into the spinal cord has been studied in cats. The amplitude, duration, and latency of the gross motor responses evoked by vestibular stimulation and recorded from cervical and lumbar levels do not show any significant or persistent changes after a selective bilateral disconnection of the descend- ing MLF. Thus, in evaluating the hierarchical importance of the three descending vestibulofugal pathways, it becomes obvious that the MLF offers a much weaker link than the connections represented by the vestibulospinal and reticulospinal tracts. By sectioning all pathways other than the MLF in the brainstem at the cerebellopontine angle, this tract could be investigated in anatomical isolation from adjacent vestibular connections. Vestibular stimulation applied to this "MLF animal" prepara- tion evoked motor responses which could be recorded as far down as midthoracic levels. No sign of activity was ever recorded from lumbosacral levels. Judged by the response, the MLF seems to have a homogeneous fiber spectrum, and the mean speed of conduction of the neurons is about 63 m/sec. Single MLF axon recordings demonstrated that the discharge frequency in response to vestibular stimulation may reach values that are more than twice the value of ventral-root a-fiber discharge in response to identical stimulation, and that the synaptic transmission across the vestibular nuclei occurs with a considerable safety factor. Excitatory and inhibitory postsynaptic potentials evoked by ves- tibular activity conducted in the MLF have been recorded intracellularly from flexor and extensor motoneurons at cervical levels, but the relative amounts of excitatory or inhibitory action on a test motoneuron are variable. Pure EPSP's or IPSP's can be recorded, but the majority of motoneurons showed EPSP's; the long latencies of each were approximately the same and indicate that spinal inter- neurons are involved in the transmission. These depolarizing and hyperpolarizing effects could be recorded in a random fashion from flexor and extensor neurons, as identified by antidromic stimulation, but no consistent sign of reciprocity was obtained when recording from neurons with antagonistic function. INTRODUCTION Among a multiplicity of descending pathways available for conducting impulses into the spinal cord are three tracts—the vestibulospinal, the reticulospinal, and the medial longitudinal fas- 1 The animals used in this study were handled in accord- ance with the "Principles of Laboratory Animal Care" estab- lished by the Committee on the Guide for Laboratory Animal Resources, National Academy of Sciences-National Research Council. 2 An expanded report appears in Exptl. Neurol., vol. 22, 1968. pp. 326-342. ciculus (MLF)—which place spinal motor cells under the reflex control of the vestibular appara- tus. The functional significance of the first two tracts has been studied extensively during the last decade (ref. 1), and the amount of neuro- anatomical work that has gone into the elucida- tion of the details of these pathways is consider- able (ref. 2). However, some experimental attempts to obtain information about the impor- tance of the descending portion of the MLF have not been successful, largely because of specific inherent limitations which preclude complete systematic investigation (ref. 3). The anatomical 237

238 THE ROLE OF THE VESTIBULAR ORGANS IN SPACE EXPLORATION properties of the fiber groups which compose col- lectively the MLF have attracted attention as well as occasional disagreement. It is known that the fibers of the MLF originate in the medial, and probably the spinal, vestibular nuclei and descend in the homolateral as well as the con- tralateral fasciculus. The extent of the descend- ing tract in the spinal cord and the manner by which the fibers articulate with the ventral horn cells have been studied (refs. 4 and 5), but to what degree this tract participates in spinal activity has been evaluated in various ways. A report describing primary vestibular fibers enter- ing the MLF (ref. 6) was not verified in a more recent investigation (ref. 7). METHODS The experiments reported here were performed on decerebellate cats anesthetized with intra- venously administered a-chloralose (60-70 mg/kg), immobilized by gallamine triethiodide, and maintained on artificial respiration. The peripheral branches of the left vestibular nerve were exposed and equipped with stimulating electrodes; for recording purposes, the deep radial, selected intercostal nerves, and lumbo- sacral ventral roots were exposed unilaterally or bilaterally and a peripheral neurotomy per- formed. To isolate the medial longitudinal fasciculus, visible through the floor of the fourth ventricle on each side of the median sulcus, a transection of the brainstem, sparing only the MLF, was carried out at the level of the cerebello- pontine angle under a Zeiss binocular dissecting microscope. The section was followed by suc- tion with a fine pipet, inducing a discernible separation of the brainstem and with only the MLF spanning the gap. As a consequence, the preparations were essentially spinal. Histo- logical controls upon Weil-Weigert stained microscopic sections cut from blocks that in- cluded the full extent of the operative lesion were carried out after each experiment in order to verify the extent and completeness of the separation. The cervical spinal cord was exposed by lam- inectomy from the third to the seventh cervical vertebrae. In some of the experiments, the dorsal and ventral roots were left intact: in others, the dural cuffs were opened and the dorsal roots sectioned extradurally in order to obtain maximal distance between the distal portion of the roots and the cord. The distal ends were gently gripped between the two Ag-AgCl wires of the stimulating electrodes and elevated to a vertical position. Exposed neural structures were bathed in mineral oil and maintained at body temperature by radiant heat. Intracellular recordings from the motoneurons of the cervical cord were carried out with glass microelectrodes of approximately 0.5-micron tip diameter, filled with 3 M KC1, having a resistance of 5-20 megohms, and connected via a Bak unity- gain negative capacitance amplifier to a dc ampli- fying channel consisting of a Tektronix type D plug-in unit and a type 555 oscilloscope. FINDINGS Figure IA shows the control response to single- shock suprathreshold vestibular stimulation re- corded from the ipsilateral deep radial nerve (upper beam) and the ventral root L7. The il- lustration was obtained by superimposing 10 sweeps. Except for a small opening through the occipital bone over the region of the obex, the SECTION THROUGH THE MLF FIGURE 1. —Control responses to single-shock suprathreshold vestibular stimulation recorded from deep radial nenv (upper beam) and ventral root L7 before (A) and after (Hi selective elimination of the descending medial longitudinal fasciculi as shown in schematic drawing. Time scale in msec.

VESTIBULAR ACTIVITY IN THE MEDIAL LONGITUDINAL FASCICULUS 239 cats were intact; i.e., the three descending ves- tibulofugal tracts were unimpaired. Between recordings A and B, a section through the MLF had been carried out as shown in the schematic drawing of figure 1. Because of some difficulties confining the MLF, particularly in the ventral direction, the section across the midline was made 3 mm wide and 3 mm deep in order to disrupt the majority of descending fibers (ref. 8). In spite of this rather extensive section beyond the main confinement of the tract, it has not been possible to demonstrate any significant or per- sistent difference in the responses after this dis- connection, not even at the cervical level of motor output (fig. IB) and no matter whether threshold, suprathreshold, or supramaximal strength of stimulation was applied. To explore the importance of the MLF in transmitting vestibular impulses to different ~ ' .{' v ". , •- FIGURE 2. —Drawing of brainstem showing medial longitudi- nal fasciculi bridging gap (A). Histological controls upon hematoxylin-eosin (B) and Weil-Weigerl (C) stained micro- scopic cross sections of bridge containing main group of fibers constituting medial longitudinal fasciculi. Ampli- fication, 15 X. Segmental response to dorsal root C5 (DRC5) stimulation and deep radial nerve recording before (D) and after (E) creating bridge according to drawing. Segmental response preceded by vestibular activity exclu- sively funneled through .MLF (F). Time scale in msec. segmental spinal motoneuron populations, the "MLF animal" preparation was employed in the present study (fig. 2A). By eliminating all other extrapyramidal and pyramidal tracts by a high lesion through the central neuraxis, a straight relay between primary and secondary vestibular fibers, exclusively represented by the medial longitudinal fasciculus, is offered in sufficient anatomical isolation from adjacent vestibulofugal connections to provide a favorable situation in which the functional significance of the tract can be evaluated without undue interference (figs. 2B and C). The response, then conducted through the isolated portion of the descending MLF, had a latency of 7 msec, a duration of 8 to 10 msec, and an amplitude of about 100 to 150 /xV. The findings appear to contribute to an under- standing of the role played by the MLF, one of the phylogenetically oldest tracts, in the trans- mission of vestibular activity into the spinal cord. However, the extent to which it is permissible to interpret activities of the central nervous system in terms of properties of axons and synapses after making extensive sections through the structure may be open to discussion. In addition to a more or less transient depression of reflexes induced by transection of the brainstem, the vestibular facilitatory influx to the cord is reduced due to the elimination of the two other vestibulofugal path- ways (refs. 9 to 13), and thus the excitability level of the motor pools is lowered when the cells are impinged upon by the evoked activity funneled through the MLF exclusively (figs. 2D to F). The isolated tract which is simple in the sense that it is easy to describe in anatomical terms may, when activated, evoke only a non- specific response, whereas the tract as a member of the descending vestibulofugal system may participate in reflex activity of much greater complexity. When the peripheral branches of the vestibular nerve were stimulated, after the bridge containing the MLF had been made, re- sponses of gradually declining amplitude and increasing latency could be obtained as far down as the Th 5 and Th 6 intercostal nerves. The effect was strictly ipsilateral. No responses were recorded from ventral lumbosacral roots and no visible effects upon the local segmental reflexes were obtained.

240 THE ROLE OF THE VESTIBULAR ORGANS IN SPACE EXPLORATION In 42 instances intracellular recordings for several minutes permitted testing the effects of MLF activation on individual extensor and flexor motoneurons, as identified by antidromic stimula- tion of the deep radial and the musculocutaneous nerves. The cervical motoneurons showed both excitatory and inhibitory effects in response to single-shock vestibular stimulation. The ma- jority of the neurons, however, displayed an excitatory postsynaptic potential. No significant differences in discharge characteristics as defined in terms of latency, magnitude, and duration of evoked EPSP's and IPSP's were found during MLF activation. Figure 3 demonstrates the arrival of the vestibulospinal volley recorded from the surface of the cord (upper beam) at the same level as the site of the microelectrode penetration. The latencies of these EPSP's, as measured from the onset of the cord surface potential, varied between 1.1 and 1.6 msec. These values indicate that the activation of cervical motoneurons by impulses conducted in the MLF occurs via in- terneurons. In many instances it was possible to shorten the latency by increasing the strength of vestibular stimulation and, therefore, the values given are the shortest measured. In about one- third of the neurons, the EPSP's were followed by a small but distinct hyperpolarizing phase which in some instances lasted as long as 75 msec. In 10 of the impaled cells, the MLF volley evoked inhibitory postsynaptic potentials having latencies varying from 1.2 to 1.8 msec. The time course of these depolarizing and hyper- FIGURE 3. — Upper traces indicate arrival of MLF volley in spinal cord at the level of microelectrode penetration. Lower traces intracellular records of postsynaptic potentials in radial motoneurons. EPSP's evoked by I pulse/sec (A) and 50 pulses/sec (B) vestibular stimulation. IPSP's elicited by 1 pulse/sec (('.) and 50 pulses/sec (D) vestibular stimulation. Time scale in 5-msec intervals. polarizing effects was about 20 to 30 msec: i.e.. longer than the duration of EPSP's and IPSP's evoked by stimulation of peripheral muscle afferents. With vestibular stimuli of subthresh- old strength for spike discharge, the irregularly shaped EPSP and IPSP waves reached values of 1 to 2 mV, but with increase in the strength or frequency (50 to 200 pulses/sec) of stimulation, values of 4 to 6 mV were obtained. No pattern of reciprocity was encountered when recording from extensor or flexor motoneurons: the ap- pearance of depolarization or hyperpolarization occurred in an unpredictable manner. REFERENCES 1. GERNANDT, B. E.: Vestibular Influence Upon Spinal Reflex Activity. Myotatic, Kinesthetic and Vestibular Mechanisms. A. V. S. de Reuck and J. Knight, eds., Churchill, London. 1967, pp. 170-183. 2. BRODAL, A.: POMPEIANO. O.; AND WALBERG, F.: The Vestibular Nuclei and Their Connections, Anatomy and Functional Correlations. Oliver & Boyd, Edin- burgh and London, 1962. 3. GERNANDT, B. E.: AND GILMAN. S.: Generation of Labyrinthine Impulses, Descending Vestibular Path- ways, and Modulation of Vestibular Activity by Pro- prioceptive, Cerebellar. and Reticular Influences. Neural Mechanisms of the Auditory and Vestibular Systems, G. L. Rasmussen and W. F. Windle. eds., Charles C Thomas. 1960, pp. 324-348. 4. MASSOPUST, L. C.: Terminal Degeneration Study of the Spinal Component of the Medial Longitudinal Fascic- ulus. Anat. Record, vol. 127,1957, p. 330. 5. NYBERG-HANSEN. R.: Origin and Termination of Fibers From the Vestibular Nuclei Descending in the Medial Longitudinal Fasciculus. An Experimental Study With Silver Impregnation Methods in the Cat. J. Comp. Neurol., vol. 122,1964, pp. 355-367. 6. CAMIS, M.: The Physiology of the Vestibular Apparatus. Clarendon Press. Oxford, 1930. 7. CARPENTER. M. B.: Experimental Anatomical-Physio- logical Studies of the Vestibular Nerve and Cerebellar Connections. Neural Mechanisms of the Auditory and Vestibular Systems. G. L. Rasmussen and W. F. Windle, eds., Charles C Thomas, I960, pp. 297-323.

VESTIBULAR ACTIVITY IN THE MEDIAL LONGITUDINAL FASCICULUS 241 8. SZENTAGOTHAI, J.: Pathways and Synaptic Articulation Patterns Connecting Vestibular Receptors and Ocu- lomotor Nuclei. The Oculomotor System, M. B. Bender, ed., Harper, New York, 1964, pp. 205-223. 9. ANDERSSON, S.; AND GERNANDT, B. E.: Ventral Root Discharge in Response to Vestibular and Propriocep- tive Stimulation. J. Neurophysiol., vol. 19, 1954, pp. 524-543. 10. BACH, L. M. N.; AND MAGOUN, H. W.: The Vestibular Nuclei as an Excitatory Mechanism for the Cord. J. DISCUSSION Wilson: This presentation is very interesting and cer- tainly suggests that this medial pathway does not mediate any motor outflows through the ventral roots of the lower cervical and lumbosacral level. In talking about the cervi- cal level, I think it is quite important to emphasize at what particular cervical level you are working, because we found a significant difference between the upper segments dealing with the neck reflexes and the lower cervical segments deal- ing with the limb. We are going to apply some of these techniques of selective cutting, as you have, to see whether they influence the monosynaptic inhibitory potentials that we have observed. As far as the stimulation in the hrain- stem is concerned, I completely agree with you that it can be quite dangerous to stimulate in the brainstem and make conclusions from this. However, when small electrodes and threshold shocks are used, and when you track through a region and the threshold changes sharply as you go through it. I think then you are entitled to make some conclu- sions. Are you implying that this bundle of fibers, approximately 3 mm deep and 3 mm wide, that you are stimulating in your bridge experiment, contains only fibers originating in the vestibular nuclei? Gernandt: Yes; in the midline. Those fibers are the medial longitudinal fasciculi. Wilson: You do not think there are any reticulospinal fibers in that bridge at all? Gernandt: No; I do not think so. According to the anatomists, that is the classical description of the MLF, and I know that it does not include all the fibers, because they are scattered in the ventral-lateral direction, as I said. But these fibers, I think, are MLF fibers. Neurophysiol., vol. 10,1947, pp. 331-337. 11. GERNANDT, B. E.: AND THULIN, C.-A.: Vestibular Mech- anism of Facilitation and Inhibition of Cord Reflexes. Am. J. Physiol., vol. 172,1953, pp. 653-660. 12. KEMPINSKY, W. H.; AND WARD, A. A., JR.: Effect of Section of Vestibular Nerve Upon Cortically Induced Movement in Cat. J. Neurophysiol., vol. 13, 1950, pp. 295-304. 13. WARD, A. A., JR.: Decerebrate Rigidity. J. Neuro- physiol., vol. 10, 1947, pp. 89-103. Wilson: There must be many more fibers of vestibular origin in the MLF than we thought. Nyberg-Hansen: I am very glad to see that you can follow the medial vestibulospinal tract to midthoracic levels. That fits very well with my own anatomical findings. Concern- ing the bilaterality, I would stress that there are many more medial vestibulospinal fibers found ipsilaterally than contra- laterally. There are few contralateral fibers, but they can be demonstrated anatomically. Have you ever stimulated more rostrally in the MLF, above the level of the vestibular nuclei? I am particularly thinking about the interstitiospinal fibers. l.crnnmil: No; that is what I was trying to tell you. If you go down with the stimulating electrode into that region and apply electric stimulation, you will activate everything. So, no, we have not. We have only used peripheral nerves as inputs for activating the central nervous system. In going down and planting electrodes in the central nervous system for recording purposes you are safe, but not for stimulating purposes. That was my point. Nyberg-Ilansen: I understand perfectly well your point. I am only interested in the interstitiospinal fibers because they also course within the MLF in the brainstem, together with reticulospinal fibers and fibers from the medial ves- tibular nucleus. Furthermore, in the spinal cord, the inter- stitiospinal fibers can be followed to the lumbosacral enlarge- ment coursing in the dorsomedial part of the ventral funiculus. They are bilateral, but most numerous on the ipsilateral side. The interstitiospinal fibers terminate within the dorsal part of lamina VIII and adjacent parts of lamina VII, as do the medial vestibulospinal fibers. While the latter fibers are restricted to the upper half of the cord, the interstitiospinal fibers can be followed the whole cord throughout.

SESSION VIII Chairman: WILLIAM D. NEFF Indiana University

Next: EVOKED POTENTIAL AND MICROELECTRICAL ANALYSIS OF SENSORY ACTIVITY WITHIN THE CEREBELLUM »
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