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Direct inhibitory projection of pause neurons to nystagmus-related pontomedullary reticular burst neurons in the cat

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Summary

Brainstem pause neurons (PNs) exhibit a tonic discharge during the slow phase of horizontal vestibular nystagmus and pause prior to and during the quick phase in both directions. One type of pontomedullary burst neurons, burst inhibitory neurons (BINs), show a high frequency burst of spikes before and during the quick phase to the ipsilateral side and this burst directly inhibits contralateral abducens motoneurons, terminating the slow phase firing of these motoneurons. The present study focused on synaptic relations between PNs and BINs.

The following data supported the conclusion that PNs probably make direct inhibitory connections with BINs and produce IPSPs in BINs during the slow phase of horizontal vestibular nystagmus: (a) there were positive field potentials in the BIN area during the slow phase; (b) PNs were antidromically activated from BIN areas bilaterally; (c) systematic microstimulation of the BIN area revealed a pattern consistent with axonal branching in the BIN area; (d) repetitive microstimulation of the PN area induced a positive shift in the field potential in the BIN area and suppressed both the characteristic bursts of BINs and nystagmic activity of the contralateral abducens nerve; (e) microstimulation of the PN area during intracellular recording of BINs induced monosynaptic latency hyperpolarizing potentials which could be reversed by Cl injection; (f) during intracellular recording from BINs during vestibular nystagmus in either direction, the membrane potential during the slow phases had a tonic hyperpolarization which was shown to be due to IPSPs by means of Cl injection.

This study suggests that burst activity of BINs during the quick phase is caused by abrupt release from PN IPSPs (disinhibition), besides some excitatory inputs from other sources.

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References

  • Anderson P, Eccles J (1962) Inhibitory phasing of neuronal discharge. Nature 196: 645–647

    Google Scholar 

  • Asanuma H, Sakata H (1967) Functional organization of a cortical efferent system examined with focal depth stimulation in cats. J Neurophysiol 30: 35–54

    Google Scholar 

  • Bagshaw EV, Evans MH (1976) Measurement of current spread from microelectrodes when stimulating within the nervous system. Exp Brain Res 25: 391–400

    Google Scholar 

  • Cohen B, Henn V (1972) Unit activity in the pontine reticular formation associated with eye movements. Brain Res 46: 403–410

    Google Scholar 

  • Curthoys IS, Nakao S, Markham CH (in prep) Cat medial pontine reticular neurons related to vestibular nystagmus: Firing pattern, location and projection to abducens nucleus

  • Duensing F, Schaefer KP (1957) Die Neuronenaktivität in der Formatio reticularis des Rhombencephalons beim vestibulären Nystagmus. Arch Psychiat Nervenkr 196: 265–290

    Google Scholar 

  • Eccles JC (1964) The physiology of synapses. Springer, Berlin Göttingen Heidelberg New York

    Google Scholar 

  • Evinger C, Kaneko CRS, Johanson GW, Fuchs AF (1977) Omnipauser cells in the cat. In: Baker R, Berthoz A (eds) Control of gaze by brain stem neurons. Developments in neuroscience, vol 1. Elsevier, New York, pp 337–340

    Google Scholar 

  • Hikosaka O, Igusa Y, Nakao S, Shimazu H (1978) Direct inhibitory synaptic linkage of pontomedullary reticular burst neurons with abducens motoneurons in the cat. Exp Brain Res 33: 337–352

    Google Scholar 

  • Hikosaka O, Kawakami T (1977) Inhibitory reticular neurons related to the quick phase of vestibular nystagmus — their location and projection. Exp Brain Res 27: 377–396

    Google Scholar 

  • Hilgard ER, MacDonald H, Marshall GD, Morgan AH (1974) Anticipation of pain and of pain control under hypnosis: Heart rate and blood pressure responses in the cold pressor test. J Abnorm Psychol 38: 561–568

    Google Scholar 

  • Hilgard ER, Morgan AH, Lange AF, Lenox JR, MacDonald H, Marshall GD, Sachs LB (1974) Heart rate changes in pain and hypnosis. Psychophysiol 11: 692–702

    Google Scholar 

  • Kandel ER, Frazier WT, Wachtel H (1969) Organization of inhibition in abdominal ganglion of aplysia. I. Role of inhibition and disinhibition in transforming neural activity. J Neurophysiol 32: 496–502

    Google Scholar 

  • Kandel ER, Spencer WA (1961) Electrophysiology of hippocampal neurons. II. Afterpotential and repetitive firing. J Neurophysiol 24: 243–259

    Google Scholar 

  • Kaneko CRS, Fuchs AF (1978) Connections of feline ominipause neurons. Neurosci Abstr 4: 164

    Google Scholar 

  • Keller EL (1974) Participation of medial pontine reticular formation in eye movement generation in the monkey. J Neurophysiol 37: 316–332

    CAS  PubMed  Google Scholar 

  • Keller EL (1977) Control of saccadic eye movements by midline brain stem neurons. In: Baker R, Berthoz A (eds) Control of gaze by brain stem neurons. Developments in neuroscience, vol 1. Elsevier, New York, pp 327–335

    Google Scholar 

  • King WM, Precht W, Dieringer N (1978) Connections of behaviorally identified cat omnipauser neurons. Exp Brain Res 32: 435–438

    Google Scholar 

  • Kryzhanovsky GN (1976) Experimental central pain and itch syndromes: modeling and general theory. In: Bonica JJ, Albe-Fessard D (eds) Advances in pain research and therapy, vol 1. Raven Press, New York, pp 225–230

    Google Scholar 

  • Lenox JR (1970) Effect of hypnotic analgesia on verbal report and cardiovascular responses to ischémic pain. J Abnorm Psychol 75: 199–206

    Google Scholar 

  • Luschei ES, Fuchs AF (1972) Activity of brain stem neurons during eye movements of alert monkeys. J Neurophysiol 35: 445–461

    Google Scholar 

  • Maeda M, Shimazu H, Shinoda Y (1972) Nature of synaptic events in cat abducens motoneurons at slow and quick phase of vestibular nystagmus. J Neurophysiol 35: 279–296

    Google Scholar 

  • Nakao S, Curthoys IS, Markham CH (1980a) Eye movement related neurons in the cat pontine reticular formation: projection to the flocculus. Brain Res 180: 291–299

    Google Scholar 

  • Nakao S, Markham CH, Curthoys IS (1980b) Modification of single neural elements in vestibular nystagmus by anesthesia. Acta Otolaryngol 89: 121–134

    Google Scholar 

  • Raybourn MS, Keller EL (1977) Collicular organization in primate oculomotor system. J Neurophysiol 40: 861–878

    Google Scholar 

  • Robinson DA (1975) Oculomotor control signals. In: Lennerstrand G, Bach-y-Rita P (eds) Basic mechanisms of ocular motility and their clinical implications. Pergamon Press, New York, pp 337–374

    Google Scholar 

  • Römer D (1968) A sensitive method of measuring analgesic effects in the monkey. In: Soulairac A, Cahn J, Carpentier J (eds) Pain. Academic Press, New York, pp 165–170

    Google Scholar 

  • Taber E, Brodal A, Walberg F (1960) The raphé nuclei of the brain stem in the cat. I. Normal topography and cytoarchitecture and general discussion. J Comp Neurol 114: 161–187

    Google Scholar 

  • Thomas RC, Wilson VJ (1965) Precise localization of Renshaw cells with a new marking technique. Nature 206: 211–213

    Google Scholar 

  • Wilson VJ, Burgess PR (1962) Disinhibition in the cat spinal cord. J Neurophysiol 25: 392–404

    Google Scholar 

  • Wolf S, Hardy JD (1941) Studies on pain. Observations on pain due to local cooling and on factors involved in the “cold pressor” effect. J Clin Invest 20: 521–533

    Google Scholar 

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Considerable personal experience of one of us (Charles H. Markham) during human neurosurgical procedures under local anesthesia only, plus consultation with neurosurgeons and ophthalmologists on operations done under local anesthesia, give us further confidence the present experiments were conducted in a humane and pain-free state

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Nakao, S., Curthoys, I.S. & Markham, C.H. Direct inhibitory projection of pause neurons to nystagmus-related pontomedullary reticular burst neurons in the cat. Exp Brain Res 40, 283–293 (1980). https://doi.org/10.1007/BF00237793

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  • DOI: https://doi.org/10.1007/BF00237793

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