Skip to main content
SpringerLink
Log in

Synaptic mechanisms acting on lumbar motoneurons during postural augmentation induced by serotonin injection into the rostral pontine reticular formation in decerebrate cats

  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

Intrapontine microinjections of serotonin in acutely decerebrated cats resulted in the bilateral augmentation of the postural muscle tone of the hindlimbs. Optimal injection sites were located in the dorsomedial part of the rostral pontine reticular formation corresponding to the nucleus reticularis ponds oralis (NRPo). In this study, attempts were made to elucidate the cellular basis for the serotoninergically induced augmentation of postural muscle tone by recording the electromyographic (EMG) activity of hindlimb extensor muscles, the monosynaptic reflex responses evoked by electrical stimulation of group Ia muscle afferent fibres and the membrane potentials of hindlimb alpha-motoneurons (MNs). Serotonin injections resulted not only in the augmentation of the EMG activity of gastrocnemius soleus muscles, but also in the restoration of EMG suppression, which was induced by previous injection of carbachol into the NRPo. Extensor and flexor monosynaptic reflex responses were facilitated by serotonin injections into the NRPo. Such reflex facilitation was not induced by serotonin injections into the mesencephalic or the medullary reticular formation. Intrapontine serotonin injections resulted in membrane depolarization of extensor and flexor MNs with decreases in input resistance and rheobase. Spontaneous depolarizing synaptic potentials (EPSPs) increased in both frequency and amplitude. Peak voltage of Ia monosynaptic EPSPs also increased. Serotonin injections which followed carbachol injections resulted in membrane depolarization of MNs along with an increase in the frequency of spontaneous EPSPs and a decrease in carbachol-induced inhibitory postsynaptic potentials. Following pontine carbachol injections, antidromic and orthodromic responses in MNs were suppressed. Discharges of MNs evoked by intracellular current injections were also suppressed, but were restored following serotonin injections. These results indicate that postsynaptic excitation, presynaptic facilitation and disinhibition (withdrawal of postsynaptic inhibition) simultaneously act on the hindlimb MNs during serotonin-induced postural augmentation and restoration.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Amatruda T, Black D, McKenna T, McCarley RW, Hobson JA (1974) The effects of carbachol injections at two brain stem sites. Sleep Res 3: 38

    Google Scholar 

  • Berman AL (1968) The brain stem of the cat: a cytoarchitectonic atlas with stereotaxic coordinates. University of Wisconsin Press, Madison

    Google Scholar 

  • Brock LG, Coombs JS, Eccles JC (1953) Intracellular recording from antidromically activated motoneurons in the cat. J Physiol (Lond) 122: 429–461

    Google Scholar 

  • Chan SHH, Barnes CD (1972) A presynaptic mechanism evoked from brain stem reticular formation in the lumbar cord and its temporal significance. Brain Res 45: 101–114

    Article  CAS  PubMed  Google Scholar 

  • Chase MH, Morales FR (1983) Subthreshold excitatory activity and motoneuron discharge during REM periods of active sleep. Science 221: 1195–1198

    Google Scholar 

  • Chase MH, Morales FR, Boxer P, Fung SJ, Soja PJ (1986) Effect of stimulation of the nucleus reticularis gigantocellularis on the membrane potential of cat lumbar motoneurons during sleep and wakefulness. Brain Res 386: 237–244

    Google Scholar 

  • Crone C, Hultborn H, Kiehn O, Mazieres L, Wingstorm H (1988) Maintained changes in motoneuronal excitability by shortlasting synaptic inputs in the decerebrate cat. J Physiol (Lond) 404: 321–343

    Google Scholar 

  • Decima EE, Haslet WL (1964) Effects of oxotremorine on gamma fiber activity. Proc West Pharmacol Soc 7: 50–52

    Google Scholar 

  • Drew T, Rossignol S (1991) Functional organization within the medullary reticular formation of intact unanaesthetized cat. II. Electromyographic activity evoked by microstimulation. J Neurophysiol 64: 782–895

    Google Scholar 

  • Fetz EE, Jankowska E, Johannisson T. Lipski J (1979) Autogenetic inhibition of motoneurons by impulses in group I muscle spindle afferents. J Physiol (Lond) 293: 173–195

    Google Scholar 

  • Fung SJ, Barnes CD (1987) Membrane excitability changes in hindlimb motoneurons induced by stimulation of the locus coeruleus in cats. Brain Res 402: 230–242

    Google Scholar 

  • Glenn LL, Dement WC (1981) Membrane potential, synaptic activity and excitability of hindlimb motoneurons during wakefulness and sleep. J Neurophysiol 46: 839–854

    Google Scholar 

  • Granit R (1970) The basis of motor control. Academic Press, New York

    Google Scholar 

  • Granit R, Job C, Kaada BR (1952) Activation of muscle spindles in pinna reflex. Act Physiol Scand 27: 161–168

    Google Scholar 

  • Graybiel (1977) Direct and indirect preoculomotor pathways of the brainstem: an autoradiographic study of the pontine reticular formation in the cat. J Comp Neurol 175: 37–78

    Google Scholar 

  • Greene RW, Carpenter DO (1985) Actions of neurotransmitters on pontine medial reticular formation neurons of the cat. J Neurophysiol 54: 520–531

    Google Scholar 

  • Greene RW, Gerber U, McCarley RW (1989a) Cholinergic activation of medial pontine reticular formation neurons in vitro. Brain Res. 476: 154–159

    Google Scholar 

  • Greene RW, Gerber U, Hass HL, McCarley RW (1989b) Noradrenergic actions of neurons of the medial pontine reticular formation in vitro. Sleep Res 18: 11

    Google Scholar 

  • Hobson JA, Goldberg M, Vivaldi E, Riew D (1983) Enhancement of desynchronized sleep signs after pontine microinjection of the muscarinic agonist bethanechol. Brain Res 275: 127–136

    Google Scholar 

  • Hobson JA, Lydie R, Baghdoyan HA (1986) Evolving concepts of sleep cycle generation: from brain centers to neuronal populations. Behav Brain Sci 9: 371–448

    Google Scholar 

  • Hosli L, Tebecis AK, Schonwetter HP (1971) A comparison of the effects of monoamines on neurons of the bulbar reticular formation. Brain Res 25: 357–370

    Google Scholar 

  • Jankowska E, McCrea D, Mackel R (1981) Pattern of ‘non-reciprocal’ inhibition of motoneurons by impulses in group Ia muscle spindle afferents in the cat. J Physiol (Lond) 316: 393–409

    Google Scholar 

  • Kanamori N, Sakai K, Jouvet M (1980) Neuronal activity specific to paradoxical sleep in the ventromedial medullary reticular formation of unrestrained cats. Brain Res 189: 251–255

    Google Scholar 

  • Katayama Y, Dewitt DS, Becker DP, Hayers RL (1984) Behavioral evidence from a cholinoceptive pontine inhibitory area: descending control of spinal motor output and sensory input. Brain Res 296: 241–262

    Google Scholar 

  • Kobayashi Y, Matsuyama K, Mori S (1991) Origins of serotonergic and cholinergic neurons projecting to the nucleus reticularis pontis oralis in the cats. Neurosci Res [Suppl] 16: S105

    Google Scholar 

  • Lai YY, Siegel J (1988) Medullary regions mediating atonia. J Neurosci 8: 4790–4796

    Google Scholar 

  • Leichnetz GR, Carlton SM, Katayama Y, Gonzalo-Ruiz A, Holstage G, DeSalles AAF, Hayes RL (1989) Afferent and efferent connections of the cholinoceptive medial pontine reticular formation (region of the ventral tegmental nucleus) in the cat. Brain Res Bull 22: 665–688

    Google Scholar 

  • Lipski j (1981) Antidromic activation of neurons as an analytical tool in the study of the central nervous system. J Neurosci Methods 4: 1–32

    Google Scholar 

  • Matsuyama K, Ohta Y, Mori S (1988) Ascending and descending projections of the nucleus reticularis gigantocellularis in the cat demonstrated by anterograde neural tracer, Phaseolus vulgaris leucoagglutinin (PHA-L). Brain Res 460: 124–141

    Google Scholar 

  • Matsuyama K, Kobayashi Y, Mori S (1991) Anatomical analyses of brainstem and spinal cord projections of the nucleus reticularis pontis oralis in the cat. Neurosci Res [Suppl] 16: 105

    Google Scholar 

  • Morales FR, Engelhardt JK, Soja PJ, Pereda AE, Chase MH (1987) Motoneuron properties during motor inhibition produced by microinjection of carbachol into the pontine reticular formation of the decerebrate cat. J Neurophysiol 57: 1118–1129

    Google Scholar 

  • Mori S (1987) Integration of posture and locomotion in acute decerebrate cats and in freely moving cats. Prog Neurobiol 28: 161–195

    Google Scholar 

  • Mori S, Kawahara K, Sakamoto T, Aoki M, Tomiyama T (1982) Setting and resetting of level of postural muscle tone in decerebrate cat by stimulation of brain stem. J Neurophysiol 48: 737–748

    Google Scholar 

  • Mori S, Sakamoto T, Ohta Y, Takakusaki K, Matsuyama K (1989) Site-specific postural and locomotor changes evoked in awake, freely moving intact cats by stimulating the brainstem. Brain Res 50: 66–74

    Google Scholar 

  • Mori S, Shimoda N, Tanaka H, Oka T, Takakusaki K (1990) Contribution of pontine reticular formation to the full execution of controlled locomotion in decerebrate cats. Somatosens Motor Res 7: 246–247

    Google Scholar 

  • Nakamura Y, Goldberg LJ, Chandler SH, Chase MH (1978) Intracellular analysis of trigeminal motoneuron activity during sleep in the cat. Science 199: 204–207

    Google Scholar 

  • Ohta Y, Kimura H, Mori S (1988) Neuronal structures of the brainstem participating in postural suppression in cats. Neurosci Res 5: 181–202

    Google Scholar 

  • Peterson BW, Maunz RA, Pitts NG, Mackel RG (1975) Patterns of projection and branching of reticulospinal neurons. Exp Brain Res 23: 333–351

    Google Scholar 

  • Peterson BW, Pitts NG, Fukushima K (1979) Reticulospinal connections with limb and axial motoneurons. Exp Brain Res 36: 1–20

    Google Scholar 

  • Pompeiano O, Horn E, d'Ascanio P (1991) Locus coeruleus and dorsal pontine reticular influences on the gain of vestibulospinal reflexes. Prog Brain Res 88: 435–462

    Google Scholar 

  • Rudomin P, Nunez R, Madrid J, Burke RE (1974) Primary afferent hyperpolarization and presynaptic facilitation of Ia afferent terminals induced by large cutaneous fibers. J Neurophysiol 37: 413–429

    CAS  PubMed  Google Scholar 

  • Rudomin P, Jimenez M, Solodkin M, Duenas S (1983) Sites of action of segmental and descending control of transmission of pathways mediating PAD of Iaand Ib-afferent fibers in cat spinal cord. J Neurophysiol 50: 743–769

    Google Scholar 

  • Sakai K (1980) Some anatomical and physiological properties of pontomesencephalic tegmental neurons with special reference to the PGO waves and postural atonia during paradoxical sleep in the cat. In: Hobson JA, Brazer MAB (eds) The reticular formation revisited. Raven Press, New York, pp 427–447

    Google Scholar 

  • Sakai K, Sastre JP, Salvert D, Touret M, Tohyama M, Jouvet M (1979) Tegmentoreticular projections with special reference to the muscular atonia during paradoxical sleep in the cat: an HRP study. Brain Res 176: 233–254

    Google Scholar 

  • Sakamoto T, Atsuta Y, Mori S (1986) Long-lasting excitability changes of soleus alpha-motoneurons induced by midpontine stimulation in decerebrate. standing cat. J Neurophysiol 55: 449–468

    Google Scholar 

  • Semba K (1991) Transmitter-specific afferent connections of the “carbachol-sensitive” region of the pontine reticular formation in the rat. Third IBRO World Congress of Neuroscience, Abstr 256, Pergamon Press, New York

    Google Scholar 

  • Sherrington CS (1906) The integrative action of the nervous system. Yale University Press, New Haven

    Google Scholar 

  • Sherrington CS (1910) Flexion-reflex of the limb, crossed extension reflex and reflex stepping and standing. J Physiol (Lond) 40: 28–121

    Google Scholar 

  • Siegel JM, McGinty DJ (1977) Pontine reticular formation neurons: relationship of discharge to motor activity. Science 196: 680–687.

    Google Scholar 

  • Snider RS, Niemer WT (1961) A stereotaxic atlas of the cat brain. University of Chicago Press, Chicago

    Google Scholar 

  • Stevens DR, Green RW, McCarley RW (1989) Excitatory and inhibitory actions of serotonin on medial pontine reticular formation neurons mediated by opposing actions on potassium conductance(s). Sleep Res 18: 23

    Google Scholar 

  • Takakusaki K (1991) Cholinergic and serotonergic control of reticulospinal actions of motor activity in decerebrate cats. Jpn J Physiol [Suppl] 41: S9

    Google Scholar 

  • Takakusaki K, Ohta Y, Mori S (1987) Neuronal mechanisms involved in postural suppression in decerebrate, reflex standing cats. Neurosci Res [Suppl] 5: S132

    Google Scholar 

  • Takakusaki K, Sakamoto T, Mori S (1988) Chemical modulation of medullary output neurons which control excitability of hindlimb alpha-motoneurons in cats. Soc Neurosci Abstr 14: 180

    Google Scholar 

  • Takakusaki K, Ohta Y, Mori S (1989a) Single medullary reticulospinal neurons exert postsynaptic inhibitory effects via inhibitory interneurons upon alpha-motoneurons innervating cat hindlimb muscles. Exp Brain Res 74: 11–23

    Google Scholar 

  • Takakusaki K, Shimoda N, Mori S (1989b) Excitability modulation of hindlimb alpha-motoneurons induced by microinjection of carbachol and monoaminergic agents into the rostral pontine reticular formation of acute decerebrate cats. Neurosci Res [Suppl] 9: S88

    Google Scholar 

  • Takakusaki K, Shimoda N, Mori S (1990) Spinal interneurons mediating the inhibition from the ‘Medullary Inhibitory Region” to hindlimb alpha-motoneurons in decerebrate cats. Somatosens Motor Res 7: 258

    Google Scholar 

  • Takakusaki K, Kohyama J, Mori S (1991) Synaptic mechanisms of hindlimb motoneurons involved in postural augmentation induced by serotonin (5-HT) injection into the rostral pons in decerebrate cats. Neurosci Res [Suppl] 14: S 67

    Google Scholar 

  • Takakusaki K, Matsuyama K, Mori S (in press) Spinal interneurons inducing non-reciprocal inhibition of hindlimb alpha-motoneurons in the cat. Jpn J Physiol [Suppl]

  • Vanni-Mercier G, Sakai K, Lin JS, Jouvet M (1989) Mapping of cholinoceptive brainstem structures responsible for the generation of paradoxical sleep in the cat. Arch Ital Biol 127: 133–164

    CAS  PubMed  Google Scholar 

  • Yamamoto K, Mamelak AN, Quattrochi JJ, Hobson JA (1990) A cholinoceptive desynchronized sleep induction zone in the anterodorsal pontine tegmentum: locus of the sensitive region. Neuroscience 39: 279–293

    Article  CAS  PubMed  Google Scholar 

  • Yamuy J, Mancillas JR, Tran RT, Morales FR, Chase MH (1991a) C-fos-like expression in the lumbar spinal cord of the cat during carbachol-induced atonia. Sleep Res 20A Abstr p 76

    Google Scholar 

  • Yamuy J, Mancillas JR, Morales FR, Chase MH (1991b) C-fos-like expression in the brainstem of the cat during carbachol-inducedn atonia. Soc Neurosci Abstr 17: 468

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Physiology II, Asahikawa Medical College, Nishikagura 4–5, 3–11, 078, Asahikawa, Japan

    Kaoru Takakusaki, Jun Kohyama, Kiyoji Matsuyama & Shigemi Mori

Authors
  1. Kaoru Takakusaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jun Kohyama
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kiyoji Matsuyama
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shigemi Mori
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Takakusaki, K., Kohyama, J., Matsuyama, K. et al. Synaptic mechanisms acting on lumbar motoneurons during postural augmentation induced by serotonin injection into the rostral pontine reticular formation in decerebrate cats. Exp Brain Res 93, 471–482 (1993). https://doi.org/10.1007/BF00229362

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00229362

Key words

Search

Navigation