Summary
Neurons histologically localized in the gigantocellular (Gc) and magnocellular (Mc) fields of the bulbar reticular formation were tested for antidromic invasion by stimulating the ventromedial (VM) and intralaminar (centralis lateralis, CL, and centrum medianum, CM) thalamic nuclei, midbrain reticular formation (MRF), and reticulospinal tract. An overwhelming majority (94%) of antidromically identified cells projected either to rostral structures (MRF, medial and intralaminar thalamic nuclei) or to the spinal cord, while only 6% had bifurcating axons.
Rostrally projecting bulbar reticular neurons were investigated during various wake-sleep behavioral states, (a) Phasic neurons were related to PGO waves, eye and head movements, and were localized in both Gc and Mc fields, (b) The majority of tonic neurons projected to MRF and VM and they were localized within Mc in a proportion of 85%. In order to test their possible role in activation of thalamocortical processes (as betrayed by EEG desynchronization), the activity of tonically discharging cells was separately evaluated in periods with and without phasic motor events. Half of the tonically discharging neurons had a high selectivity of discharge during paradoxical sleep without REM bursts (PS-); the ratio of their mean discharge rate during PS- to that in quiet wakefulness (QW) or slow-wave sleep (SWS) was 8 and 6, respectively. The other half of the tonic neurons equally increased firing rates from SWS to either QW or PS.
The firing rate of rostrally projecting bulbar reticular neurons with tonic discharge patterns was analyzed during transitions from SWS to PS. An increase in discharge rate was found about 30 to 60 s prior to the first sign of EEG desynchronization in PS, during fully synchronized sleep with PGO waves (S-PGO). Statistical testing showed that the increased firing rate was not associated to PGO waves, but was temporally related to the appearance of EEG desynchronization at PS onset. We conclude, on the basis of these and other recent data, that tonically discharging bulbar reticular neurons with identified projections to the midbrain and thalamic nuclei act synergically with rostrally projecting MRF neurons as sources of thalamocortical activation.
Similar content being viewed by others
References
Bowsher D, Mallart A, Petit D, Albe-Fessard D (1968) A bulbar relay to the centre median. J Neurophysiol 31: 288–300
Chase MH, Enomoto S, Murakami T, Nakamura Y, Taura M (1981) Intracellular potential of medullary reticular neurons during sleep and wakefulness. Exp Neurol 71: 226–233
Eccles JC, Nicoll RA, Schwarz DWF, Táboříková H, Willey TJ (1975a) Reticulospinal neurons with and without monosynaptic inputs from cerebellar nuclei. J Neurophysiol 38: 513–530
Eccles JC, Nicoll RA, Táboříková H, Willey TJ (1975b) Medial reticular neurons projecting rostrally. J Neurophysiol 38: 531–538
Edwards SB, DeOlmos JS (1976) Autoradiographic studies of the projections of the midbrain reticular formation: ascending projections of nucleus cuneiformis. J Comp Neurol 165: 417–432
Fuller JH (1975) Brain stem reticular units: some properties of the course and origin of the ascending trajectory. Brain Res 83: 349–367
Glenn LL, Hada J, Roy JP, Deschênes M, Steriade M (1982) Anterograde tracer and field potential analysis of the neocortical layer I projection from nucleus ventralis medialis of the thalamus in cat. Neuroscience 7: 1861–1877
Grantyn R, Margnelli M, Mancia M, Grantyn A (1973) Postsynaptic potentials in the mesencephalic and ponto-medullary reticular regions underlying descending limbic influences. Brain Res 56: 107–121
Graybiel AN (1977) Direct and indirect preoculomotor pathways of the brain-stem. An autoradiographic study of the pontine reticular formation in the cat. J Comp Neurol 175: 37–78
Gustaffson B, Lipski J (1980) Effect of membrane polarization and synaptic activity on the timing of antidromic invasion. Brain Res 181: 61–74
Henneman E, Somjen G, Carpenter DO (1965) Functional significance of cell size in spinal motoneurons. J Neurophysiol 28: 560–580
Herkenham M (1979) The afferent and efferent connections of the ventromedial thalamic nucleus in the rat. J Comp Neurol 183: 487–518
Hobson JA, McCarley RW, Pivik RT, Freedman R (1974) Selective firing by cat pontine brainstem neurons in desynchronized sleep. J Neurophysiol 37: 497–511
Inubushi S, Kobayashi T, Oshima T, Torii S (1978a) Intracellular recordings from the motor cortex during EEG arousal in unanesthetized brain preparations of the cat. Jpn J Physiol 28: 669–688
Inubushi S, Kobayashi T, Oshima T, Torii S (1978b) An intracellular analysis of EEG arousal in cat motor cortex. Jpn J Physiol 28: 689–708
Ito M, Udo M, Mano N (1970) Long inhibitory and excitatory pathways converging onto cat reticular and Deiters' neurons and their relevance to reticulofugal axons. J Neurophysiol 33: 210–226
Jones EG, Leavitt RY (1974) Retrograde axonal transport and the demonstration of non-specific projections to cerebral cortex and striatum from thalamic intralaminar nuclei in the rat, cat and monkey. J Comp Neurol 154: 349–378
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
Kitsikis A, Steriade M (1981) Immediate behavioral effects of kainic acid injections into the midbrain reticular core. Behav Brain Res 3: 361–380
Lipski J (1981) Antidromic activation of neurones as an analytical tool in the study of the central nervous system. J Neurosci Meth 4: 1–32
Macchi G, Bentivoglio M, D'Atena C, Rossini P, Tempesta E (1977) The cortical projection of the thalamic intralaminar nuclei restudied by means of the HRP retrograde axonal transport. Neurosci Lett 4: 121–126
Magni F, Willis WD (1963) Identification of reticular formation neurons by intracellular recording. Arch Ital Biol 101: 681–702
McCarley RW, Hobson JA (1975) Discharge patterns of cat pontine brain stem neurons during desynchronized sleep. J Neurophysiol 38: 751–766
Moruzzi G (1972) The sleep-waking cycle. Ergeb Physiol 64: 1–165
Nauta WJH, Kuypers HGJM (1958) Some ascending pathways in the brainstem reticular formation. In: Jasper HH, Proctor LD, Knighton RS, Noshay WC, Costello RT (eds) Reticular formation of the brain. Little Brown, Boston pp 3–30
Peterson BW (1979) Reticulo-motor pathways: their connections and possible role in motor behavior. In: Asanuma H, Wilson VJ (eds), Integration in the nervous system. Igaku-Shoin, Tokyo-New York, pp 185–200
Peterson BW, Maunz RA, Pitts NG, Mackel RG (1975) Patterns of projections and branching of reticulospinal neurons. Exp Brain Res 23: 333–351
Robertson RT, Feiner AR (1982) Diencephalic projections from the pontine reticular formation: autoradiographic studies in the cat. Brain Res 239: 3–16
Ropert N, Steriade M (1981) Input-output organization of the midbrain reticular core. J Neurophysiol 46: 17–31
Sakai K, Sastre JP, Kanamori N, Jouvet M (1981) State-specific neurons in the ponto-medullary reticular formation with special reference to the postural atonia during paradoxical sleep in the cat. In: Pompeiano O, Ajmone-Marsan C (eds), Brain mechanisms of perceptual awareness. Raven Press, New York, pp 405–429
Sasaki K, Matsuda Y, Oka H, Mizuno N (1975) Thalamo-cortical projections for recruiting responses and spindling-like responses in the parietal cortex. Exp Brain Res 22: 87–96
Sastre JP, Sakai K, Jouvet M (1981) Are the gigantocellular tegmental field neurons responsible for paradoxical sleep? Brain Res 229: 147–161
Scheibel ME, Scheibel AB (1958) Structural substrates for integrative patterns in the brain stem reticular core. In: Jasper HH, Proctor LD, Knighton RS, Noshay WC, Costello RT (eds) Reticular formation of the brain. Little Brown, Boston, pp 31–55
Siegel JM (1979) Behavioral functions of the reticular formation. Brain Res Rev 1: 69–105
Siegel JM, McGinty DG, Breedlove SM (1977) Sleep and waking activity of pontine gigantocellular field neurons. Exp Neurol 56: 553–573
Steriade M (1981) Mechanisms underlying cortical activation: neuronal organization and properties of the midbrain reticular core and intralaminar thalamic nuclei. In: Pompeiano O, Ajmone-Marsan C (eds) Brain mechanisms of perceptual awareness. Raven Press, New York, pp 327–377
Steriade M (1983) Cellular mechanisms of wakefulness and slowwave sleep. In: Mayes A (ed) Sleep in animals and human: an evolutionary view. Van Nostrand Reinhold, Workingham (England), pp 161–217
Steriade M (1984) The excitatory-inhibitory response sequence in thalamic and neocortical cells: state-related changes and regulatory systems. In: Edelman GM, Cowan WM, Gall WE (eds) Dynamic aspects of neocortical function. John Wiley & Sons, New York (in press)
Steriade M, Diallo A, Oakson G, White-Guay B (1977) Some synaptic inputs and telencephalic projections of lateralis posterior thalamic neurons. Brain Res 131: 39–53
Steriade M, Glenn LL (1982) Neocortical and caudate projections of intralaminar thalamic neurons and their synaptic excitation from midbrain reticular core. J Neurophysiol 48: 352–371
Steriade M, Oakson G, Ropert N (1982) Firing rates and patterns of midbrain reticular neurons during steady and transitional states of the sleep-waking cycle. Exp Brain Res 46: 37–51
Vertes RP (1979) Brain stem gigantocellular neurons. Patterns of activity during behavior and sleep in the freely moving rat. J Neurophysiol 42: 214–228
Author information
Authors and Affiliations
Additional information
Supported by grant MT-3689 from Medical Research Council of Canada
Supported by INSERM (U 52), CNRS (LA 162) and DRET (grant 81-205)
Rights and permissions
About this article
Cite this article
Steriade, M., Sakai, K. & Jouvet, M. Bulbo-thalamic neurons related to thalamocortical activation processes during paradoxical sleep. Exp Brain Res 54, 463–475 (1984). https://doi.org/10.1007/BF00235472
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00235472