Spontaneous synaptic activities in rat nucleus tractus solitarius neurons in vitro: evidence for re-excitatory processing

The pattern of synaptic interactions between neurons of the nucleus tractus solitarius (NTS) has been analyzed using whole cell recording in rat brainstem slices. Following tractus solitarius (TS) stimulation 15/55 neurons presented a prolonged (up to 300 ms) increased excitability (PIE neurons) and 40/55 neurons presented a prolonged (up to 200 ms) reduced excitability (PRE neurons). In the absence of afferent sensory input all neurons showed spontaneous synaptic activity. Ongoing synaptic activity in PIE cells was glutamatergic and characterized by the absence of detectable inhibitory potentials while in PRE cells it was 90% GABAergic and 10% glutamatergic. Glutamatergic synaptic currents in PIE cells and GABAergic synaptic currents in PRE were studied using probability density and intensity functions. Distribution of time intervals between synaptic events indicated the latter were generated, in both PIE and PRE cells, by two simultaneous processes: (1) a close to Poisson process generating independent events; and (2) a subsidiary re-excitatory process generating synaptic events separated by intervals shorter than 20 ms. Blockade of glutamatergic transmission by 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX; 10 microM) or blockade of action potentials by tetrodotoxin (TTX; 1 microM) suppressed the subsidiary process. In conclusion, we propose that PIE cells (1) form a re-excitatory network contributing to generation of excitatory activity in the NTS and (2) are located presynaptically with respect to PRE cells.

[1]  K. Anders,et al.  Inhibition of caudal medullary expiratory neurones by retrofacial inspiratory neurones in the cat. , 1991, The Journal of physiology.

[2]  B G Lindsey,et al.  Functional associations among simultaneously monitored lateral medullary respiratory neurons in the cat. I. Evidence for excitatory and inhibitory actions of inspiratory neurons. , 1987, Journal of neurophysiology.

[3]  Burns Bd,et al.  Repetitive firing of respiratory neurones during their burst activity. , 1960 .

[4]  A. Loewy,et al.  Projections of the aortic nerve to the nucleus tractus solitarius in the rabbit , 1980, Brain Research.

[5]  J. Feldman,et al.  Discharge properties of dorsal medullary inspiratory neurons: relation to pulmonary afferent and phrenic efferent discharge. , 1984, Journal of neurophysiology.

[6]  J. Velluti,et al.  Responses to repetitive afferent activity of rat solitary complex neurons isolated in brainstem slices , 1992, Neuroscience Letters.

[7]  CCK modulates inhibitory synaptic transmission in the solitary complex through CCKB sites. , 1992, Neuroreport.

[8]  R. McCarley,et al.  Alterations in membrane potential and excitability of cat medial pontine reticular formation neurons during changes in naturally occurring sleep-wake states , 1984, Brain Research.

[9]  P. Kirkwood On the use and interpretation of cross-correlation measurements in the mammalian central nervous system , 1979, Journal of Neuroscience Methods.

[10]  P. Branchereau,et al.  Rhythmic activities in the rat solitary complex in vitro , 1992, Neuroscience Letters.

[11]  H. Kita,et al.  The stochastic properties of spontaneous quantal release of transmitter at the frog neuromuscular junction , 1974, The Journal of physiology.

[12]  N. Ropert,et al.  Characteristics of miniature inhibitory postsynaptic currents in CA1 pyramidal neurones of rat hippocampus. , 1990, The Journal of physiology.

[13]  D. Cox,et al.  The statistical analysis of series of events , 1966 .

[14]  J. Champagnat,et al.  Rhythmic neuronal activities in the nucleus of the tractus solitarius isolated in vitro , 1983, Brain Research.

[15]  J. Champagnat,et al.  Effects of opiates and methionine-enkephalin on pontine and bulbar respiratory neurones of the cat , 1978, Brain Research.

[16]  James Duffin,et al.  The neuronal determinants of respiratory rhythm , 1986, Progress in Neurobiology.

[17]  K. Spyer,et al.  The actions of baclofen on neurones and synaptic transmission in the nucleus tractus solitarii of the rat in vitro. , 1992, The Journal of physiology.

[18]  J. Champagnat,et al.  Differentiation of two respiratory areas in the cat medulla using kainic acid. , 1984, Respiration physiology.

[19]  K. Ezure,et al.  Synaptic connections between medullary respiratory neurons and considerations on the genesis of respiratory rhythm , 1990, Progress in Neurobiology.

[20]  S Grillner,et al.  Central pattern generators for locomotion, with special reference to vertebrates. , 1985, Annual review of neuroscience.

[21]  M. Kalia,et al.  Brainstem projections of sensory and motor components of the vagus nerve in the rat , 1982, The Journal of comparative neurology.

[22]  H. Kirchheim Systemic arterial baroreceptor reflexes. , 1976, Physiological reviews.

[23]  K. M. Spyer Central nervous integration of cardiovascular control. , 1982, The Journal of experimental biology.

[24]  A. Bianchi,et al.  A cross-correlation study of interactions among respiratory neurons of dorsal, ventral and retrofacial groups in cat medulla , 1984, Brain Research.

[25]  John Orem,et al.  Characteristics of midbrain respiratory neurons in sleep and wakefulness in the cat , 1982, Brain Research.

[26]  C N Christakos,et al.  Fast rhythms in phrenic motoneuron and nerve discharges. , 1991, Journal of neurophysiology.

[27]  C. D. Stern,et al.  Handbook of Chemical Neuroanatomy Methods in Chemical Neuroanatomy. Edited by A. Bjorklund and T. Hokfelt. Elsevier, Amsterdam, 1983. Cloth bound, 548 pp. UK £140. (Volume 1 in the series). , 1986, Neurochemistry International.

[28]  K. Grant,et al.  Organization of synaptic transmission in the mammalian solitary complex, studied in vitro. , 1986, The Journal of physiology.

[29]  T. Dick,et al.  Electrophysiological determination of the axonal projections of single dorsal respiratory group neurons to the cervical spinal cord of cat , 1988, Brain Research.

[30]  M. Chase,et al.  Synaptic mechanisms and circuitry involved in motoneuron control during sleep. , 1983, International review of neurobiology.