Repetitive firing properties of developing rat brainstem motoneurones.

1. The repetitive firing properties of neonatal and adult rat hypoglossal motoneurones (HMs) were investigated in a brainstem slice preparation. Neonatal HMs could be classified into two main groups: (1) neurones with a decrementing or adapting firing pattern (type D); exhibiting an early and a late phase; and (2) neurones with an incrementing or accelerating firing pattern (type I). 2. The pattern of repetitive firing changed markedly during development. While most HMs recorded from young rats (< postnatal day (P) 4) were type D, the majority of HMs recorded during the second postnatal week were type I. In adults (> P21), nearly all HMs had a decrementing firing pattern, characterized by a brief period of adaptation and high steady‐state firing rates. 3. The calcium‐dependent after‐hyperpolarization (AHP) was shortest in type I neonatal HMs, and decreased in amplitude during trains of action potentials (APs). In type D neurones, these same trains caused a slight enhancement of AHP amplitude. In adult HMs, with a decrementing firing pattern, trains of APs also caused summation of the AHP. 4. Type D neonatal HMs showed a progressive prolongation of the AP during repetitive firing. In contrast, type I neonatal HMs had almost no change in AP duration. In adult HMs the AP was short and experienced only a modest increase in duration during fast repetitive firing. 5. The function relating steady‐state firing frequency to injected current (f‐I curve) was linear. The mean steady‐state f‐I slope was significantly higher in neonates than in adults (approximately 30 vs. approximately 20 Hz nA‐1), and was weakly correlated with input resistance. The f‐I slope was negatively correlated with AHP duration in neonatal HMs only. In addition, for a given AHP duration the slope was higher in neonatal HMs. 6. Two threshold behaviours were observed among neonatal HMs: (a) a progressive rhythmic firing threshold, and (b) a sudden transition from subthreshold to regular repetitive firing. Current threshold for repetitive firing was strongly correlated with cell input conductance. Type I neonatal HMs had higher minimal steady firing rates (fmin) than type D HMs. In neonates, fmin was strongly correlated with AHP duration. Adult HMs showed a weaker correlation between these two parameters, and fmin was higher than predicted by AHP duration. 7. In summary, HMs responded to depolarizing current pulses with different firing patterns during postnatal development.(ABSTRACT TRUNCATED AT 400 WORDS)

[1]  P. A. Getting,et al.  Biophysical properties of hypoglossal neurons in vitro: intracellular studies in adult and neonatal rats. , 1990, Journal of applied physiology.

[2]  Ole Kiehn,et al.  Neuromodulation of vertebrate motor neuron membrane properties , 1992, Current Opinion in Neurobiology.

[3]  P. Zangger,et al.  Effect of repetitive activation on the afterhyperpolarization in dorsal spinocerebellar tract neurones. , 1978, The Journal of physiology.

[4]  P. Schwindt,et al.  Post‐inhibitory excitation and inhibition in layer V pyramidal neurones from cat sensorimotor cortex. , 1991, The Journal of physiology.

[5]  G. Vrbóva,et al.  Matching of muscle properties and motoneurone firing patterns during early stages of development. , 1985, The Journal of experimental biology.

[6]  D. Kernell,et al.  Organization and properties of spinal motoneurones and motor units. , 1986, Progress in brain research.

[7]  P. Schwindt,et al.  Equivalence of synaptic and injected current in determining the membrane potential trajectory during motoneuron rhythmic firing. , 1973, Brain research.

[8]  B. Gustafsson,et al.  Afterhyperpolarization conductance time course in lumbar motoneurones of the cat. , 1974, Acta physiologica Scandinavica.

[9]  D. Kernell.  High-Frequency Repetitive Firing of Cat Lumbosacral Motoneurones Stimulated by Long-Lasting Injected Currents , 1965 .

[10]  Repetitive firing properties of phrenic motoneurons in the cat. , 1988, Journal of neurophysiology.

[11]  B. Gustafsson.  Afterhyperpolarization and the control of repetitive firing in spinal neurones of the cat. , 1974, Acta physiologica Scandinavica. Supplementum.

[12]  G. Vrbóva,et al.  Activity-dependent interactions between motoneurones and muscles: Their role in the development of the motor unit , 1993, Progress in Neurobiology.

[13]  D. Kernell,et al.  Input Resistance, Electrical Excitability, and Size of Ventral Horn Cells in Cat Spinal Cord , 1966, Science.

[14]  G. Somjen,et al.  FUNCTIONAL SIGNIFICANCE OF CELL SIZE IN SPINAL MOTONEURONS. , 1965, Journal of neurophysiology.

[15]  J. Rekling,et al.  Electrophysiological properties of hypoglossal motoneurons of guinea-pigs studied in vitro , 1989, Neuroscience.

[16]  D. Kernell.  Functional properties of spinal motoneurons and gradation of muscle force. , 1983, Advances in neurology.

[17]  P. Schwindt,et al.  Factors influencing motoneuron rhythmic firing: results from a voltage-clamp study. , 1982, Journal of neurophysiology.

[18]  D A Bayliss,et al.  Multiple potassium conductances and their role in action potential repolarization and repetitive firing behavior of neonatal rat hypoglossal motoneurons. , 1993, Journal of neurophysiology.

[19]  Richard J Martin,et al.  Genioglossus Response to Airway Occlusion in Apneic Versus Nonapneic Infants , 1987, Pediatric Research.

[20]  Recruitment and firing rate modulation of motor unit tension in a small muscle of the cat's foot , 1975, Brain Research.

[21]  E. Barrett,et al.  Separation of two voltage‐sensitive potassium currents, and demonstration of a tetrodotoxin‐resistant calcium current in frog motoneurones. , 1976, The Journal of physiology.

[22]  G. Barrionuevo,et al.  In vitro electrophysiology of developing genioglossal motoneurons in the rat. , 1993, Journal of neurophysiology.

[23]  R. Burke.  Motor Units: Anatomy, Physiology, and Functional Organization , 1981 .

[24]  D. Bayliss,et al.  Calcium conductances and their role in the firing behavior of neonatal rat hypoglossal motoneurons. , 1993, Journal of neurophysiology.

[25]  Randall K. Powers,et al.  How different afferent inputs control motoneuron discharge and the output of the motoneuron pool , 1993, Current Opinion in Neurobiology.

[26]  D. Bayliss,et al.  Postnatal changes in rat hypoglossal motoneuron membrane properties , 1994, Neuroscience.

[27]  P. Schwindt,et al.  Repetitive firing in layer V neurons from cat neocortex in vitro. , 1984, Journal of neurophysiology.

[28]  P. Schwindt,et al.  Membrane-potential trajectories underlying motoneuron rhythmic firing at high rates. , 1973, Journal of neurophysiology.

[29]  K. Walton,et al.  Electrophysiological properties of neonatal rat motoneurones studied in vitro. , 1986, The Journal of physiology.

[30]  M. Bellingham,et al.  Characteristics and postnatal development of a hyperpolarization-activated inward current in rat hypoglossal motoneurons in vitro. , 1994, Journal of neurophysiology.

[31]  D. Kernell,et al.  Matching between motoneurone and muscle unit properties in rat medial gastrocnemius. , 1993, The Journal of physiology.

[32]  D. Kernell.  The Limits of Firing Frequency in Cat Lumbosacral Motoneurones Possessing Different Time Course of Afterhyperpolarization , 1965 .

[33]  B. Gustafsson,et al.  An investigation of threshold properties among cat spinal alpha‐motoneurones. , 1984, The Journal of physiology.

[34]  D. McCormick,et al.  Post‐natal development of electrophysiological properties of rat cerebral cortical pyramidal neurones. , 1987, The Journal of physiology.

[35]  D. Kernell.  The Adaptation and the Relation between Discharge Frequency and Current Strength of Cat Lumbosacral Motoneurones Stimulated by Long‐Lasting Injected Currents , 1965 .

[36]  R. Llinás,et al.  Identification of a critical period for motor development in neonatal rats , 1992, Neuroscience.

[37]  D. Bayliss,et al.  Mechanisms underlying excitatory effects of thyrotropin-releasing hormone on rat hypoglossal motoneurons in vitro. , 1992, Journal of neurophysiology.

[38]  T. Dick,et al.  Electrical properties of phrenic motoneurons in the cat: correlation with inspiratory drive. , 1987, Journal of neurophysiology.

[39]  M. Umemiya,et al.  Properties and function of low- and high-voltage-activated Ca2+ channels in hypoglossal motoneurons , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  D. Kernell,et al.  Repetitive impulse firing: comparisons between neurone models based on 'voltage clamp equations' and spinal motoneurones. , 1973, Acta physiologica Scandinavica.

[41]  P. Schwindt,et al.  Electrical properties of facial motoneurons in brainstem slices from guinea pig , 1989, Brain Research.