Neural mechanisms generating respiratory pattern in mammalian brain stem-spinal cord in vitro. I. Spatiotemporal patterns of motor and medullary neuron activity

Abstract

1. An analysis of the spatial and temporal patterns of activity of neurons of the respiratory motor-pattern generation system in an in vitro neonatal rat brain stem-spinal cord preparation is presented. Impulse discharge patterns of spinal and cranial moto-neurons as well as respiratory neurons in the medulla were analyzed. Patterns of motoneuronal discharge were characterized at the population level from recordings of motor-nerve discharge and at the single-cell level from intracellular recordings. These patterns were compared to patterns generated in the neonatal rat and adult mammal in vivo to establish the correspondence between in vitro and in vivo states. 2. The in vitro system generated a complex spatiotemporal pattern of spinal and cranial motoneuron activity during inspiratory (I) and expiratory (E) phases of the respiratory cycle. The respiratory cycle consisted of three distinct phases of neuronal activity (I, early E, and late E phase) similar to the temporal organization of the cycle in the intact mammal. The spike discharge pattern of motoneurons during the I phase consisted of a rapidly peaking-slowly decrementing discharge envelope with a high degree of synchronization on a time scale of 25-50 ms (approximately 20-40 Hz). A similar pattern was generated in the neonate in vivo under conditions comparable with the in vitro state (i.e., nervous system isolated from mechanosensory afferent inputs). However, the I-phase-motoneuron discharge pattern and cycle-phase durations differed from those characteristic of the intact neonatal or adult systems in vivo. This difference could be accounted for primarily by removal of vagal mechanosensory afferent inputs. 3. The synaptic drive potentials of spinal motoneurons during the I phase in vitro consisted of a rapidly peaking-slowly decrementing potential envelope similar in shape to the spike-frequency histogram of single motoneurons and the envelope of the motoneuron-population discharge. The drive potentials had prominent high-frequency amplitude fluctuations superimposed on the slower drive-potential envelope that were temporally correlated with the generation of motoneuron action potentials. The dominant frequency components of these fast-membrane-potential oscillations (20-35 Hz) were similar to the frequency components of the amplitude fluctuations in the motoneuron-population discharge. One class of medullary neurons with I-phase discharge also exhibited a rapidly peaking-slowly decrementing pattern of impulse discharge and synaptic drive potential with similar high-frequency components.(ABSTRACT TRUNCATED AT 400 WORDS)