Spinal connections of ventral-group bulbospinal inspiratory neurons studied with cross-correlation in the decerebrate rat

Abstract

We examined the synaptic connections from ventral-group bulbospinal inspiratory neurons to upper-cervical inspiratory neurons and phrenic and intercostal motoneurons in decerebrate rats using cross-correlation. Inspiratory neurons were recorded in the medulla (n = 28) at the level of the obex and from the upper-cervical segments (C1 and C2) of the spinal cord (n = 29) in 18 vagotomized, paralyzed, ventilated, and decerebrated rats. The neurons were identified by their inspiratory firing pattern and antidromic activation from the spinal cord at C7. Whole-nerve recordings were made using bipolar electrodes from the central cut ends of the C5 phrenic nerve and the external and internal intercostal nerves at various thoracic levels. Cross-correlation histograms were computed between these recordings to detect short time scale synchronizations indicative of synaptic connections. Cross-correlation histograms (n = 20), computed between the activities of ventral-group bulbospinal inspiratory neurons and the phrenic nerve, all showed peaks (mean half-amplitude width +/- SD, 1.1 +/- 0.3 ms) at short latencies (mean latency +/- SD, 2.0 +/- 0.6 ms) suggestive of monosynaptic excitation. Cross-correlation histograms (n = 33), computed between the activities of ventral-group bulbospinal inspiratory neurons and upper-cervical inspiratory neurons, displayed four (12%) peaks (mean half-amplitude width +/- SD, 0.9 +/- 0.1 ms) at short latencies (mean latency +/- SD, 1.8 +/- 0.6 ms) suggestive of monosynaptic excitation, and six (18%) peaks (mean half-amplitude width +/- SD, 1.4 +/- 0.4 ms) at latencies near zero suggestive of excitation from a common source. Cross-correlation histograms (n = 34), computed between the activities of ventral-group bulbospinal inspiratory neurons and the internal and external intercostal nerves at various thoracic levels (T2-8), showed six (18%) peaks (mean half-amplitude width +/- SD, 2.5 +/- 0.5 ms) at short latency (mean latency +/- SD, 4.5 +/- 1.1 ms) suggestive of oligosynaptic connections. Cross-correlation histograms (n = 42) computed between activities of intercostal nerves at various levels of the thoracic spinal cord showed central peaks suggestive of excitation from a common source. Although the size of the peaks decreased with segmental separation, the displacement of the peaks from time zero did not increase with segmental separation (mean displacement +/- SD, 0.6 +/- 0.6 ms) as would be expected if the common excitation resulted from a descending monosynaptic excitation by a source such as the ventral-group bulbospinal inspiratory neurons. We conclude that all ventral-group bulbospinal inspiratory neurons make monosynaptic connections to phrenic motoneurons, a few make monosynaptic connections to upper-cervical, inspiratory neurons, but connections to intercostal motoneurons are made via interneurons.