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Phase-coupling of the respiratory network by somatosensory receptors during locomotion
Respiratory Researchvolume 2, Article number: P7 (2001)
Phase-coupling of the respiratory rhythm to locomotor activity has been reported in quadrupeds and humans . Ventral respiratory group (VRG) neurons are involved in respiratory rhythm generation due, in part, to both intrinsic and synaptic interactions between pre-Botzinger and Botzinger complex neurons , as well as the influence of extrinsic synaptic drive to the VRG network. The aim of this study was to determine the role of neuro-genic input from somatosensory receptors on the bursting patterns of respiratory neurons in the VRG network. We hypothesized that neural input from contraction-sensitive somatosensory receptors entrained respiration by modulating the phasic activity of VRG neurons. Experiments were performed using the working heart-brainstem preparation . Rats (70–100 g) were anesthetized, decerebrated pre-collicularly, paralyzed and perfused with a Ringers solution plus an oncotic agent. Somatosensory afferents were stimulated by intermittent contraction of the forelimb (3 ms pulses, 90–150 V, 10–15 g of developed tension). Phrenic (PNA) and central vagus (CVA) nerve activities were recorded using suction electrodes and the extra-cellular single-unit activity of VRG neurons was recorded using glass microelectrodes (tip resistance: 5–15 mΩ). Neurons were classified based on their bursting patterns relative to the phase of the respiratory cycle as inspiratory (I; n = 18), post-inspiratory (PI; n = 21) or augmenting expiratory (E-AUG; n = 12). Intermittent activation of somatosensory afferents entrained respiratory motor outflow to the frequency of forelimb contraction and generated a 1:1 phase-coupled rhythm. In order to determine the effect of somatosensory receptor activation on the bursting patterns of respiratory neurons, forelimb contraction was evoked during specific phases of the respiratory cycle. Once a respiratory neuron was identified and its ongoing activity was characterized, somatosensory afferents were activated by a single twitch contraction of the forelimb. When somatic afferents were activated during early PI phase 67% of PI neurons were inhibited (n = 14); whereas, 58% of E-AUG neurons were excited (n = 7). In contrast, only 33% of Ineurons were inhibited when the forelimb was contracted during early inspiration (n = 6). From these findings, we conclude that the phase-locking of respiratory rhythm to repetitive muscle contraction is mediated by somatosensory-evoked excitation of E-AUG neurons and inhibition of PIneurons. Our findings suggest that peripheral feedback from somatosensory afferents modulates respiratory network activity in discrete phases of the respiratory cycle during locomotion.
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This work was funded by the National Institutes of Health HL49167 (JTP) and the British Heart Foundation BS/93003 (JFRP).