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The Journal of Neuroscience, February 23, 2005, 25(8):1965-1978; doi:10.1523/JNEUROSCI.3881-04.2005
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Behavioral/Systems/Cognitive
Respiratory Rhythm Entrainment by Somatic Afferent Stimulation
Jeffrey T. Potts,1 Ilya A. Rybak,2 andJulian F. R. Paton3 1Department of Physiology, Wayne State University School of Medicine, Detroit, Michigan 48201, 2School of Biomedical Engineering, Science and Health Systems, Drexel University, Philadelphia, Pennsylvania 19104, and 3Department of Physiology, School of Medical Sciences, University of Bristol, Bristol BS8 1TD, United Kingdom
Respiratory and locomotor patterns are coupled during locomotion. The objectives of this study were to (1) demonstrate that respiratory rhythms are entrained by sensory input from somatic afferents, (2) establish whether the parabrachial nucleus mediates entrainment, (3) examine responses of single respiratory neurons in the ventral respiratory group (VRG) to somatic afferent stimulation, and (4) use a computational model of the pontomedullary respiratory network (Rybak et al., 2004a,b) to suggest neuronal mechanisms for entrainment.
We used an in situ preparation in young rats that retained pontomedullary respiratory circuits and spinal pathways transmitting somatosensory input. We demonstrate that rhythmic stimulation of somatic afferents entrains respiratory rhythm on a 1:1 basis (1:1), increasing breathing frequency up to
1.4-2.2 times greater than spontaneous frequency. Stable entrainment occurred only when stimuli were delivered during expiration. Reversible blockade of the lateral parabrachial nucleus eliminated entrainment. Somatic afferent stimulation produced significant increases in the firing rate of augmenting expiratory (E2) neurons but shortened the firing duration of postinspiratory (post-I) neurons. A computational model reproduced 1:1 entrainment and other experimental findings based on the assumption that the somatic afferents initiate early onset of inspiration via activation of medullary E2 neurons. The model also predicted that afferent stimulation evoked transient hyperpolarization of ramp-inspiratory (ramp-I) neurons. This was confirmed experimentally by intracellular recording from ramp-I neurons. Our experimental and modeling results demonstrate that an entrainment pathway from somatic afferents to the VRG via the lateral parabrachial nucleus causes resetting of respiratory rhythm through excitation of E2 and consequent inhibition of post-I neurons.
Key words: respiratory control; somatosensory input; pontomedullary respiratory network; entrainment; sensory-motor integration; locomotion
Received Sep 24, 2004; revised January 7, 2005; accepted January 8, 2005.
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