Bimodal Respiratory–Locomotor Neurons in the Neonatal Rat Spinal Cord

Jean-Patrick Le Gal, Laurent Juvin, Laura Cardoit, Didier Morin
J. Neurosci.. 2016-01-20; 36(3): 926-937
DOI: 10.1523/jneurosci.1825-15.2016

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Le Gal JP(1), Juvin L(1), Cardoit L(1), Morin D(2).

Author information:
(1)Institut de Neurosciences Cognitives et Intégratives d’Aquitaine, CNRS, UMR
5287, Université de Bordeaux, 33076 Bordeaux, France.
(2)Institut de Neurosciences Cognitives et Intégratives d’Aquitaine, CNRS, UMR
5287, Université de Bordeaux, 33076 Bordeaux, France .

Neural networks that can generate rhythmic motor output in the absence of sensory
feedback, commonly called central pattern generators (CPGs), are involved in many
vital functions such as locomotion or respiration. In certain circumstances,
these neural networks must interact to produce coordinated motor behavior adapted
to environmental constraints and to satisfy the basic needs of an organism. In
this context, we recently reported the existence of an ascending excitatory
influence from lumbar locomotor CPG circuitry to the medullary respiratory
networks that is able to depolarize neurons of the parafacial respiratory group
during fictive locomotion and to subsequently induce an increased respiratory
rhythmicity (Le Gal et al., 2014b). Here, using an isolated in vitro
brainstem-spinal cord preparation from neonatal rat in which the respiratory and
the locomotor networks remain intact, we show that during fictive locomotion
induced either pharmacologically or by sacrocaudal afferent stimulation, the
activity of both thoracolumbar expiratory motoneurons and interneurons is
rhythmically modulated with the locomotor activity. Completely absent in spinal
inspiratory cells, this rhythmic pattern is highly correlated with the hindlimb
ipsilateral flexor activities. Furthermore, silencing brainstem neural circuits
by pharmacological manipulation revealed that this locomotor-related drive to
expiratory motoneurons is solely dependent on propriospinal pathways. Together
these data provide the first evidence in the newborn rat spinal cord for the
existence of bimodal respiratory-locomotor motoneurons and interneurons onto
which both central efferent expiratory and locomotor drives converge, presumably
facilitating the coordination between the rhythmogenic networks responsible for
two different motor functions. Significance statement: In freely moving animals,
distant regions of the brain and spinal cord controlling distinct motor acts must
interact to produce the best adapted behavioral response to environmental
constraints. In this context, it is well established that locomotion and
respiration must to be tightly coordinated to reduce muscular interferences and
facilitate breathing rate acceleration during exercise. Here, using
electrophysiological recordings in an isolated in vitro brainstem-spinal cord
preparation from neonatal rat, we report that the locomotor-related signal
produced by the lumbar central pattern generator for locomotion selectively
modulates the intracellular activity of spinal respiratory neurons engaged in
expiration. Our results thus contribute to our understanding of the cellular
bases for coordinating the rhythmic neural circuitry responsible for different
behaviors.

Copyright © 2016 the authors 0270-6474/16/360926-12$15.00/0.

 

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