A brainstem neural substrate for stopping locomotion
Article [Accepted Manuscript]
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Journal of neuroscience ; vol. 39, no. 6, pp. 1044-1057.Publisher(s)
Society for NeuroscienceAuthor(s)
Abstract(s)
Locomotion occurs sporadically and needs to be started, maintained, and stopped.
The neural substrate underlying the activation of locomotion is partly known, but
little is known about mechanisms involved in termination of locomotion. Recently,
reticulospinal neurons (stop cells) were found to play a crucial role in stopping
locomotion in the lamprey: their activation halts ongoing locomotion and their
inactivation slows down the termination process. Intracellular recordings of
these cells revealed a distinct activity pattern, with a burst of action
potentials at the beginning of a locomotor bout and one at the end (termination
burst). The termination burst was shown to be time linked to the end of
locomotion, but the mechanisms by which it is triggered have remained unknown. We
studied this in larval sea lampreys (Petromyzon marinus; the sex of the animals
was not taken into account). We found that the mesencephalic locomotor region
(MLR), which is known to initiate and control locomotion, stops ongoing
locomotion by providing synaptic inputs that trigger the termination burst in
stop cells. When locomotion is elicited by MLR stimulation, a second MLR
stimulation stops the locomotor bout if it is of lower intensity than the initial
stimulation. This occurs for MLR-induced, sensory-evoked, and spontaneous
locomotion. Furthermore, we show that glutamatergic and, most likely,
monosynaptic projections from the MLR activate stop cells during locomotion.
Therefore, activation of the MLR not only initiates locomotion, but can also
control the end of a locomotor bout. These results provide new insights onto the
neural mechanisms responsible for stopping locomotion.SIGNIFICANCE STATEMENT The
mesencephalic locomotor region (MLR) is a brainstem region well known to initiate
and control locomotion. Since its discovery in cats in the 1960s, the MLR has
been identified in all vertebrate species tested from lampreys to humans. We now
demonstrate that stimulation of the MLR not only activates locomotion, but can
also stop it. This is achieved through a descending glutamatergic signal, most
likely monosynaptic, from the MLR to the reticular formation that activates
reticulospinal stop cells. Together, our findings have uncovered a neural
mechanism for stopping locomotion and bring new insights into the function of the
MLR.
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