Multiple mechanisms for integrating proprioceptive inputs that converge on the same motor pattern-generating network.
Journal of Neuroscience. 2008-08-27; 28(35): 8810-8820
DOI: 10.1523/JNEUROSCI.2095-08.2008
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Movement-derived sensory feedback adapts centrally generated motor programs to
changing behavioral demands. Motor circuit output may also be shaped by distinct
proprioceptive systems with different central actions, although little is known
about the integrative processes by which such convergent sensorimotor regulation
occurs. Here, we explore the combined actions of two previously identified
proprioceptors on the gastric mill motor network in the lobster stomatogastric
nervous system. Both mechanoreceptors [anterior gastric receptor (AGR) and
posterior stomach receptor (PSR)] access the gastric circuit via the same pair of
identified projection interneurons that either excite [commissural gastric (CG)]
or inhibit [gastric inhibitor (GI)] different subsets of gastric network neurons.
Mechanosensory information from the two receptors is integrated upstream to the
gastric circuit at two levels: (1) postsynaptically, where both receptors excite
the GI neuron while exerting opposing effects on the CG neuron, and (2)
presynaptically, where PSR reduces AGR’s excitation of the CG projection neuron.
Concomitantly PSR selectively enhances AGR’s activation of the GI neuron,
possibly also via a presynaptic action. PSR’s influences also far outlast its
transient synaptic effects, indicating the additional involvement of modulatory
processes. Consequently, PSR activation causes parallel input from AGR to be
conveyed preferentially via the GI interneuron, resulting in a prolonged switch
in the pattern of gastric circuit output. Therefore, via a combination of short-
and long-lasting, presynaptic and postsynaptic actions, one proprioceptive system
is able to promote its impact on a target motor network by biasing the access of
a different sensory system to the same circuit.