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The Journal of Neuroscience, August 25, 2004, 24(34):7455-7463; doi:10.1523/JNEUROSCI.1840-04.2004
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Behavioral/Systems/Cognitive
Intercircuit Control via Rhythmic Regulation of Projection Neuron Activity
Debra E. Wood,1,2
Yair Manor,3
Farzan Nadim,4 and
Michael P. Nusbaum1
1Department of Neuroscience, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania 19104-6074, 2Department of Biology, Case Western Reserve University, Cleveland, Ohio 44106, 3Zlotowski Center for Neuroscience and Department of Life Science, Ben-Gurion University, BeerSheva 84105, Israel, and 4Department of Biological Sciences, Rutgers University, and Department of Mathematical Sciences, New Jersey Institute of Technology, Newark, New Jersey 07102
Synaptic feedback from rhythmically active neuronal circuits commonly causes their descending inputs to exhibit the rhythmic activity pattern generated by that circuit. In most cases, however, the function of this rhythmic feedback is unknown. In fact, generally these inputs can still activate the target circuit when driven in a tonic activity pattern. We are using the crab stomatogastric nervous system (STNS) to test the hypothesis that the neuronal circuit-mediated rhythmic activity pattern in projection neurons contributes to intercircuit regulation. The crab STNS contains an identified projection neuron, modulatory commissural neuron 1 (MCN1), whose tonic stimulation activates and modulates the gastric mill (chewing) and pyloric (filtering of chewed food) motor circuits in the stomatogastric ganglion (STG). During tonic stimulation of MCN1, the pyloric circuit regulates both gastric mill cycle frequency and gastropyloric coordination via a direct synapse onto a gastric mill neuron in the STG. However, when MCN1 is spontaneously active, it has a pyloric-timed activity pattern attributable to synaptic input from the pyloric circuit. This pyloric-timed activity in MCN1 provides the pyloric circuit with a second pathway for regulating the gastric mill rhythm. At these times, the direct STG synapse from the pyloric circuit to the gastric mill circuit is not necessary for pyloric regulation of the gastric mill rhythm. However, in the intact system, these two pathways play complementary roles in this intercircuit regulation. Thus, one role for rhythmicity in modulatory projection neurons is to enable them to mediate the interactions between distinct but related neuronal circuits.
Key words: central pattern generator; neuromodulation; stomatogastric ganglion; pyloric circuit; gastric mill circuit; modulatory projection neuron
Received May 12, 2004;
revised July 2, 2004;
accepted July 3, 2004.
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