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The Journal of Neuroscience, February 20, 2008, 28(8):1916-1928; doi:10.1523/JNEUROSCI.4755-07.2008

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Behavioral/Systems/Cognitive
An Input-Representing Interneuron Regulates Spike Timing and Thereby Phase Switching in a Motor Network

Kosei Sasaki, Jian Jing, Michael R. Due, and Klaudiusz R. Weiss

Department of Neuroscience, Mount Sinai School of Medicine, New York, New York 10029

Correspondence should be addressed to Dr. Klaudiusz R. Weiss, Department of Neuroscience, Box 1065, Mount Sinai School of Medicine, 1 Gustave Levy Place, New York, NY 10029. Email: Klaudiusz.Weiss{at}mssm.edu

Despite the importance of spike-timing regulation in network functioning, little is known about this regulation at the cellular level. In the Aplysia feeding network, we show that interneuron B65 regulates the timing of the spike initiation of phase-switch neurons B64 and cerebral-buccal interneuron-5/6 (CBI-5/6), and thereby determines the identity of the neuron that acts as a protraction terminator. Previous work showed that B64 begins to fire before the end of protraction phase and terminates protraction in CBI-2-elicited ingestive, but not in CBI-2-elicited egestive programs, thus indicating that the spike timing and phase-switching function of B64 depend on the type of the central pattern generator (CPG)-elicited response rather than on the input used to activate the CPG. Here, we find that CBI-5/6 is a protraction terminator in egestive programs elicited by the esophageal nerve (EN), but not by CBI-2, thus indicating that, in contrast to B64, the spike timing and protraction-terminating function of CBI-5/6 depends on the input to the CPG rather than the response type. Interestingly, B65 activity also depends on the input in that B65 is highly active in EN-elicited programs, but not in CBI-2-elicited programs independent of whether the programs are ingestive or egestive. Notably, during EN-elicited egestive programs, hyperpolarization of B65 delays the onset of CBI-5/6 firing, whereas in CBI-2-elicited ingestive programs, B65 stimulation simultaneously advances CBI-5/6 firing and delays B64 firing, thereby substituting CBI-5/6 for B64 as the protraction terminator. Thus, we identified a neural mechanism that, in an input-dependent manner, regulates spike timing and thereby the functional role of specific neurons.

Key words: Aplysia; central pattern generator; feeding; spike timing; phase transition; motor programs


Received Oct. 19, 2007; revised Jan. 13, 2007; accepted Jan. 15, 2008.

Correspondence should be addressed to Dr. Klaudiusz R. Weiss, Department of Neuroscience, Box 1065, Mount Sinai School of Medicine, 1 Gustave Levy Place, New York, NY 10029. Email: Klaudiusz.Weiss{at}mssm.edu




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