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The Journal of Neuroscience, September 23, 2009, 29(38):11732-11744; doi:10.1523/JNEUROSCI.3051-09.2009

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Behavioral/Systems/Cognitive
Distinct Inhibitory Neurons Exert Temporally Specific Control over Activity of a Motoneuron ReceivingConcurrent Excitation and Inhibition

Kosei Sasaki, Vladimir Brezina, Klaudiusz R. Weiss, and Jian Jing

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

Correspondence should be addressed to Dr. Jian Jing, Department of Neuroscience, Box 1065, Mount Sinai School of Medicine, 1 Gustave Levy Place, New York, NY 10029. Email: jingj01{at}gmail.com

Recent work suggests that concurrent excitation and inhibition originating in central pattern generators (CPGs) may be used to control rhythmic motoneuronal activity. The specific roles that the inhibition plays in such cases are not well understood, however, in part because of the lack of identification of presynaptic inhibitory neurons. Here we demonstrate that, in the Aplysia feeding CPG, inhibitory inputs may be critical for flexible control of the activity of motoneurons in different forms of behavior. The feeding CPG generates ingestive and egestive motor programs, differing in the high and low activity, respectively, of the motoneuron B8 during the retraction phase of the programs. We show that, during retraction, B8 receives concurrent excitation and inhibition that produces a high-conductance state. The inhibition originates in two types of CPG neurons, B4/5 and B70, that are more active in egestion than ingestion and play a role in suppressing B8 activity during egestion. In turn, the activities of both B4/5 and B70 are suppressed by the ingestion-promoting descending interneuron CBI-3 (for cerebral–buccal interneuron 3). Thus, concurrent excitation and inhibition may be an effective means of controlling motoneuronal activity in a behavior-dependent manner. More detailed analyses reveal, furthermore, that B4/5 and B70 exert complementary actions by acting preferentially in the early and late part of retraction, respectively. Thus, the use of multiple neurons to generate inhibitory inputs to motoneurons that receive concurrent excitation and inhibition brings an additional level of flexibility that allows a temporally specific control of motoneuronal activity within a single phase of motor programs.

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Received June 26, 2009; revised Aug. 1, 2009; accepted Aug. 5, 2009.

Correspondence should be addressed to Dr. Jian Jing, Department of Neuroscience, Box 1065, Mount Sinai School of Medicine, 1 Gustave Levy Place, New York, NY 10029. Email: jingj01{at}gmail.com

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