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New vistas on the initiation and maintenance of insect motor behaviors revealed by specific lesions of the head ganglia

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Abstract

In insects, thoracic pattern generators are modulated by the two head ganglia, the supraesophageal ganglion (brain) and the subesophageal ganglion, which act as higher-order neuronal centers. To explore the contribution of each head ganglion to the initiation and maintenance of specific motor behaviors in cockroaches (Periplaneta americana), we performed specific lesions to remove descending inputs from either the brain or the subesophageal ganglion or both, and quantified the behavioral outcome with a battery of motor tasks. We show that ‘emergency’ behaviors, such as escape, flight, swimming or righting, are initiated at the thoracic level independently of descending inputs from the head ganglia. Yet, the head ganglia play a major role in maintaining these reflexively initiated behaviors. By separately removing each of the two head ganglia, we show that the brain excites flight behavior and inhibits walking-related behaviors, whereas the subesophageal ganglion exerts the opposite effects. Thus, control over specific motor behaviors in cockroaches is anatomically and functionally compartmentalized. We propose a comprehensive model in which the relative permissive versus inhibitory inputs descending from the two head ganglia, combined with thoracic afferent sensory inputs, select a specific thoracic motor pattern while preventing the others.

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Abbreviations

B-DINs:

Brain descending interneurons

CirC:

Circumesophageal connectives

Df:

Fast coxal depressors

DMI:

Descending mechanosensory interneuron

Ds:

Slow coxal depressors

EMG:

Electromyogram

PG:

Pattern generator

SEG:

Subesophageal ganglion

SEG-DINs:

SEG descending interneurons

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Acknowledgements

We thank Gustavo Glusman for his valuable technical assistance. We also thank Aviva Weisel-Eichler, Lior Ann Rosenberg, Yael Lavi, Gal Haspel and two anonymous reviewers for valuable comments. This work was supported by Grant 2001044 from the United States-Israel Binational Science Foundation (BSF). These experiments comply with the “Principles of animal care”, publication No. 86–23, revised 1985 of the National Institute of Health, and also with the current laws of the State of Israel.

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  1. Department of Life Sciences and the Zlotowski Center for Neuroscience, Ben-Gurion University of the Negev, P.O. Box 653, Beer-Sheva, 84105, Israel

    Ram Gal & Frederic Libersat

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  1. Ram Gal
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  2. Frederic Libersat
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Correspondence to Frederic Libersat.

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Gal, R., Libersat, F. New vistas on the initiation and maintenance of insect motor behaviors revealed by specific lesions of the head ganglia. J Comp Physiol A 192, 1003–1020 (2006). https://doi.org/10.1007/s00359-006-0135-4

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