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Cellular substrates of action selection: a cluster of higher-order descending neurons shapes body posture and locomotion

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Abstract

The selection of distinct movements involved in various body postures and locomotion is often dependent on higher-order descending neurons. To study how such cells select different actions, we used a nearly-intact leech preparation (Hirudo sp.) in which cephalic projection interneurons were recorded and stimulated while the leech generated overt behaviors. Two long-distance projecting neurons were identified in the sub-packet of the third neuromere (R3b) of the subesophageal ganglion. These interneurons, named R3b2 and R3b3, produced changes in whole-body posture, crawling and swimming. Cell R3b2 reliably caused the body to become turgid, to hyper-elongate, and to thrash cyclically. Such robust activity resembled struggling behavior exhibited by intact leeches when grasped. The neighboring cell R3b3 elicited body elongation accompanied by a static whole-body bend to the left or right. R3b3 activity was context-dependent, oscillated in phase with crawling, reset the crawl rhythm, and terminated swimming. Both neuronal types responded to multi-modal sensory stimulation delivered to various rostral and caudal regions of the body. Our study illustrates the need to study behavioral selection with a neuroethological approach, and provides a cellular substrate for the motor action-selection cluster proposed for the vertebrate brainstem.

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Abbreviations

CPG:

Central pattern generator

DP nerve:

Dorsal posterior nerve

M 1–21:

Midbody ganglia 1–21

R3b:

Posterior packet of third neuromere

SEG:

Subesophageal ganglion

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Acknowledgments

We wish to thank Kathleen A. Klukas for her expert assistance with preparation of some of the figures, and Dr. Alan Roberts for helpful comments on a draft of this manuscript. This work was funded, in part, by grants from the National Science Foundation IOB-0523959 (KAM and WBK) and the National Institutes of Health (NIH) MH43396 and NS35336 (WBK). Additional funding was provided by a National Research Service Award MH12029 and NIH Training Grant NS07220 (TE), and University of Minnesota Career Development Grant (KAM).

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Authors and Affiliations

  1. Departments of Entomology and Neuroscience, University of Minnesota, 219 Hodson Hall, 1980 Folwell Ave, St Paul, MN, 55108, USA

    Karen A. Mesce

  2. Section of Neurobiology, Division of Biological Sciences, University of California, San Diego, La Jolla, CA, 92093, USA

    Teresa Esch & William B. Kristan Jr

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  1. Karen A. Mesce
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Correspondence to Karen A. Mesce.

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Mesce, K.A., Esch, T. & Kristan, W.B. Cellular substrates of action selection: a cluster of higher-order descending neurons shapes body posture and locomotion. J Comp Physiol A 194, 469–481 (2008). https://doi.org/10.1007/s00359-008-0319-1

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