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

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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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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Keywords

  • Central pattern generator
  • Command neuron
  • Reticulospinal neurons
  • Locomotion
  • Leech