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Embryonic electrical connections appear to prefigure a behavioral circuit in the leech CNS

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Abstract

During development, many embryos show electrical coupling among neurons that is spatially and temporally regulated. For example, in vertebrate embryos extensive dye coupling is seen during the period of circuit formation, suggesting that electrical connections could prefigure circuits, but it has been difficult to identify which neuronal types are coupled. We have used the leech Hirudo medicinalis to follow the development of electrical connections within the circuit that produces local bending. This circuit consists of three layers of neurons: four mechanosensory neurons (P cells), 17 identified interneurons, and approximately 24 excitatory and inhibitory motor neurons. These neurons can be identified in embryos, and we followed the spatial and temporal dynamics as specific connections developed. Injecting Neurobiotin into identified cells of the circuit revealed that electrical connections were established within this circuit in a precise manner from the beginning. Connections first appeared between motor neurons; mechanosensory neurons and interneurons started to connect at least a day later. This timing correlates with the development of behaviors, so the pattern of emerging connectivity could explain the appearance first of spontaneous behaviors (driven by a electrically coupled motor network) and then of evoked behaviors (when sensory neurons and interneurons are added to the circuit).

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Acknowledgements

This work was supported by NIH research grant NS35336 to WBK, a Fundacion Antorchas grant to AMB and an NIH training grant T32AG00216 to FJE. We thank Pablo E. Schilman for assistance with statistical analyses and comments on the manuscript. The experiments comply with the “Principles of animal care”, publication No. 86–23, revised 1985, of the National Institute of Health.

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Authors and Affiliations

  1. Section of Neurobiology, Division of Biological Sciences, University of California, 3119 Pacific Hall, San Diego, La Jolla, CA, 92093-0357, USA

    Antonia Marin-Burgin, William B. Kristan Jr & Kathleen A. French

  2. Microsoft Research, 810 W. Emerson St., Seattle, WA, 98119, USA

    F. James Eisenhart

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  1. Antonia Marin-Burgin
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  2. F. James Eisenhart
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  3. William B. Kristan Jr
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Correspondence to Antonia Marin-Burgin.

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Marin-Burgin, A., Eisenhart, F.J., Kristan, W.B. et al. Embryonic electrical connections appear to prefigure a behavioral circuit in the leech CNS. J Comp Physiol A 192, 123–133 (2006). https://doi.org/10.1007/s00359-005-0055-8

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