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Journal of Experimental Biology 153,141-153 (1990)
Published by Company of Biologists 1990

The Specificity of Synapse Formation by identified Leech Neurones in culture

J. G. NICHOLLS ¹, Y. LIU ², B. W. PAYTON ³, and D. P. KUFFLER ⁴

¹ Department of Pharmacology, Biocenter, University of Basel, Klingelbergstrasse 70, 4056 Basel, Switzerland
² Department of Pharmacology, Biocenter, University of Basel, Klingelbergstrasse 70, 4056 Basel, Switzerland; Department of Neurobiology and Behavior, SUNY at Stony Brook, NY 11794, USA
³ Department of Pharmacology, Biocenter, University of Basel, Klingelbergstrasse 70, 4056 Basel, Switzerland; Faculty of Medicine, The Health Sciences Center, Memorial University of Newfoundland, St John's, Newfoundland, Canada A1B 3V6
⁴ Department of Pharmacology, Biocenter, University of Basel, Klingelbergstrasse 70, 4056 Basel, Switzerland; Institute of Neurobiology, University of Puerto Rico, Old San Juan, PR 00901, USA

The physiological and fine structural events accompanying synapse formation have been followed while identified neurones of known function make contact in tissue culture. Particular pairs of identified neurones isolated from the central nervous system (CNS) of the leech form chemical synapses; other pairs of cells form nonrectifying electrical junctions, rectifying electrical junctions, mixed chemical and electrical synapses or no synapses at all, depending upon the partners that have been paired. Moreover, certain specific regions on the cell surface (such as the soma, initial cell segment or axon tips) preferentially develop chemical or electrical synapses. Of particular interest are the large, serotonergic Retzius cells that form mixed chemical and electrical synapses in culture, as in the animal. When these cells are juxtaposed at their initial segments, it has been shown that chemical synapses can develop reliably within 6h of contact in culture. Shortly after transmission can be detected physiologically, the principal features of synaptic structure are evident. The physiological and morphological characteristics resemble those of mature synapses studied within the central nervous system. Only at later times, after the chemical synapses have been formed, do electrical connections appear. By contrast, when other specialized regions of the Retzius cells are apposed (the tips of their axons), electrical synapses appear earlier. By comparing the connections that different types of serotonergic neurones make in culture we have been able to assess the role played by the transmitter in determining specificity: the results show that the transmitter does not determine what type of synapse is made on a particular partner. For example, Retzius cells make purely chemical synapses upon the sensory P neurone in culture; other serotonergic neurones (known as DL and VL) make purely electrical connections on this same pressure sensory neurone. Together, these results demonstrate that highly specific cell-cell recognition is a necessary feature of synapse formation after neurones have grown to their appropriate destinations.

Key words: leech, tissue culture, chemical synapses, electrical synapses

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