Identified nonspiking local interneurons mediate nonrecurrent, lateral inhibition of crayfish mechanosensory interneurons

Abstract

1. We have used intracellular neuropil recordings and dye injection to identify a pair of nonspiking, Local, Directionally Selective (LDS) interneurons in the terminal ganglion of the crayfish,Procambarus clarkii. The neurons have bilateral but asymmetric processes connected by a thick (ca. 17 μm) segment in the dorsal neuropil. The processes ipsilateral to the soma are smooth while those on the other side have numerous varicosities (Figs. 1, 2). 2. We found headward water movement to be the best natural stimulus for depolarizing the LDS interneurons (Fig. 3). Neither water movement nor any combination of electrical stimulation of afferents and current injection into the LDS interneurons ever caused them to spike. 3. The receptive field of the LDS interneuron is mainly restricted to the uropods ipsilateral to its cell body, and within that field the afferents from the endopodite provide the strongest excitation. The afferent-produced PSPs are chemically mediated and are probably monosynaptic; they occur with an estimated synaptic delay of approximately 1 ms (Figs. 4, 5). 4. The output of the LDS interneuron is contralateral to the input side and is associated with the processes having varicosities. Thus, although the neuron is nonspiking, it is functionally polarized to receive input on one side of the ganglion and convey it to the other side. 5. All known output connections of the LDS interneuron are inhibitory and highly specific. The LDS interneuron exclusively inhibits projection interneurons excited by headward afferents on the output side. Not all headward projection interneurons are inhibited equally (Fig. 6 and Table 1). 6. The inhibitory effect of the LDS interneuron is mediated postsynaptically by chemical IPSPs (Fig. 7). The LDS cell does not cause inhibition at rest potential, and the threshold for causing inhibition in at least one postsynaptic interneuron was 10 mV of depolarization of the LDS cell. The inhibitory pathway between the LDS interneuron and the postsynaptic neurons is stable (Figs. 8, 9). 7. The LDS interneurons mediate lateral inhibition that is both nonrecurrent and reciprocal. Because the LDS interneurons are nonspiking, once above threshold they deliver a precise but inverted copy of the afference on one side to the projecting interneurons on the other side. These features have many consequences, including the ability to attenuate common signals that arise from ambient water movement, and conversely to accentuate the different afference produced by laterally asymmetric signals. We have used intracellular neuropil recordings and dye injection to identify a pair of nonspiking, Local, Directionally Selective (LDS) interneurons in the terminal ganglion of the crayfish,Procambarus clarkii. The neurons have bilateral but asymmetric processes connected by a thick (ca. 17 μm) segment in the dorsal neuropil. The processes ipsilateral to the soma are smooth while those on the other side have numerous varicosities (Figs. 1, 2). We found headward water movement to be the best natural stimulus for depolarizing the LDS interneurons (Fig. 3). Neither water movement nor any combination of electrical stimulation of afferents and current injection into the LDS interneurons ever caused them to spike. The receptive field of the LDS interneuron is mainly restricted to the uropods ipsilateral to its cell body, and within that field the afferents from the endopodite provide the strongest excitation. The afferent-produced PSPs are chemically mediated and are probably monosynaptic; they occur with an estimated synaptic delay of approximately 1 ms (Figs. 4, 5). The output of the LDS interneuron is contralateral to the input side and is associated with the processes having varicosities. Thus, although the neuron is nonspiking, it is functionally polarized to receive input on one side of the ganglion and convey it to the other side. All known output connections of the LDS interneuron are inhibitory and highly specific. The LDS interneuron exclusively inhibits projection interneurons excited by headward afferents on the output side. Not all headward projection interneurons are inhibited equally (Fig. 6 and Table 1). The inhibitory effect of the LDS interneuron is mediated postsynaptically by chemical IPSPs (Fig. 7). The LDS cell does not cause inhibition at rest potential, and the threshold for causing inhibition in at least one postsynaptic interneuron was 10 mV of depolarization of the LDS cell. The inhibitory pathway between the LDS interneuron and the postsynaptic neurons is stable (Figs. 8, 9). The LDS interneurons mediate lateral inhibition that is both nonrecurrent and reciprocal. Because the LDS interneurons are nonspiking, once above threshold they deliver a precise but inverted copy of the afference on one side to the projecting interneurons on the other side. These features have many consequences, including the ability to attenuate common signals that arise from ambient water movement, and conversely to accentuate the different afference produced by laterally asymmetric signals.

DOI: 10.1007/BF00623903

9 Figures and Tables

Statistics

050100150'03'05'07'09'11'13'15'17
Citations per Year

193 Citations

Semantic Scholar estimates that this publication has 193 citations based on the available data.

See our FAQ for additional information.

Cite this paper

@article{Reichert2004IdentifiedNL, title={Identified nonspiking local interneurons mediate nonrecurrent, lateral inhibition of crayfish mechanosensory interneurons}, author={Heinrich Reichert and Mark R. Plummer and Jeffrey J. Wine}, journal={Journal of comparative physiology}, year={2004}, volume={151}, pages={261-276} }