Abstract
Intracellular recordings and dye injections were used to examine mutual coupling among slow abdominal postural motoneurons in the 4th abdominal ganglion in crayfish (Procambarus clarkii). Intracellular current injection into one motoneuron altered the spike firing rate of some of its synergists. Depending on the polarity of the injected current, the premotor effect on the synergists was excitatory or inhibitory. The magnitude of the effect was intensity dependent. No dye coupling was found among the motoneurons following injection of Lucifer yellow. The morphological basis of the coupling was examined by differential filling of motoneuron pairs, one with horseradish peroxidase and the other with Lucifer yellow. The stained motoneurons were simultaneously visualized under light microscopy to determine the proximity of their differently colored dendrites. It was thus possible to locate the site of the presumed monosynaptic contacts between them. Combined physiological and morphological evidence suggests that these neurons are mutually coupled, forming part of an integrative system for abdominal posture control in crayfish.
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Chrachri A, Clarac F (1989) Synaptic connections between motor neurons and interneurons in the fourth thoracic ganglion of the crayfish, Procambarus clarkii. J Neurophysiol 62: 1237–1250
DeRiemer SA, Macagno ER (1981) Light microscopic analysis of contacts between pairs of identified leech neurons with combined use of horseradish peroxidase and Lucifer yellow. J Neurosci 1:650–657
Evoy WH, Kennedy D (1967) The central nervous organization underlying control of antagonistic muscles in the crayfish. I. Types of command fibers. J Exp Zool 165:223–238
Heitier WJ (1978) Coupled motoneurones are part of the crayfish swimmeret central oscillator. Nature (London) 275:231–233
Jellies J, Larimer JL (1985) Synaptic interactions between neurons involved in the production of abdominal posture in crayfish. J Comp Physiol A 156:861–873
Kennedy D (1969) The control of output by central neurons. In: Brazier MAB (ed) The interneuron. UCLA forum in medical sciences No. 11. Berkeley, University of California Press
Kennedy D, Takeda K (1965) Reflex control of abdominal flexor muscles in the crayfish. II. The tonic system. J Exp Biol 43:229–246
Kennedy D, Evoy WH, Hanawalt JT (1966a) Release of coordinated behavior in crayfish by single central neurons. Science 154:917–919
Kennedy D, Evoy WH, Fields HL (1966b) The unit basis of some crustacean reflexes. Symp Soc Exp Biol 75–109
Larimer JL (1988) The command hypothesis: a new view using an old example. Trends Neurosci 11:506–510
Leise EM, Hall WM, Mulloney B (1986) Functional organization of crayfish abdominal ganglia. I. The flexor systems. J Comp Neurol 253: 25–45
Macagno ER, Muller KJ, Kristan WB, DeRiemer SA, Stewart R, Granzow B (1981) Mapping of neuronal contacts with intracellular injection of horseradish peroxidase and Lucifer yellow in combination. Brain Res 217:143–149
Miall RC, Larimer JL (1982) Central organization of crustacean abdominal posture motoneurons: connectivity and command fiber inputs. J Exp Zool 224:45–56
Murphy BF, McAnelly ML, Larimer JL (1989) Abdominal positioning interneurons in crayfish: participation in behavioral acts. J Comp Physiol A 165:461–470
Nagayama T, Takahata M, Hisada M (1983) Local spikeless interaction of motoneuron dendrites in the crayfish Procambarus clarkii Girard. J Comp Physiol 152:335–345
Purves D, Hadley RD, Voyvodic JT (1986) Dynamic changes in the dendritic geometry of individual neurons visualized over periods of up to three months in the superior cervical ganglion of living mice. J Neurosci 6:1051–1060
Skinner K (1985) The structure of the fourth abdominal ganglion of the crayfish, Procambarus clarki (Girard). I. Tracts in the ganglionic core. J Comp Neurol 234:168–181
Sokolove PG, Tatton WG (1975) Analysis of postural motoneuron activity in crayfish abdomen. I. Coordination by premotoneuron connections. J Neurophysiol 38:313–331
Stewart WW (1978) Functional connections between cells as revealed by dye-coupling with a highly fluorescent naphthalimide tracer. Cell 14:741–759
Tatton WG, Sokolove PG (1975) Analysis of postural motoneuron activity in crayfish abdomen. II. Coordination by excitatory and inhibitory connections between motoneurons. J Neurophysiol 38:332–346
Toga T, Takahata M, Hisada M (1990) An identified set of local nonspiking interneurones which control the activity of abdominal postural motoneurones in crayfish. J Exp Biol 148:477–482
Van Harreveld A (1936) A physiological solution for freshwater crustaceans. Proc Soc Exp Biol Med 34:428–432
Watson AHD, Burrows M (1982) The ultrastructure of identified locust motor neurones and their synaptic relationships. J Comp Neurol 205:383–397
Wiersma CAG, Ikeda K (1964) Interneurons commanding swimmeret movements in the crayfish, Procambarus clarkii (Girard). Comp Biochem Physiol 12:509–525
Wine JJ, Hagiwara G (1977) Crayfish escape behavior. I. The structure of efferent and afferent neurons involved in abdominal extension. J Comp Physiol 121:145–172
Wine JJ, Mittenthal JE, Kennedy D (1974) The structure of tonic flexor motoneurons in crayfish abdominal ganglia. J Comp Physiol 93:315–335
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Toga, T., Hisada, M. Cross-connections coordinate postural motoneuron activity in the crayfish abdomen. J Comp Physiol A 173, 77–84 (1993). https://doi.org/10.1007/BF00209620
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DOI: https://doi.org/10.1007/BF00209620