Abstract
Nonspiking local interneurones are the important premotor elements in arthropod motor control systems. We have analyzed the synaptic interactions between nonspiking interneurones in the crayfish terminal (6th) abdominal ganglion using simultaneous intracellular recordings. Only 15% of nonspiking interneurones formed bi-directional excitatory connections. In 77% of connections, however, the nonspiking interneurones showed a one-way inhibitory interaction. In these cases, the presynaptic nonspiking interneurones received excitatory synaptic inputs from the sensory afferents innervating hairs on the surface of the uropods and the postsynaptic nonspiking interneurones received inhibitory synaptic inputs that were partly mediated by the inputs to the presynaptic nonspiking interneurones. The membrane hyperpolarization of the postsynaptic nonspiking interneurones mediated by the presynaptic nonspiking interneurones was reduced in amplitude when the hyperpolarizing current was injected into the postsynaptic interneurones, or when the external bathing solution was replaced with one containing low calcium and high magnesium concentrations. The role of these interactions in the circuits controlling the movements of the terminal appendages is discussed.
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Abbreviations
- AL:
-
antero-lateral
- epsp:
-
excitatory postsynaptic potential
- ipsp:
-
inhibitory postsynaptic potential
- PL:
-
postero-lateral
References
Aonuma H, Nagayama T (1999) GABAergic and non-GABAergic spiking interneurons of local and intersegmental groups in the crayfish terminal abdominal ganglion. J Comp Neurol 410:677–688
Burrows M (1979) Graded synaptic interactions between local pre-motor interneurons of the locust. J Neurophysiol 42:1108–1123
Burrows M (1992) Local circuits for the control of leg movements in an insect. TINS 15:226–232
Burrows M, Siegler MVS (1976) Transmission without spikes between locust interneurones and motoneurones. Nature 262:222–224
Büschges A, Schmitz J (1991) Nonspiking pathways antagonize the resistance reflex in the thoraco-coxal joint of stick insects. J Neurobiol 22:224–237
DiCaprio RA, Fourtner CR (1988) Neural control of ventilation in the shore crab, Carcinus maenas. II. Frequency-modulating interneurons. J Comp Physiol A 162:375–388
Harreveld A van (1936) A physiological solution for freshwater crustaceans. Proc Soc Exp Biol Med 34:428–442
Heitler WJ, Pearson KG (1980) Non-spiking interactions and local interneurones in the central pattern generator of the crayfish swimmeret system. Brain Res 187:206–211
Kobashi M, Yamaguchi T (1984) Local non-spiking interneurons in the cercus-to-giant interneuron system of crickets. Naturwissenschaften 71:154–156
Mendelson M (1971) Oscillator neurons in crustacean ganglia. Science 171:1170–1173
Nagayama T (1997) Organization of exteroceptive inputs onto nonspiking local interneurones in the crayfish terminal abdominal ganglion. J Exp Zool 279:29–42
Nagayama T (1999) Uropod common inhibitory motor neurone in the terminal abdominal ganglion of the crayfish. J Exp Zool 283:541–547
Nagayama T (2002) Synaptic organization of local circuit neurons in the terminal abdominal ganglion of the crayfish. In: Wiese K (ed) The crustacean nervous system. Springer, Berlin Heidelberg New York, pp 591–600
Nagayama T, Hisada M (1987) Opposing parallel connections through crayfish local nonspiking interneurons. J Comp Neurol 257:347–358
Nagayama T, Sato M (1993) the organization of exteroceptive information from the uropod to ascending interneurones of the crayfish. J Comp Physiol A 172:281–294
Nagayama T, Takahata M, Hisada M (1983) Local spikeless interaction of motoneuron dendrites in the crayfish Procambarus clarkii Girard. J Comp Physiol A 152:335–345
Nagayama T, Takahata M, Hisada M (1984) Functional characteristics of local non-spiking interneurons as the pre-motor elements in crayfish. J Comp Physiol A 154:499–510
Nagayama T, Namba H, Aonuma H (1994) Morphological and physiological bases of crayfish local circuit neurones. Histol Histopathol 9:791–805
Nagayama T, Aonuma H, Miyata H (1996) GABA-like immunoreactivity of an identified nonspiking local interneurone in the crayfish terminal abdominal ganglion. J Exp Biol 199:2447–2450
Nagayama T, Namba H, Aonuma H (1997) Distribution of GABAergic pre-motor nonspiking local interneurones in the terminal abdominal ganglion of the crayfish. J Comp Neurol 389:139–148
Nagayama T, Kimura K, Araki M, Aonuma H, Newland PL (2004) Distribution of glutamatergic immunoreactive neurons in the terminal abdominal ganglion of the crayfish. J Comp Neurol (in press)
Namba H, Nagayama T, Hisada M (1994) Descending control of nonspiking local interneurons in the terminal abdominal ganglion of the crayfish. J Neurophysiol 72:235–247
Namba H, Nagayama T, Takahata M (1997) Non-spiking local interneurones mediate abdominal extension related descending control of uropod motor neurones in the crayfish terminal abdominal ganglion. J Comp Physiol A 180:463–472
Newland PL, Nagayama T (1993) Parallel processing of proprioceptive information in the terminal abdominal ganglion of the crayfish. J Comp Physiol A 172:389–400
Pearson KG, Fourtner CR (1975) Nonspiking interneurons in walking system of the cockroach. J Neurophysiol 88:33–52
Takahata M, Nagayama T, Hisada M (1981) Physiological and morphological characterization of anaxonic non-spiking interneurons in the crayfish motor control system. Brain Res 226:309–314
Vaney DI (1991) Many diverse types of retinal neurons show tracer coupling when injected with biocytin or neurobiotin. Neurosci Lett 125:187–190
Wildman M, Ott SR, Burrows M (2002) GABA-like immunoreactivity in nonspiking interneurons of the locust metathoracic ganglion. J Exp Biol 205:3651–3659
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This work was supported by Ministry of Education, Science, Sport, Culture and Technology Grant to T.N.
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Namba, H., Nagayama, T. Synaptic interactions between nonspiking local interneurones in the terminal abdominal ganglion of the crayfish. J Comp Physiol A 190, 615–622 (2004). https://doi.org/10.1007/s00359-004-0516-5
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DOI: https://doi.org/10.1007/s00359-004-0516-5