Skip to main content
Log in

Excitatory connections of nonspiking interneurones in the terminal abdominal ganglion of the crayfish

  • Original Paper
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

The output effects of the nonspiking interneurones in the crayfish terminal abdominal ganglion upon the uropod motor neurones were characterized using simultaneous intracellular recordings. Inhibitory interactions from nonspiking interneurones to the uropod motor neurones were one-way and chemically mediated. The depolarization of the motor neurones with current injection increased the amplitude of the nonspiking interneurone-mediated hyperpolarization, while hyperpolarization of the motor neurone decreased it. By contrast, excitatory interactions from the nonspiking interneurones to the motor neurones were not mediated via chemical synaptic transmissions. These excitatory connections with the slow motor neurones were one-way while connections with fast motor neurones were bidirectional. Nonspiking interneurone-mediated membrane depolarization of the motor neurones was not affected by the passage of hyperpolarizing current. Each motor neurone spike elicited a time-locked EPSP in the nonspiking interneurones with very short delay (0.2 ms) that suggested electrical coupling between nonspiking interneurones and motor neurones. Nonspiking interneurones directly control the organization of slow motor neurone activity, while they appear to regulate the background activity of the fast motor neurones. A single nonspiking interneurone is possible to inhibit some inter and/or motor neurones via direct chemical synapses and simultaneously excite other neurones via electrical synapses.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

AL:

Antero-lateral

cl:

Closer

EPSP:

Excitatory postsynaptic potential

mn:

Motor neurone

ns int:

Nonspiking interneurone

op:

Opener

PL:

Postero-lateral

r1:

Nerve root 1

r2:

Nerve root 2

r3:

Nerve root 3

red mn:

Reductor motor neurone

References

  • Antonsen BL, Edwards DH (2003) Differential dye coupling reveals lateral giant escape circuit in crayfish. J Comp Neurol 466:1–13

    Article  PubMed  Google Scholar 

  • Burrows M (1980) The control of sets of motoneurones by local interneurones in the locust. J Physiol (Lond) 298:213–233

    Article  CAS  Google Scholar 

  • Burrows M (1992) Local circuits for the control of leg movements in an insect. TINS 15:226–232

    CAS  PubMed  Google Scholar 

  • Bush BMH (1981) Non-impulsive stretch receptors in crustaceans. In: Roberts A, Bush BMH (eds) Neurones without impulses. Cambridge University Press, Cambridge, pp 147–176

    Google Scholar 

  • Curti S, Pereda AE (2004) Voltage-dependent enhancement of electrical coupling by a subthreshold sodium current. J Neurosci 24:3999–4010

    Article  CAS  PubMed  Google Scholar 

  • El Manira A, Cattaert D, Wallen P, DiCaprio RA, Clarac F (1993) Electrical coupling of mechanoreceptor afferents in the crayfish: a possible mechanism for enhancement of sensory signal transmission. J Neurophysiol 69:2248–2251

    PubMed  Google Scholar 

  • Fan RJ, Marin-Burgin A, French KA, Otto Friesen W (2005) A dye mixture (Neurobiotin and Alexa 488) reveals extensive dye-coupling among neurons in leeches; physiology confirms the connections. J Comp Physiol A 191:1157–1171

    Article  Google Scholar 

  • Furshpan EJ, Potter DD (1959) Slow post-synaptic potentials recorded from the giant motor fibre of the crayfish. J Physiol 145:326–335

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Haag J, Borst A (2005) Dye-coupling visualizes networks of large-field motion-sensitive neurons in the fly. J Comp Physiol A 191:445–454

    Article  Google Scholar 

  • Heitler WJ, Fraser K, Edwards DH (1991) Different types of rectification at electrical synapses made by a single crayfish neurone investigated experimentally and by computer simulation. J Comp Physiol A 169:707–718

    Article  CAS  PubMed  Google Scholar 

  • Marder E (1987) Neurotransmitters and neuromodulators. In: Selverston AI, Moulins M (eds) The crustacean stomatogastric system. Springer, Berlin, pp 263–300

    Chapter  Google Scholar 

  • Nagayama T (1999) The uropod common inhibitory motor neurone in the terminal abdominal ganglion of the crayfish. J Exp Zool 279:29–42

    Article  Google Scholar 

  • Nagayama T (2005) GABAergic and glutamatergic inhibition of nonspiking local interneurones in the terminal abdominal ganglion of the crayfish. J Exp Zool 303A:66–75

    Article  CAS  Google Scholar 

  • Nagayama T, Hisada M (1987) Opposing parallel connections through crayfish local nonspiking interneurons. J Comp Neurol 257:347–358

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Nagayama T, Takahata M, Hisada M (1986) Behavioural transition of crayfish avoidance reaction in response to uropod stimulation. Exp Biol 46:75–82

    CAS  PubMed  Google Scholar 

  • Nagayama T, Namba H, Aonuma H (1994) Morphological and physiological bases of crayfish local circuit neurones. Histol Histopath 9:791–805

    CAS  Google Scholar 

  • 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 389:138–148

    Article  Google Scholar 

  • Nagayama T, Araki M, Newland PL (2002) Lateral giant fibre activation of exopodite motor neurones in the crayfish tailfan. J Comp Physiol A 188:621–630

    Article  CAS  Google Scholar 

  • 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 474:123–135

    Article  PubMed  Google Scholar 

  • Namba H, Nagayama T (2004) Synaptic interactions between nonspiking local interneurones in the terminal abdominal ganglion of the crayfish. J Comp Physiol A 190:615–622

    Article  CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Newland PL, Aonuma H, Nagayama T (1997) Monosynaptic excitation of lateral giant fibres by proprioceptive afferents in the crayfish. J Comp Physiol A 181:103–109

    Article  Google Scholar 

  • Paul DH, Mulloney B (1985) Nonspiking local interneuron in the motor pattern generator for the crayfish swimmeret. J Neurophysiol 54:28–39

    CAS  PubMed  Google Scholar 

  • Pereda AE, Bell TD, Faber DS (1995) Retrograde synaptic communication via gap junctions coupling auditory afferents to the Mauthner cell. J Neurosci 15:5943–5955

    CAS  PubMed  Google Scholar 

  • Rela L, Szczupak L (2003) Coactivation of motoneurons regulated by a network combining electrical and chemical synapses. J Neurosci 23:682–692

    CAS  PubMed  Google Scholar 

  • Rodriguez MJ, Perez-Etchegoyen CB, Szczupak L (2009) Premotor nonspiking neurons regulate coupling among motoneurons that innervate overlapping muscle fiber population. J Comp Physiol A 195:491–500

    Article  Google Scholar 

  • Rodriguez MJ, Alvarez RJ, Szczupak L (2012) Effect of a nonspiking neuron on motor patterns of the leech. J Neurophysiol 107:1917–1924

    Article  PubMed  Google Scholar 

  • Shepherd GM (1981) Synaptic and impulse loci in olfactory bulb dendritic circuits. In: Roberts A, Bush BMH (eds) Neurones without impulses. Cambridge University Press, Cambridge, pp 255–267

    Google Scholar 

  • Smarandache-Wellmann C, Weller C, Mulloney B (2014) Mechanisms of coordination in distributed neural circuits: decoding and integration of coordinating information. J Neurosci 34:793–803

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Takeuchi A, Takeuchi N (1965) Localized action of gamma-aminobutyric acid on the crayfish muscle. J Physiol 177:225–238

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • van Harreveld A (1936) A physiological solution for freshwater crustaceans. Proc Soc Exp Biol Med 34:428–432

    Article  Google Scholar 

  • Werblin FS (1979) Integrative pathways in local circuits between slow-potential cells in the retina. In: Schmitt FO, Worden FG (eds) The neurosciences, fourth study program, 8th edn. MIT Press, Cambridge, pp 193–211

    Google Scholar 

  • Wildman M, Ott SR, Burrows M (2002) GABA-like immunoreactivity in nonspiking interneurons of the locust metathoracic ganglion. J Exp Biol 205:3651–3659

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by Grants-in-Aid from the Ministry of Education, Science, Sport, and Culture to TN (25440165). All experiments were carried out in accordance with the Guide for the care and use of Laboratory animals of Yamagata University (Japan).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Toshiki Nagayama.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Namba, H., Nagayama, T. Excitatory connections of nonspiking interneurones in the terminal abdominal ganglion of the crayfish. J Comp Physiol A 201, 773–781 (2015). https://doi.org/10.1007/s00359-015-1017-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-015-1017-4

Keywords

Navigation