Skip to main content
Log in

Sensory-synaptic interactions in crayfish stretch receptor neurones

  • Published:
Biological Cybernetics Aims and scope Submit manuscript

Abstract

1. This communication describes, in the tonic stretch receptor organ (RM1) of crayfish, the inhibitory fibre's influence upon sensory modulated discharges. Periodic trapezoidal length changes were imposed, and rate plots of the afferent discharges were compared without inhibition (C) and with inhibition, either irregular (P) or regular (R), and at different rates. 2. Inhibition changed all sensory response components. Changes were dependent on issues as inhibitory rates and patterns, RM 1 discharge modulations, and pre-post-synaptic rate ratios. The most common effect was rate reduction, usually non-uniform along the cycle and with little evidence of proportionality. Saturation, i.e., inefficacy of shifts around extreme inhibitory rates was apparent. Rate increases occurred also. Accelerations were manifest by increased phasic lengthening response slopes and heights, by “faster inhibitor-faster inhibited” relations, or by postinhibitory rebounds. 3. Irregular inhibitory discharges (i) favoured variability along individual and average cycles, (ii) favoured monotonicity, (iii) rarely silenced the RM 1, and (iv) reduced without eliminating nonproportionality and saturation. 4. Regular inhibitory discharges showed the most clear-cut nonmonotonicities and saturations silencing the RM 1 effectively. Furthermore, they included characteristic epochs where (i) the RM 1 spike slid across the invariant interinhibition intervals, (ii) intervals recurred in stereotyped sequences and (iii) rate ratios had special values (e.g., 1:1, 1:2). Thus, the gradually decaying slope of the control adaptation after the lengthening transient was changed into a staircase profile or a sudden drop to a constant plateau. 5. Inhibition changed phasic and tonic sensitivities, usually refucing them (phasic decreasing less than tonic); increases, joint or individual, occurred also. The fidelity with which the rate plot reproduced the sensory stimulus was modified in many ways (e.g., by conversion into a phasic prototype, or into a system with perfect reproduction, etc.). Changes depended on the inhibitory discharge, and on the stimulus features. 6. These experiments have implications in two fields. In that of synaptic rate effects, (i) they confirm that the inhibition repertory includes slowings (predominant here) and accelerations, plus special effects, and (ii) they demonstrate extensively their dependence on the post-synaptic features. In the field of sensory control, they note sensory-synaptic interactions that, in intact animals, must arise but whose characteristics and roles can only be conjectured about.

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.

Similar content being viewed by others

References

  • Alexandrowicxz JS (1967) Receptor organs in thoracic and abdominal muscles of crustacea. Biol Rev 42:288–326

    Google Scholar 

  • Barrio LC (1986) Interacciones Dinámicas Excitatorio-Inhibitorias en una Neurona Marcapasos. (PhD thesis): U.A.M., Madrid

  • Barrio LC, Buño W Jr (1984) Dynamics of excitatoryinhibitory interactions in the slow-adapting stretch receptor organ of crayfish. Neurosci Lett [Suppl] 18:s258

  • Barrio LC, Buño W Jr (1986) Biphasic effect of synaptic inhibition and hyperpolarizing current pulses in an isolated neuron. Neurosci Lett [Suppl] 26:s495

    Google Scholar 

  • Barrio LC, Buño W Jr (1988) Dynamic analysis of sensoryinhibitory interactions in the crayfish stretch receptor. J Neurophysiol (submitted for publication)

  • Brown HM, Ottoson D, Rydqvist R (1978) Crayfish stretch receptor: an investigation with voltage-clamp and ionsensitive electrodes. J Physiol (London) 284:55–179

    Google Scholar 

  • Buño W Jr (1984) Information processing by pacemaker neurons. In: Reinoso-Suarez F., Ajmone-Marsan C (eds) Cortical integration. Basic, archicortical and cortical association levels of neural integration. Raven Press, New York, pp 37–51

    Google Scholar 

  • Buño W. Jr, Fuentes J, Segundo JP (1978) Crayfish stretchreceptor organs: effects of length-steps with and without perturbations. Biol Cybern 31:99–110

    Article  PubMed  Google Scholar 

  • Buño W Jr, Bustamante J, Fuentes J (1983) Modifications of dynamic and static behavior by small-length perturbations in crayfish stretch receptor organ. J Neurobiol 14:177–194

    Article  PubMed  Google Scholar 

  • Buño W Jr, Fuentes J, Barrio LC (1987) Modulation of pacemaker activity by IPSP and brief length perturbations in the crayfish stretch receptor. J Neurophysiol 57:819–834

    Google Scholar 

  • Calvin WH, Hartline DK (1977) Retrograde invasion of lobster stretch receptor somata in control of firing rate and extra spike patterning. J Neurophysiol 40:106–118

    PubMed  Google Scholar 

  • Eckert RO (1961) Reflex relationships of abdominal stretch receptors of the crayfish. I. Feedback inhibition of the receptors. J Cell Comp Physiol 57:149–162

    Article  PubMed  Google Scholar 

  • Jansen JKS, Nja A, Ormsad D, Walloe L (1970a) Inhibitory control of abdominal stretch receptors of the crayfish. III. The accessory reflex as a recurrent inhibitory feedback. Acta Physiol Scand 81:472–483

    Google Scholar 

  • Jansen JKS, Nja A, Walloe L (1970b) Inhibitory control of the abdominal stretch receptors of the crayfish. I. Existence of double inhibitory feed-back. Acta Physiol Scand 80:420–425

    PubMed  Google Scholar 

  • Kandel ER, Frazier WT, Wachtel H (1969) Organization of inhibition in abdominal ganglion of Aplysia. I. Role of inhibition and disinhibition in transforming neural activity. J Neurophysiol 32:496–508

    PubMed  Google Scholar 

  • Kohn AF, Segundo JP (1983) Neuromime and computer simulations of synaptic interactions between pacemakers. Mathematical expansions of existing models. J Theor Neurobiol 2:101–125

    Google Scholar 

  • Kohn AF, Rocha AF, Segundo JP (1981) Presynaptic irregularity and pacemaker inhibition. Biol Cybern 41:5–18

    Article  Google Scholar 

  • Kuffler SW, Eyzaguirre C (1955) Synaptic inhibition in isolated nerve cell. J Gen Physiol 39:155–184

    Article  PubMed  Google Scholar 

  • Liestol K (1983) The effect of the time pattern of presynaptic impulses on the transfer of information across an inhibitory synapse. Acta Physiol Scand 117:227–232

    PubMed  Google Scholar 

  • Nakajima S, Onodera K (1969a) Membrane properties of the stretch receptor neurons of crayfish with particular reference to mechanism of sensory adaptation. J Physiol (London) 200:161–185

    Google Scholar 

  • Nakajima S, Onodera K (1969b) Adaptation of generator potential in the crayfish stretch receptor under constant length and constant tension. J Physiol (London) 200:186–204

    Google Scholar 

  • Nakajima S, Takahashi K (1966) Post-tetanic hyperpolarization and electrogenic Na pump in stretch receptor neurone of crayfish. J Physiol (London) 187:105–127

    Google Scholar 

  • Perkel DH, Schulman JH, Bullock TH, Moore GP, Segundo JP (1964) Pacemaker neurons: effects of regularly spaced synaptic input. Science (NY) 145:61–63

    Google Scholar 

  • Schulman JH (1969) Information transfer across an inhibitory to pacemaker synapse at the crayfish stretch receptor. (PhD thesis). University of California, Los Angeles

  • Segundo JP (1979) Pacemaker synaptic interaction: modelled locking and paradoxical features. Biol Cybern 35:56–62

    Article  Google Scholar 

  • Segundo JP (1987) Synaptic rate effects. In: Adelman G (ed) Encyclopaedia of the neurosciences. Birkhäuser, Boston

    Google Scholar 

  • Segundo JP, Diez Martinez O (1985) Stretch receptor responses to sinusoidal stimuli depend critically on modulation depth and background length. Biol Cybern 51:375–382

    Article  Google Scholar 

  • Segundo JP, Tolkunov BF, Wolfe GE (1976) Relation between trains of action potentials across an inhibitory synapse. Influence of presynaptic irregularity. Biol Cybern 24:167–179

    Article  Google Scholar 

  • Sokolove PG, Cooke IM (1971) Inhibition of impulse activity in a sensory neuron by an electrogenic pump. J Gen Physiol 57:125–163

    Article  PubMed  Google Scholar 

  • Swerup C, Rydqvist B, Ottoson D (1983) Time characteristics and potential dependence of early and late adaptation in crustacean stretch receptor. Acta Physiol Scand 199:91–99

    Google Scholar 

  • Terzuolo CA, Purple RL, Bayly E, Handelman E (1968) Postsynaptic inhibition: its action upon the transducer and encoder systems of neurons. In: Structure and function of inhibitory neuronal mechanism. Pergamon Press London, pp 261–285

    Google Scholar 

  • Torras i Genis C (1985) Temporal-pattern learning in neural models Springer, Berlin Heidelberg New York

    Google Scholar 

  • Van Harreveld A (1936) A physiological solution for fresh water crustacean. Proc Soc Exp Biol Med 34:428–432

    Google Scholar 

  • Vibert JF, Davis M, Segundo JP (1979) Recurrent inhibition. Influence upon transduction and afferent discharges in slowly adapting stretch receptor organs. Biol Cybern 33:167–178

    Article  PubMed  Google Scholar 

  • Vibert JF, Caille D, Segundo JP (1985) Examination with a computer of how parameter changes and variabilities influence a model of oscillator entrainment. Biol Cybern 53:79–91

    Article  Google Scholar 

  • Wilkens LA, Wolfe GE (1974) A new electrode design for en passant recording. Comp Biochem Physiol 48:217–220

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Visiting Professor from the Department of Anatomy and Brain Rescarch Institute, University of California, Los Angeles, USA

Rights and permissions

Reprints and permissions

About this article

Cite this article

Barrio, L.C., Buño, W. & Segundo, J.P. Sensory-synaptic interactions in crayfish stretch receptor neurones. Biol. Cybern. 59, 385–394 (1988). https://doi.org/10.1007/BF00336112

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00336112

Keywords

Navigation