Skip to main content
Log in

Roles for inhibition: studies on networks controlling swimming in young frog tadpoles

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

Abstract

The hatchling frog tadpole provides a simple preparation where the fundamental roles for inhibition in the central nervous networks controlling behaviour can be examined. Antibody staining reveals the distribution of at least ten different populations of glycinergic and GABAergic neurons in the CNS. Single neuron recording and marker injections have been used to study the roles and anatomy of three types of inhibitory neuron in the swimming behaviour of the tadpole. Spinal commissural interneurons control alternation of the two sides by producing glycinergic reciprocal inhibition. By interacting with the special membrane properties of excitatory interneurons they also contribute to rhythm generation through post-inhibitory rebound. Spinal ascending interneurons produce recurrent glycinergic inhibition of sensory pathways that gates reflex responses during swimming. In addition their inhibition also limits firing in CPG neurons during swimming. Midhindbrain reticulospinal neurons are excited by pressure to the head and produce powerful GABAergic inhibition that stops swimming when the tadpole swims into solid objects. They may also produce tonic inhibition while the tadpole is at rest that reduces spontaneous swimming and responsiveness of the tadpole, keeping it still so it is not noticed by predators.

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

aIN:

Ascending interneuron

cIN:

Commissural interneuron

CPG:

Central pattern generator

dIN:

Descending interneuron

dla:

Dorsolateral ascending interneuron

dlc:

Dorsolateral commissural interneuron

K–A:

Kolmer–Agduhr cell

mhr:

Midhindbrain reticulospinal interneuron

mn:

Motoneuron

PIR:

Post-inhibitory rebound

RB:

Rohon–Beard neuron

References

  • Binor E, Heathcote RD (2001) Development of GABA-immunoreactive neuron patterning in the spinal cord. J Comp Neurol 438:1–11

    Article  PubMed  CAS  Google Scholar 

  • Boothby KM, Roberts A (1992) The stopping response of Xenopus laevis embryos: pharmacology and intracellular physiology of rhythmic spinal neurones and hindbrain neurones. J Exp Biol 169:65–86

    PubMed  CAS  Google Scholar 

  • Boothby KM, Roberts A (1995) Effects of site and strength of tactile stimulation on the swimming responses of Xenopus laevis embryos. J Zool (Lond) 235:113–125

    Article  Google Scholar 

  • Cangiano L, Grillner S (2005) Mechanisms of rhythm generation in a spinal locomotor network deprived of crossed connections: the lamprey hemicord. J Neurosci 25:923–935

    Article  PubMed  CAS  Google Scholar 

  • Dale N (1985) Reciprocal inhibitory interneurones in the Xenopus embryo spinal cord. J Physiol (Lond) 363:61–70

    CAS  Google Scholar 

  • Dale N (1995) Experimentally derived model for the locomotor pattern generator in the Xenopus embryo. J Physiol (Lond) 489:489–510

    CAS  Google Scholar 

  • Dale N (2003) Coordinated motor activity in simulated spinal networks emerges from simple biologically plausible rules of connectivity. J Comput Neurosci 14:55–70

    Article  PubMed  Google Scholar 

  • Dale N, Ottersen OP, Roberts A, Storm-Mathisen J (1986) Inhibitory neurones of a motor pattern generator in Xenopus revealed by antibodies to glycine. Nature 324:255–257

    Article  PubMed  CAS  Google Scholar 

  • Dale N, Roberts A, Ottersen OP, Storm-Mathisen J (1987) The morphology and distribution of ‘‘Kolmer–Agduhr cells,’’ a class of cerebrospinal-fluid-contacting neurons revealed in the frog embryo spinal cord by GABA immunocytochemistry. Proc R Soc B 232:193–203

    CAS  Google Scholar 

  • Green CS, Soffe SR (1998) Roles of ascending inhibition during two rhythmic motor patterns in Xenopus tadpoles. J Neurophysiol 79:2316–2328

    PubMed  CAS  Google Scholar 

  • Higashijima S, Masino MA, Mandel G, Fetcho JR (2004) Engrailed-1 expression marks a primitive class of inhibitory spinal interneuron. J Neurosci 24:5827–5839

    Article  PubMed  CAS  Google Scholar 

  • Jamieson D, Roberts A (2000) Responses of young Xenopus laevis tadpoles to light dimming: possible roles for the pineal eye. J Exp Biol 203(Pt 12):1857–1867

    PubMed  CAS  Google Scholar 

  • Kahn JA, Roberts A (1982) The neuromuscular basis of rhythmic struggling movements in embryos of Xenopus laevis. J Exp Biol 99:197–205

    PubMed  CAS  Google Scholar 

  • Kahn JA, Roberts A, Kashin SM (1982) The neuromuscular basis of swimming movements in embryos of the amphibian Xenopus laevis. J Exp Biol 99:175–184

    PubMed  CAS  Google Scholar 

  • Lambert TD, Li WC, Soffe SR, Roberts A (2004a) Brainstem control of activity and responsiveness in resting frog tadpoles: tonic inhibition. J Comp Physiol A 190:331–342

    Article  CAS  Google Scholar 

  • Lambert TD, Howard J, Plant A, Soffe S, Roberts A (2004b) Mechanisms and significance of reduced activity and responsiveness in resting frog tadpoles. J Exp Biol 207:1113–1125

    Article  PubMed  Google Scholar 

  • Li WC, Perrins R, Soffe SR, Yoshida M, Walford A, Roberts A (2001) Defining classes of spinal interneuron and their axonal projections in hatchling Xenopus laevis tadpoles. J Comp Neurol 441:248–265

    Article  PubMed  CAS  Google Scholar 

  • Li WC, Soffe SR, Roberts A (2002) Spinal inhibitory neurons that modulate cutaneous sensory pathways during locomotion in a simple vertebrate. J Neurosci 22:10924–10934

    PubMed  CAS  Google Scholar 

  • Li WC, Soffe SR, Roberts A (2003a) The spinal interneurons and properties of glutamatergic synapses in a primitive vertebrate cutaneous flexion reflex. J Neurosci 23:9068–9077

    PubMed  CAS  Google Scholar 

  • Li WC, Perrins R, Walford A, Roberts A (2003b) The neuronal targets for GABAergic reticulospinal inhibition that stops swimming in hatchling frog tadpoles. J Comp Physiol A 189:29–37

    CAS  Google Scholar 

  • Li W-C, Soffe SR, Roberts A (2004a) Dorsal spinal interneurons forming a primitive, cutaneous sensory pathway. J Neurophysiol 92:895–904

    Article  PubMed  CAS  Google Scholar 

  • Li WC, Higashijima S, Parry DM, Roberts A, Soffe SR (2004b) Primitive roles for inhibitory interneurons in developing frog spinal cord. J Neurosci 24:5840–5848

    Article  PubMed  CAS  Google Scholar 

  • Li W-C, Soffe SR, Wolf E, Roberts A (2006) Persistent pesponses to brief stimuli: feedback excitation among brainstem neurons. J Neurosci 26:4026–4035

    Article  PubMed  CAS  Google Scholar 

  • Nabekura J, Katsurabayashi S, Kakazu Y, Shibata S, Matsubara A, Jinno S, Mizoguchi Y, Sasaki A, Ishibashi H (2004) Developmental switch from GABA to glycine release in single central synaptic terminals. Nat Neurosci 7:17–23

    Article  PubMed  CAS  Google Scholar 

  • Pearson KG (1993) Common principles of motor control in vertebrates and invertebrates. Annu Rev Neurosci 16:265–297

    Article  PubMed  CAS  Google Scholar 

  • Perkel DH, Mulloney B (1974) Motor pattern production in reciprocally inhibitory neurons exhibiting post-inhibitory rebound. Science 185:181–183

    Article  PubMed  CAS  Google Scholar 

  • Perrins R, Walford A, Roberts A (2002) Sensory activation and role of inhibitory reticulospinal neurons that stop swimming in hatchling frog tadpoles. J Neurosci 22:4229–4240

    PubMed  CAS  Google Scholar 

  • Poulet JFA, Hedwig B (2007) New insights into corollary discharges mediated by identified neural pathways. Trends Neurosci 30:14

    Article  PubMed  CAS  Google Scholar 

  • Renshaw B (1946) Central effects of centripetal impulses in axons of spinal ventral roots. J Neurophysiol 9:191–204

    Google Scholar 

  • Roberts A (1980) The function and role of two types of mechanoreceptive ‘free’ nerve endings in the head skin of amphibian embryos. J Comp Physiol A 135:341–348

    Article  Google Scholar 

  • Roberts A (2000) Early functional organization of spinal neurons in developing lower vertebrates. Brain Res Bull 53:585–593

    Article  PubMed  CAS  Google Scholar 

  • Roberts A, Blight AR (1975) Anatomy, physiology and behavioural role of sensory nerve endings in the cement gland of embryonic Xenopus. Proc R Soc B 192:111–127

    CAS  Google Scholar 

  • Roberts A, Clarke JDW (1982) The neuroanatomy of an amphibian embryo spinal cord. Phil Trans R Soc 296:195–212

    Article  CAS  Google Scholar 

  • Roberts A, Tunstall MJ (1990) Mutual re-excitation with post-inhibitory rebound: a simulation study on the mechanisms for locomotor rhythm generation in the spinal cord of Xenopus embryos. Eur J Neurosci 2:11–23

    Article  PubMed  Google Scholar 

  • Roberts A, Dale N, Ottersen OP, Storm-Mathisen J (1987) The early development of neurons with GABA immunoreactivity in the CNS of Xenopus laevis embryos. J Comp Neurol 261:435–449

    Article  PubMed  CAS  Google Scholar 

  • Roberts A, Dale N, Ottersen OP, Storm-Mathisen J (1988) Development and characterization of commissural interneurones in the spinal cord of Xenopus laevis embryos revealed by antibodies to glycine. Development 103:447–461

    PubMed  CAS  Google Scholar 

  • Satterlie RA (1985) Reciprocal inhibition and postinhibitory rebound produce reverberation in a locomotor pattern generator. Science 229:402–404

    Article  PubMed  Google Scholar 

  • Sautois B, Soffe SR, Li W-C, Roberts A (2007) Role of type-specific neuron properties in a spinal cord motor network. J Comput Neurosci 23:59–77

    Article  PubMed  Google Scholar 

  • Seki K, Perlmutter SI, Fetz EE (2003) Sensory input to primate spinal cord is presynaptically inhibited during voluntary movement. Nat Neurosci 6:1309–1316

    Article  PubMed  CAS  Google Scholar 

  • Sherrington CS (1906) The integrative action of the nervous system, Yale University Press, New Haven

    Google Scholar 

  • Sillar KT, Roberts A (1988) A neuronal mechanism for sensory gating during locomotion in a vertebrate. Nature 331:262–265

    Article  PubMed  CAS  Google Scholar 

  • Sillar KT, Roberts A (1992) The role of premotor interneurons in phase-dependent modulation of a cutaneous reflex during swimming in Xenopus laevis embryos. J Neurosci 12:1647–1657

    PubMed  CAS  Google Scholar 

  • Sillar KT, Wedderburn JF, Simmers AJ (1991) The development of swimming rhythmicity in post-embryonic Xenopus laevis. Proc R Soc B 246:147–153

    Article  PubMed  CAS  Google Scholar 

  • Soffe SR (1989) Roles of glycinergic inhibition and N-methyl-d-aspartate receptor mediated excitation in the locomotor rhythmicity of one half of the Xenopus embryo central nervous system. Eur J Neurosci 1:561–571

    Article  PubMed  Google Scholar 

  • Soffe SR (1990) Active and passive membrane properties of spinal cord neurons that are rhythmically active during swimming in Xenopus embryos. Eur J Neurosci 2:1–10

    Article  PubMed  Google Scholar 

  • Soffe SR (1991) Triggering and gating of motor responses by sensory stimulation: behavioural selection in Xenopus embryos. Proc R Soc Lond B 246:197–203

    Article  CAS  Google Scholar 

  • Soffe SR (1993) Two distinct rhythmic motor patterns are driven by common premotor and motor neurons in a simple vertebrate spinal cord. J Neurosci 13:4456–4469

    PubMed  CAS  Google Scholar 

  • Soffe SR, Clarke JD, Roberts A (1984) Activity of commissural interneurons in spinal cord of Xenopus embryos. J Neurophysiol 51:1257–1267

    PubMed  CAS  Google Scholar 

  • Soffe SR, Zhao FY, Roberts A (2001) Functional projection distances of spinal interneurons mediating reciprocal inhibition during swimming in Xenopus tadpoles. Europ J Neurosci 13:617–627

    Article  CAS  Google Scholar 

  • Vu ET, Krasne FB (1993) Crayfish tonic inhibition: prolonged modulation of behavioral excitability by classical GABAergic inhibition. J Neurosci 13:4394–4402

    PubMed  CAS  Google Scholar 

  • Wu LG, Saggau P (1997) Presynaptic inhibition of elicited neurotransmitter release. Trends Neurosci 20:204–212

    Article  PubMed  CAS  Google Scholar 

  • Yoshida M, Roberts A, Soffe SR (1998) Axon projections of reciprocal inhibitory interneurons in the spinal cord of young Xenopus tadpoles and implications for the pattern of inhibition during swimming and struggling. J Comp Neurol 400:504–518

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank firstly our colleagues past and present for making the work reported here possible and providing a stimulating and friendly environment and secondly, the Wellcome Trust and MRC for many years of financial support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alan Roberts.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Roberts, A., Li, WC. & Soffe, S.R. Roles for inhibition: studies on networks controlling swimming in young frog tadpoles. J Comp Physiol A 194, 185–193 (2008). https://doi.org/10.1007/s00359-007-0273-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-007-0273-3

Keywords

Navigation