Skip to main content
Log in

Heterosynaptic modulation of the dorsal root potential in the turtle spinal cord in vitro

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

In the somatosensory system, the flow of sensory information is regulated at early stages by presynaptic inhibition. Recent findings have shown that the mechanisms generating the primary afferent depolarization (PAD) associated with presynaptic inhibition are complex, with some components mediated by a non-spiking mechanism. How sensory inputs carried by neighbouring afferent fibres interact to regulate the generation of PAD, and thus presynaptic inhibition, is poorly known. Here, we investigated the interaction between neighbouring primary afferents for the generation of PAD in an in vitro preparation of the turtle spinal cord. To monitor PAD we recorded the dorsal root potential (DRP), while the simultaneous cord dorsum potential (CDP) was recorded to assess the population postsynaptic response. We found that the DRP and the CDP evoked by a primary afferent test stimulus was greatly reduced by a conditioning activation of neighbouring primary afferents. This depression had early and late components, mediated in part by GABAA and GABAB receptors, since they were reduced by bicuculline and SCH 50911 respectively. However, with the selective stimulation of C and Aδ fibres in the presence of TTX, the early and late depression of the DRP was replaced by facilitation of the GABAergic and glutamatergic components of the TTX-resistant DRP. Our findings suggest a subtle lateral excitatory interaction between primary afferents for the generation of PAD mediated by a non-spiking mechanism that may contribute to shaping of information transmitted by C and Aδ fibres in a spatially confined scale in analogy with the retina and olfactory bulb.

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

References

  • Bardoni R, Torsney C, Tong CK, Prandini M, MacDermott AB (2004) Presynaptic NMDA receptors modulate glutamate release from primary sensory neurons in rat spinal cord dorsal horn. J Neurosci 24:2774–2781

    Article  PubMed  CAS  Google Scholar 

  • Büschges A, El Manira A (1998) Sensory pathways and their modulation in the control of locomotion. Curr Opin Neurobiol 8:733–739

    Article  PubMed  Google Scholar 

  • Cook PB, McReynolds JS (1998) Lateral inhibition in the inner retina is important for spatial tuning of ganglion cells. Nat Neurosci 1:714–719

    Article  PubMed  CAS  Google Scholar 

  • Curtis DR, Lacey G. (1994) GABA-B receptor-mediated spinal inhibition. Neuroreport 5:540–542

    Article  PubMed  CAS  Google Scholar 

  • Dib-Hajj SD, Tyrrell L, Black JA, Waxman SG (1998) NaN, a novel voltage-gated Na channel, is expressed preferentially in peripheral sensory neurons and down-regulated after axotomy. Proc Natl Acad Sci USA 95:8963–8968

    Article  PubMed  CAS  Google Scholar 

  • Djouhri L, Fang X, Okuse K, Wood JN, Berry CM, Lawson SN (2003) The TTX-resistant sodium channel Nav1.8 (SNS/PN3): expression and correlation with membrane properties in rat nociceptive primary afferent neurons. J Physiol 550:739–752

    Article  PubMed  CAS  Google Scholar 

  • Duguid IC, Smart TG (2004) Retrograde activation of presynaptic NMDA receptors enhances GABA release at cerebellar interneuron-Purkinje cell synapses. Nat Neurosci 7:419–420

    Article  Google Scholar 

  • Eccles JC (1964) Presynaptic inhibition. In: The physiology of synapses. Springer, Berlin, Heidelberg, New York, pp 220–238

  • Flores-Herr N, Protti DA, Wassle H. (2001) Synaptic currents generating the inhibitory surround of ganglion cells in the mammalian retina. J Neurosci 21:4852–4863

    PubMed  CAS  Google Scholar 

  • Gobell S (1976). Dendroaxonic synapses in the substantia gelatinosa glomeruli of the spinal trigeminal nucleus of the cat. J Comp Neurol 167:165–176

    Article  PubMed  CAS  Google Scholar 

  • Gossard JP, Rossignol S (1990) Phase-dependent modulation of dorsal root potentials evoked by peripheral nerve stimulation during fictive locomotion in the cat. Brain Res 537:1–13

    Article  PubMed  CAS  Google Scholar 

  • Gossard JP, Cabelguen JM, Rossignol S (1989) Intra-axonal recordings of cutaneous primary afferents during fictive locomotion in the cat. J Neurophysiol 62:1177–1188

    PubMed  CAS  Google Scholar 

  • Johnston D, Wu SM-S (1997) Foundations of cellular neurophysiology. Extracellular field recordings, 3rd edn. The MIT Press, Cambridge, London, England, pp 23–439

    Google Scholar 

  • Kobayashi J, Ohta M, Terada Y (1993) C fiber generates a slow Na+ spike in the frog sciatic nerve. Neurosci Lett. 162:93–96

    Article  PubMed  CAS  Google Scholar 

  • Kremer E, Lev-Tov A. (1998) GABA-receptor-independent dorsal root afferents depolarization in the neonatal rat spinal cord. J Neurophysiol 79:2581–2592

    PubMed  CAS  Google Scholar 

  • Lacey G (1996) Synaptic inhibition mediated by GABAB receptors in the neonatal rat spinal cord in vitro. Brain Res 717:76–80

    Article  PubMed  CAS  Google Scholar 

  • Lloyd DPC (1952) Electrotonus in dorsal root nerves. Cold Spring Harbor Symp Quant Biol 17:203–219

    PubMed  CAS  Google Scholar 

  • Lomeli J, Quevedo J, Linares P, Rudomin P (1998) Local control of information flow in segmental and ascending collaterals of single afferents. Nature 395:600–604

    Article  PubMed  CAS  Google Scholar 

  • MacDermott AB, Role LW, Siegelbaum SA (1999) Presynaptic ionotropic receptors and the control of transmitter release. Annu Rev Neurosci 22:443–485

    Article  PubMed  CAS  Google Scholar 

  • Roska B, Nemeth E, Orzo L, Werblin FS (2000) Three levels of lateral inhibition: A space-time study of the retina of the tiger salamander. J Neurosci 20:1941–1951

    PubMed  CAS  Google Scholar 

  • Rudomin P (1999) Presynaptic selection of afferent inflow in the spinal cord. J Physiol (Paris) 93:329–347

    Article  CAS  Google Scholar 

  • Rudomin P, Schmidt RF (1999) Presynaptic inhibition in the vertebrate spinal cord revisited. Exp Brain Res 129:1–37

    Article  PubMed  CAS  Google Scholar 

  • Russo RE, Hounsgaard J (1996) Plateau-generating neurones in the dorsal horn in an in vitro preparation of the turtle spinal cord. J Physiol 493:39–54

    PubMed  CAS  Google Scholar 

  • Russo RE, Nagy F, Hounsgaard J (1998) Inhibitory control of plateau properties in dorsal horn neurons in the turtle spinal cord in vitro. J Physiol 506:795–808

    Article  PubMed  CAS  Google Scholar 

  • Russo RE, Delgado-Lezama R, Hounsgaard J (2000) Dorsal root potential produced by a TTX-insensitive micro-circuitry in the turtle spinal cord. J Physiol 528:115–122

    Article  PubMed  CAS  Google Scholar 

  • Sangameswaran L, Delgado SG, Fish LM, Koch BD, Jakeman LB, Stewart GR, Sze P, Hunter JC, Eglen RM, Herman RC (1996) Structure and function of a novel voltage-gated, tetrodotoxin-resistant sodium channel specific to sensory neurons. J Biol Chem 271:5953–5956

    Article  PubMed  CAS  Google Scholar 

  • Schoppa NE, Urban NN (2003) Dendritic processing within olfactory bulb circuits. TINS 26:501–506

    PubMed  CAS  Google Scholar 

  • Tate S, Benn S, Hick C, Trezise D, John V, Mannion RJ, Costigan M, Plumpton C, Grose D, Gladwell Z, Kendall G, Dale K, Bountra C, Woolf CJ (1998) Two sodium channels contribute to the TTX-R sodium current in primary sensory neurons. Nat Neurosci 1:653–655

    Article  PubMed  CAS  Google Scholar 

  • Todd AJ (1996). GABA and glycine in synaptic glomeruli of the rat spinal dorsal horn. Eur J Neurosci 8:2492–2498

    Article  PubMed  CAS  Google Scholar 

  • Trujillo-Cenóz O, Fernández A, Radmilovich M (1990) Fine structure and synaptic connections of the spinal dorsal root terminals in the turtle Chrysemys d’orbigny. Tissue Cell 22:811–826

    Article  Google Scholar 

  • Urban NN (2002) Lateral inhibition in the olfactory bulb and in olfaction. Physiol Behav 77:607–612

    Article  PubMed  CAS  Google Scholar 

  • Wall PD (1995) Do nerve impulses penetrate terminal arborizations? A pre-presynaptic control mechanism. Trends Neurosci 18:99–103

    Article  PubMed  CAS  Google Scholar 

  • Willis WD (1999) Dorsal root potentials and dorsal root reflexes: a double-edged sword. Exp Brain Res 124:395–421

    Article  PubMed  CAS  Google Scholar 

  • Willis WD, Coggeshall RE (2004) Sensory mechanisms of the spinal cord. Willis WD, Coggeshall RE (eds) Primary afferent neurons and the spinal dorsal horn, 3rd edn, vol 1. Kluwer and Plenum Publishers, Dordrecht and New York, pp 155–267

  • Yoshimura M, Jessell T (1990) Amino acid-mediated EPSPs at primary afferent synapses with substantia gelatinosa neurones in the rat spinal cord. J Physiol 430:315–335

    PubMed  CAS  Google Scholar 

Download references

Acknowledgment

This work was partly supported by CSIC and PEDECIBA (R.E.R.), CONACyT (R.D.L.) and the Lundbeck Foundation and The Danish MRC (J.H.).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Raúl E. Russo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Russo, R.E., Delgado-Lezama, R. & Hounsgaard, J. Heterosynaptic modulation of the dorsal root potential in the turtle spinal cord in vitro. Exp Brain Res 177, 275–284 (2007). https://doi.org/10.1007/s00221-006-0668-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-006-0668-3

Keywords

Navigation