Excitatory interneurons dominate sensory processing in the spinal substantia gelatinosa of rat

Journal of Physiology

Volumn 581, Issue 1, 2007, Pages 241-254

  Santos, Sónia F A ^a,b   Rebelo, Sandra ^b   Derkach, Victor A ^c   Safronov, Boris V ^a,b  

^a UNIVERSITY OF PORTO   (Portugal)

^b University of Porto   (Portugal)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EVOKED SOMATOSENSORY RESPONSE; EXCITATORY POSTSYNAPTIC POTENTIAL; INHIBITORY POSTSYNAPTIC POTENTIAL; INTERNEURON; LAMINA PROPRIA; MONOSYNAPTIC PATHWAY; NERVE CELL NETWORK; NERVE CELL STIMULATION; NOCICEPTION; NONHUMAN; PATCH CLAMP; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; RAT; SPINAL CORD NERVE CELL; SUBSTANTIA GELATINOSA; WHOLE CELL; CELL ATTACHED PATCH CLAMP; FIRING RATE; GLUTAMATERGIC SYNAPSE; POSTSYNAPTIC POTENTIAL; SENSORIMOTOR FUNCTION; SIGNAL TRANSDUCTION; SYNAPTIC INHIBITION; SYNAPTIC TRANSMISSION; WHOLE CELL PATCH CLAMP;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ACTION POTENTIALS; ANIMALS; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; GABA ANTAGONISTS; GLUTAMATES; GLYCINE AGENTS; INTERNEURONS; NEURONS, AFFERENT; PATCH-CLAMP TECHNIQUES; PICROTOXIN; PRESYNAPTIC TERMINALS; RATS; STRYCHNINE; SUBSTANTIA GELATINOSA;

EID: 34248211748     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2006.126912     Document Type: Article

References (51)

1. Bentley GN & Gent JP (1994). Electrophysiological properties of substantia gelatinosa neurones in a novel adult spinal slice preparation. J Neurosci Methods 53, 157-162.
2. Brown AG (1981). Organization in the Spinal Cord. Springer-Verlag, Berlin, Heidelberg.
3. Burstein R, Cliffer KD & Giesler GJ Jr (1987). Direct somatosensory projections from the spinal cord to the hypothalamus and telencephalon. J Neurosci 7, 4159-4164.
4. Cervero F (1987). Dorsal horn neurones and their sensory inputs. In Spinal Afferent Processing, ed. Yaksh TL, pp. 197-216. Plenum Press, New York.
5. Chéry N & De Koninck Y (1999). Junctional versus extrajunctional glycine and GABA A receptor-mediated IPSCs in identified lamina I neurons of the adult rat spinal cord. J Neurosci 19, 7342-7355.
6. Cossart R, Epsztein J, Tyzio R, Becq H, Hirsch J, Ben-Ari Y & Crepel V (2002). Quantal release of glutamate generates pure kainate and mixed AMPA/kainate EPSCs in hippocampal neurons. Neuron 35, 147-159.
7. Duggan AW, Hall JG & Headley PM (1977). Suppression of transmission of nociceptive impulses by morphine: Selective effects of morphine administered in the region of the substantia gelatinosa. Br J Pharmacol 61, 65-76.
8. Engelman HS & MacDermott AB (2004). Presynaptic ionotropic receptors and control of transmitter release. Nat Rev Neurosci 5, 135-145.
9. Frerking M, Malenka RC & Nicoll RA (1998). Synaptic activation of kainate receptors on hippocampal interneurons. Nat Neurosci 1, 479-486.
10. Graham BA, Brichta AM & Callister RJ (2004). In vivo responses of mouse superficial dorsal horn neurones to both current injection and peripheral cutaneous stimulation. J Physiol 561, 749-763.
11. Grudt TJ & Perl ER (2002). Correlations between neuronal morphology and electrophysiological features in the rodent superficial dorsal horn. J Physiol 540, 189-207.
12. Hantman AW, van den Pol AN & Perl ER (2004). Morphological and physiological features of a set of spinal substantia gelatinosa neurons defined by green fluorescent protein expression. J Neurosci 24, 836-842.
13. Hartmann B, Ahmadi S, Heppenstall PA, Lewin GR, Schott C, Borchardt T, Seeburg PH, Zeilhofer HU, Sprengel R & Kuner R (2004). The AMPA receptor subunits GluR-A and GluR-B reciprocally modulate spinal synaptic plasticity and inflammatory pain. Neuron 44, 637-650.
14. Horn R & Marty A (1988). Muscarinic activation of ionic currents measured by a new whole-cell recording method. J Gen Physiol 92, 145-159.
15. Hu H-J & Gereau RW (2003). ERK integrates PKA and PKC signaling in superficial dorsal horn neurons. II. Modulation of neuronal excitability. J Neurophysiol 90, 1680-1688.
16. + currents. J Neurophysiol 90, 1671-1679.
17. Ji RR, Kohno T, Moore KA & Woolf CJ (2003). Central sensitization and LTP: Do pain and memory share similar mechanisms?Trends Neurosci 26, 696-705.
18. Johnston SM & Duggan AW (1981). Evidence that opiate receptors of the substantia gelatinosa contribute to the depression, by intravenous morphine, of the spinal transmission of impulses in unmyelinated afferents. Brain Res 207, 223-228.
19. Kemp T, Spike RC, Watt C & Todd AJ (1996). The μ-opioid receptor (MOR1) is mainly restricted to neurons that do not contain GABA or glycine in the superficial dorsal horn of the rat spinal cord. Neurosci 75, 1231-1238.
20. LaMotte C (1977). Distribution of the tract of lissauer and the dorsal root fibers in the primate spinal cord. J Comp Neurol 172, 529-561.
21. Landry M, Bouali-Benazzouz R, El Mestikawy S, Ravassard P & Nagy F (2004). Expression of vesicular glutamate transporters in rat lumbar spinal cord, with a note on dorsal root ganglia. J Comp Neurol 468, 380-394.
22. Lee CJ, Labrakakis C, Joseph DJ & Macdermott AB (2004). Functional similarities and differences of AMPA and kainate receptors expressed by cultured rat sensory neurons. Neuroscience 129, 35-48.
23. Light AR & Perl ER (1977). Differential termination of large-diameter and small-diameter primary afferent fibers in the spinal dorsal gray matter as indicated by labelling with horseradish peroxidase. Neurosci Lett 6, 59-63.
24. Lima D (1996). Endogenous pain modulatory system in the light of the gate control theory. Pain Forum 5, 31-39.
25. Lima D (1998). Anatomical basis for the dynamic processing of nociceptive input. Eur J Pain 2, 195-202.
26. Lima D & Coimbra A (1988). The spinothalamic system of the rat: structural types of retrogradely labelled neurons in the marginal zone (lamina I). Neurosci 27, 215-230.
27. Lisman J & Spruston N (2005). Postsynaptic depolarization requirements for LTP and LTD: A critique of spike timing-dependent plasticity. Nat Neurosci 8, 839-841.
28. Lopez-Garcia JA & King AE (1994). Membrane properties of physiologically classified rat dorsal horn neurons in vitro: Correlation with cutaneous sensory afferent input. Eur J Neurosci 6, 998-1007.
29. Lu Y & Perl ER (2003). A specific inhibitory pathway between substantia gelatinosa neurons receiving direct C-fiber input. J Neurosci 23, 8752-8758.
30. Lu Y & Perl ER (2005). Modular organization of excitatory circuits between neurons of the spinal superficial dorsal horn (laminae I and II). J Neurosci 25, 3900-3907.
31. Malenka RC & Bear MF (2004). LTP and LTD: An embarrassment of riches. Neuron 44, 5-21.
32. Malenka RC & Nicoll RA (1999). Long-term potentiation -a decade of progress?Science 285, 1870-1874.
33. Melnick IV, Santos SFA & Safronov BV (2004 b). Mechanism of spike frequency adaptation in substantia gelatinosa neurones of rat. J Physiol 559, 383-395.
34. Melnick IV, Santos SFA, Szokol K, Szucs P & Safronov BV (2004 a). Ionic basics of tonic firing in spinal substantia gelatinosa neurons of rat. J Neurophysiol 91, 646-655.
35. Petralia RS, Wang YX, Mayat E & Wenthold RJ (1997). Glutamate receptor subunit 2-selective antibody shows a differential distribution of calcium-impermeable AMPA receptors among populations of neurons. J Comp Neurol 385, 456-476.
36. Prescott SA & De Koninck Y (2002). Four cell types with distinctive membrane properties and morphologies in lamina I of the spinal dorsal horn of the adult rat. J Physiol 539, 817-836.
37. Rae J, Cooper K, Gates P & Watsky M (1991). Low access resistance perforated patch recordings using amphotericin B. J Neurosci Methods 37, 15-26.
38. Rethelyi M (1977). Preterminal and terminal axon arborizations in the substantia gelatinosa of cat's spinal cord. J Comp Neurol 172, 511-521.
39. Ruscheweyh R & Sandkuhler J (2002). Lamina-specific membrane and discharge properties of rat spinal dorsal horn neurones in vitro. J Physiol 541, 231-244.
40. Salter MW (2005). Cellular signalling pathways of spinal pain neuroplasticity as targets for analgesic development. Curr Top Med Chem 5, 557-567.
41. Santos SFA, Melnick IV & Safronov BV (2004). Selective inhibition of tonic-firing neurons in substantia gelatinosa by μ-opioid agonist. Anesthesiology 101, 1177-1183.
42. Sugiura Y, Lee CL & Perl ER (1986). Central projections of identified, unmyelinated (C) afferent fibers innervating mammalian skin. Science 234, 358-361.
43. Tachibana M, Wenthold RJ, Morioka H & Petralia RS (1994). Light and electron microscopic immunocytochemical localization of AMPA-selective glutamate receptors in the rat spinal cord. J Comp Neurol 344, 431-454.
44. Thomson AM, West DC & Headley PM (1989). Membrane characteristics and synaptic responsiveness of superficial dorsal horn neurons in a slice preparation of adult rat spinal cord. Eur J Neurosci 1, 479-488.
45. Todd AJ & Sullivan AC (1990). Light microscope study of the coexistence of GABA-like and glycine-like immunoreactivities in the spinal cord of the rat. J Comp Neurol 296, 496-505.
46. Tolle TR, Berthele A, Zieglgansberger W, Seeburg PH & Wisden W (1995). Flip and Flop variants of AMPA receptors in the rat lumbar spinal cord. Eur J Neurosci 7, 1414-1419.
47. Turrigiano GG & Nelson SB (2004). Homeostatic plasticity in the developing nervous system. Nat Rev Neurosci 5, 97-107.
48. Willis WD & Coggeshall RE (1991). Sensory Mechanisms of the Spinal Cord. Plenum Press, New York.
49. Woolf CJ & Salter MW (2000). Neuronal plasticity: Increasing the gain in pain. Science 288, 1765-1769.
50. Yoshimura M & Jessell TM (1989). Membrane properties of rat substantia gelatinosa neurons in vitro. J Neurophysiol 62, 109-118.
51. Youn DH & Randic M (2004). Modulation of excitatory synaptic transmission in the spinal substantia gelatinosa of mice deficient in the kainate receptor GluR5 and/or GluR6 subunit. J Physiol 555, 683-698.