Modular organization of excitatory circuits between neurons of the spinal superficial dorsal horn (laminae I and II)

Journal of Neuroscience

Volumn 25, Issue 15, 2005, Pages 3900-3907

  Lu, Yan ^a   Perl, Edward R ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

Connected neurons; Dorsal horn; Marginal zone; Neural circuits; Pain; Substantia gelatinosa

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DELTA NERVE FIBER; EXCITATORY JUNCTION POTENTIAL; INHIBITORY POSTSYNAPTIC POTENTIAL; MONOSYNAPTIC PATHWAY; NERVE FIBER C; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; RAT; SPINAL CORD; SPINAL CORD DORSAL HORN; SPINAL CORD POTENTIAL; SPINAL SUPERFICIAL DORSAL HORN LAMINA I; SUBSTANTIA GELATINOSA; SYNAPTIC INHIBITION; SYNAPTIC TRANSMISSION; TISSUE SLICE;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ACTION POTENTIALS; ANIMALS; ELECTRIC STIMULATION; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; LYSINE; MODELS, NEUROLOGICAL; NERVE NET; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; REACTION TIME; STILBAMIDINES; SUBSTANCE P; SUBSTANTIA GELATINOSA; SYNAPTIC TRANSMISSION; TETRODOTOXIN;

EID: 17644396711     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0102-05.2005     Document Type: Article

References (37)

1. Bennett GJ, Abdelmoumene M, Hayashi H, Dubner R (1980) Physiology and morphology of substantia gelatinosa neurons intracellularly stained with horseradish peroxidase. J Comp Neurol 194:809-827.
2. Craig AD (1994) Spinal and supraspinal processing of specific pain and temperature. In: Touch, temperature, and pain in health and disease: mechanisms and assessments (Boivie J, Hansson P, Lindblom U, eds), pp 421-437. Seattle: International Association for the Study of Pain.
3. Craig AD, Kniffki KD (1985) The multiple representation of nociception in the spinothalamic projection of lamina I cells in the cat. In: Development, organization, and processing in somatosensory pathways (Rowe M, Willis W, eds), pp 347-353. New York: Alan R. Liss.
4. Earle KM (1952) The tract of Lissauer and its possible relation to the pain pathway. J Comp Neurol 96:93-109.
5. Gobel S (1978) Golgi studies of the neurons in layer II of the dorsal horn of the medulla (trigeminal nucleus caudalis). J Comp Neurol 180:395-414.
6. Gobel S, Falls WM, Bennett GJ, Abdelmoumene M, Hayashi H, Humphrey E (1980) An EM analysis of the synaptic connections of horseradish peroxidase-filled stalked cells and islet cells in the substantia gelatinosa of adult cat spinal cord. J Comp Neurol 194:781-807.
7. Grudt TJ, Perl ER (2002) Correlations between neuronal morphology and electrophysiological features in the rodent superficial dorsal horn. J Physiol (Lond) 540:189-207.
8. Han Z-S, Zhang E-T, Craig AD (1998) Nociceptive and thermoreceptive lamina 1 neurons are anatomically distinct. Nat Neurosci 1:218-225.
9. Honoré T, Davies SN, Drejer J, Fletcher EJ, Jacobsen P, Lodge D, Nielsen FE (1988) Quinoxalinediones: potent competitive non-NMDA glutamate receptor antagonists. Science 241:701-703.
10. Ikeda H, Heinke B, Ruscheweyh R, Sandkuhler J (2003) Synaptic plasticity in spinal lamina I projection neurons that mediate hyperalgesia. Science 299:1237-1240.
11. Kuru M (1949) The sensory paths in the spinal cord and brain stem of man. Resume, pp 3-35. Tokyo: Sogensya.
12. Lawson SN, Crepps B, Perl ER (1997) Relationship of substance P to afferent characteristics of dorsal root ganglion neurones in guinea-pig. J Physiol (Lond) 505:177-191.
13. Leise EM (1990) Modular construction of nervous systems: a basic principal of design for invertebrates and vertebrates. Brain Res Brain Res Rev 15:1-23.
14. Li J, Perl ER (1995) ATP modulation of synaptic transmission in the spinal substantia gelatinosa. J Neurosci 15:3357-3365.
15. Light AR (1992) The organization of nociceptive neurons in the spinal grey matter. In: The initial processing of pain and its descending control: spinal and trigeminal systems, Chap 6, pp 109-150. Basel: Karger.
16. Light AR, Perl ER (1979a) Reexamination of the dorsal root projection to the spinal dorsal horn including observations on the differential termination of coarse and fine fibers. J Comp Neurol 186:117-132.
17. Light AR, Perl ER (1979b) Spinal termination of functionally identified primary afferent neurons with slowly conducting myelinated fibers. J Comp Neurol 186:133-150.
18. Light AR, Willcockson HH (1999) Spinal laminae I-II neurons in rat recorded in vivo in whole cell, tight seal configuration: properties and opioid responses. J Neurophysiol 82:3316-3326.
19. Light AR, Trevino DL, Perl ER (1979) Morphological features of functionally defined neurons in the marginal zone and substantia gelatinosa of the spinal dorsal horn. J Comp Neurol 186:151-171.
20. Lorente de No R (1938) Cerebral cortex: architecture, intracortical connections, motor projections. In: Physiology of the nervous system (Fulton JF, ed), pp 291-339. Oxford: Oxford UP.
21. Lu Y, Perl ER (2003) A specific inhibitory pathway between substantia gelatinosa neurons receiving direct C-fiber input. J Neurosci 23:8752-8758.
22. Lynn B, Carpenter SE (1982) Primary afferent units from the hairy skin of the rat hind limb. Brain Res 238:23-43.
23. Mountcastle VB (1957) Modality and topographic properties of single neurons of cat's somatic sensory cortex. J Neurophysiol 20:408-434.
24. Pearson AA (1952) Role of gelatinous substance of spinal cord in conduction of pain. Arch Neurol Psychiatry 68:515-529.
25. Perl ER (1984) Pain and nociception. In: Handbook of physiology. The nervous system, Vol 3 (Darian-Smith I, ed), pp 915-975. Bethesda, MD: American Physiological Society.
26. Perl ER (1992) Function of dorsal root ganglion neurons: an overview. In: Sensory neurons: diversity, development and plasticity (Scott S, ed), pp 3-23. New York: Oxford.
27. Ramon y Cajal S (1999) Texture of the nervous system of man and the vertebrates, Vol 1 (Pasik P, Pasik T, translators and eds), pp 287-291, 355-366. Wien, Austria: Springer.
28. Ranson SW (1914) The tract of Lissauer and the substantia gelatinosa rolandi. Am J Anat 16:97-126.
29. Réthelyi M, Szentágothai J (1969) The large synaptic complexes of the substantia gelatinosa. Exp Brain Res 7:258-274.
30. Rexed B (1952) The cytoarchitectonic organization of the spinal cord in the cat. J Comp Neurol 96:415-495.
31. Ruscheweyh R, Ikeda H, Heinke B, Sandkuhler J (2004) Distinctive membrane and discharge properties of rat spinal lamina I projection neurones in vitro. J Physiol (Lond) 555:527-543.
32. Sugiura Y, Lee CL, Perl ER (1986) Central projections of identified, unmyelinated afferent fibers innervating mammalian skin. Science 234:358-361.
33. Szentágothai J (1964) Neuronal and synaptic arrangement in the substantia gelatinosa rolandi. J Comp Neurol 122:219-239.
34. Todd AJ, Puskar Z, Spike RC, Hughes C, Watt C, Forrest L (2002) Projection neurons in lamina I of rat spinal cord with the neurokinin 1 receptor are selectively innervated by substance p-containing afferents and respond to noxious stimulation. J Neurosci 22:4103-4113.
35. Todd AJ, Spike RC, Young S, Puskar Z (2005) Fos induction in lamina I projection neurons in response to noxious thermal stimuli. Neuroscience 131:209-217.
36. Woodbury CJ, Ritter AM, Koerber HR (2000) On the problem of lamination in the superficial dorsal horn of mammals: a reappraisal of the substantia gelatinosa in postnatal life. J Comp Neurol 417:88-102.
37. Yoshimura M, Jessell TM (1989) Primary afferent-evoked synaptic responses and slow potential generation in rat substantia gelatinosa neurons in vitro. J Neurophysiol 62:96-108.