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The Journal of Neuroscience, April 13, 2005, 25(15):3900-3907; doi:10.1523/JNEUROSCI.0102-05.2005

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Behavioral/Systems/Cognitive
Modular Organization of Excitatory Circuits between Neurons of the Spinal Superficial Dorsal Horn (Laminae I and II)

Yan Lu and Edward R. Perl

Department of Cell and Molecular Physiology, University of North Carolina, Chapel Hill, Chapel Hill, North Carolina 27599

Neural circuitry of the spinal superficial dorsal horn (SDH) (laminae I and II) and its relationship to pain and other somatosensory phenomena remain poorly understood. To gain information on this issue, synaptic connections between identified SDH neurons were studied in rat spinal cord slices by simultaneous whole-cell recordings from pairs of cells. Both excitatory and inhibitory connections were noted. This report focuses on the observed excitatory linkages. Synaptic excitatory connections between SDH neurons proved highly selective and consistently were unidirectional. Two patterns repeatedly appeared (for neuron classification, see Materials and Methods) (Grudt and Perl, 2002). Lamina II central neurons, with dorsal root (DR) C-fiber input, monosynaptically excited lamina II vertical neurons with DR A{delta} input. Lamina II outer vertical neurons with DR A{delta} input monosynaptically excited lamina I neurons. Some of the postsynaptic lamina I cells were shown to project rostrally. In contrast to the usual case for connected neurons, in unconnected pairs, primary afferent input to the same type of neuron proved closely similar. Together, these observations indicate that the neural circuitry in the SDH, including its substantia gelatinosa (lamina II), has an explicit organization in which particular combinations of neurons comprise modules arranged to modify and transmit sensory information arriving from A{delta} and C primary afferent fibers.

Key words: substantia gelatinosa; marginal zone; connected neurons; neural circuits; pain; dorsal horn


Received Jan 10, 2005; revised March 4, 2005; accepted March 5, 2005.




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