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J Physiol Volume 581, Number 2, 603-618, June 1, 2007 DOI: 10.1113/jphysiol.2006.123919
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NEUROSCIENCE

Cell-type-specific excitatory and inhibitory circuits involving primary afferents in the substantia gelatinosa of the rat spinal dorsal horn in vitro

Toshiharu Yasaka1, Go Kato1, Hidemasa Furue1, Md Harunor Rashid1, Motoki Sonohata1, Akihiro Tamae1, Yuzo Murata2, Sadahiko Masuko2 and Megumu Yoshimura1

1 Department of Integrative Physiology, Graduate School of Medical Sciences, Kyushu University, Fukuoka 812-8582, Japan
2 Division of Histology and Neuroanatomy, Department of Anatomy and Physiology, Saga Medical School, Nabeshima 5-1-1, Saga 849-8501, Japan

The substantia gelatinosa (SG) of the spinal dorsal horn shows significant morphological heterogeneity and receives primary afferent input predominantly from A{delta}- and C-fibres. Despite numerous anatomical and physiological studies, correlation between morphology and functional connectivity, particularly in terms of inhibitory inputs, remains elusive. To compare excitatory and inhibitory synaptic inputs on individual SG neurones with morphology, we performed whole-cell recordings with Neurobiotin-filled-pipettes in horizontal slices from adult rat spinal cord with attached dorsal roots. Based on dendritic arborization patterns, four major cell types were confirmed: islet, central, radial and vertical cells. Dorsal root stimulation revealed that each class was associated with characteristic synaptic inputs. Islet and central cells had monosynaptic excitatory inputs exclusively from C-afferents. Islet cells received primary-afferent-evoked inhibitory inputs only from A{delta}-fibres, while those of central cells were mediated by both A{delta}- and C-fibres. In contrast, radial and vertical cells had monosynaptic excitatory inputs from both A{delta}- and C-fibres and inhibitory inputs mediated by both fibre types. We further characterized the neurochemical nature of these inhibitory synaptic inputs. The majority of islet, central and vertical cells exhibited GABAergic inhibitory inputs, while almost all radial cells also possessed glycinergic inputs. The present study demonstrates that SG neurones have distinct patterns of excitatory and inhibitory inputs that are related to their morphology. The neurotransmitters responsible for inhibitory inputs to individual SG neurones are also characteristic for different morphological classes. These results make it possible to identify primary afferent circuits associated with particular types of SG neurone.

(Received 19 December 2006; accepted after revision 5 March 2007; first published online 8 March 2007)
Corresponding author T. Yasaka: Spinal Cord Group, West Medical Building, University of Glasgow, University Avenue, Glasgow G12 8QQ, UK. Email: t.yasaka{at}bio.gla.ac.uk




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