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The Journal of Neuroscience, April 22, 2009, 29(16):5088-5099; doi:10.1523/JNEUROSCI.6175-08.2009

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Behavioral/Systems/Cognitive
Organization of Intralaminar and Translaminar Neuronal Connectivity in the Superficial Spinal Dorsal Horn

Go Kato,¹ Yasuhiko Kawasaki,² Kohei Koga,³ Daisuke Uta,³ Masafumi Kosugi,¹ Toshiharu Yasaka,⁴ Megumu Yoshimura,³ Ru-Rong Ji,² and Andrew M. Strassman¹

Department of Anesthesia, ¹Beth Israel Deaconess Medical Center and ²Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts 02215, ³Department of Integrative Physiology, Kyushu University, School of Medicine, Fukuoka 812-8582, Japan, and ⁴Spinal Cord Group, Institute of Biomedical and Life Sciences, University of Glasgow, Glasgow G12 8QQ, United Kingdom

Correspondence should be addressed to Go Kato, Department of Orthopaedic Surgery, Graduate School of Medical Sciences, Kyushu University, 3-1-1 Maidashi Higashi-ku, Fukuoka 812-8582, Japan. Email: gkato{at}ortho.med.kyushu-u.ac.jp

The spinal dorsal horn exhibits a high degree of intrinsic connectivity that is critical to its role in the processing of nociceptive information. To examine the spatial organization of this intrinsic connectivity, we used laser-scanning photostimulation in parasagittal and transverse slices of lumbar spinal cord to stimulate presynaptic neurons by glutamate uncaging, and mapped the location of sites that provide excitatory and inhibitory synaptic input to neurons of the superficial laminae. Excitatory interneuronal connectivity within lamina II exhibited a pronounced sagittal orientation, in keeping with the somatotopic organization present in the pattern of primary afferent projections. Excitatory inputs to all classes of lamina II neurons arose from a wider rostrocaudal area than inhibitory inputs, whereas both excitatory and inhibitory input zones were restricted mediolaterally. Lamina I–II neurons exhibited cell type-specific patterns in the laminar distribution of their excitatory inputs that were related to their dorsoventral dendritic expanse. All cell types received excitatory input predominantly from positions ventral to that of their soma, but in lamina I neurons and lamina II vertical cells this ventral displacement of the excitatory input zone was greater than in the other cell types, resulting in a more pronounced translaminar input pattern. A previously unknown excitatory input to the superficial dorsal horn from lamina III–IV was identified in a subset of the vertical cell population. These results reveal a specific three-dimensional organization in the local patterns of excitatory and inhibitory connectivity that has implications for the processing of information related to both somatotopy and sensory modality.

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Received Dec. 29, 2008; revised Feb. 12, 2009; accepted Feb. 19, 2009.

Correspondence should be addressed to Go Kato, Department of Orthopaedic Surgery, Graduate School of Medical Sciences, Kyushu University, 3-1-1 Maidashi Higashi-ku, Fukuoka 812-8582, Japan. Email: gkato{at}ortho.med.kyushu-u.ac.jp

This article has been cited by other articles:

				H. Wang and M. J. Zylka Mrgprd-Expressing Polymodal Nociceptive Neurons Innervate Most Known Classes of Substantia Gelatinosa Neurons J. Neurosci., October 21, 2009; 29(42): 13202 - 13209. [Abstract] [Full Text] [PDF]

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