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The Journal of Neuroscience, March 15, 1999, 19(6):2081-2089

The Distribution of Neurons Expressing Calcium-Permeable AMPA Receptors in the Superficial Laminae of the Spinal Cord Dorsal Horn

Holly S. Engelman, Thomas B. Allen, and Amy B. MacDermott

Department of Physiology and Cellular Biophysics and the Center for Neurobiology and Behavior, Columbia University, New York, New York 10032

The superficial dorsal horn is a major site of termination of nociceptive primary afferents. Fast excitatory synaptic transmission in this region is mediated mainly by release of glutamate onto postsynaptic AMPA and NMDA receptors. NMDA receptors are known to be Ca²⁺-permeable and to provide synaptically localized Ca²⁺ signals that mediate short-term and long-term changes in synaptic strength. Less well known is a subpopulation of AMPA receptors that is Ca²⁺-permeable and has been shown to be synaptically localized on dorsal horn neurons in culture (Gu et al., 1996) and expressed by dorsal horn neurons in situ (Nagy et al., 1994; Engelman et al., 1997). We used kainate-induced cobalt uptake as a functional marker of neurons expressing Ca²⁺-permeable AMPA receptors and combined this with markers of nociceptive primary afferents in the postnatal rat dorsal horn. We have shown that cobalt-positive neurons are located in lamina I and outer lamina II, a region strongly innervated by nociceptors. These cobalt-positive neurons colocalize with afferents labeled by LD2, and with the most dorsal region of capsaicin-sensitive and IB4- and LA4-positive afferents. In contrast, inner lamina II has a sparser distribution of cobalt-positive neurons. Some lamina I neurons expressing the NK1 receptor, the receptor for substance P, are also cobalt positive. These neurons are likely to be projection neurons in the nociceptive pathway. On the basis of all of these observations, we propose that Ca²⁺-permeable AMPA receptors are localized to mediate transmission of nociceptive information.

Key words: dorsal horn; calcium-permeable AMPA receptors; glutamate; cobalt; spinal cord; NK1 receptor; dorsal root ganglia; nociception

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Copyright © 1999 Society for Neuroscience  0270-6474/99/1962081-09$05.00/0

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