Abstract

Between 25–40% of neurons in laminae I–III are GABAergic, and some of these express neuropeptide Y (NPY). We previously reported that NPY-immunoreactive axons form numerous synapses on lamina III projection neurons that possess the neurokinin 1 receptor (NK1r). The aims of this study were to determine the proportion of neurons and GABAergic boutons in this region that contain NPY, and to look for evidence that they selectively innervate different neuronal populations. We found that 4–6% of neurons in laminae I–III were NPY-immunoreactive and based on the proportions of neurons that are GABAergic, we estimate that NPY is expressed by 18% of inhibitory interneurons in laminae I–II and 9% of those in lamina III. GABAergic boutons were identified by the presence of the vesicular GABA transporter (VGAT) and NPY was found in 13–15% of VGAT-immunoreactive boutons in laminae I–II, and 5% of those in lamina III. For both the lamina III NK1r-immunoreactive projection neurons and protein kinase Cγ (PKCγ)-immunoreactive interneurons in lamina II, we found that around one-third of the VGAT boutons that contacted them were NPY-immunoreactive. However, based on differences in the sizes of these boutons and the strength of their NPY-immunoreactivity, we conclude that these originate from different populations of interneurons. Only 6% of VGAT boutons presynaptic to large lamina I projection neurons that lacked NK1rs contained NPY. These results show that NPY-containing neurons make up a considerable proportion of the inhibitory interneurons in laminae I–III, and that their axons preferentially target certain classes of dorsal horn neuron. J. Comp. Neurol. 519:1007–1023, 2011. © 2010 Wiley-Liss, Inc.

Highlights

  • F vesicular gamma-aminobutyric acid (GABA) transporter (VGAT)-immunoreactive boutons in laminae I–II, and 5% of those in lamina III

  • It has been shown that neuropeptide Y (NPY), parvalbumin, and neuronal form of nitric oxide synthase (nNOS) are not colocalized in laminae I–III (Laing et al, 1994), which suggests that these compounds may define distinctive populations of inhibitory interneurons

  • Bundles of immunoreactive axons were often seen passing through the superficial laminae and penetrating into the deep dorsal horn, and many of these are likely to correspond to the clusters that have been shown to innervate the dorsal dendrites of lamina III NK1rexpressing projection neurons (Polgar et al, 1999b)

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Summary

Introduction

F VGAT-immunoreactive boutons in laminae I–II, and 5% of those in lamina III. For both the lamina III NK1r-immunoreactive projection neurons and protein kinase Cc (PKCc)-immunoreactive interneurons in lamina II, we found that around one-third of the VGAT boutons that contacted them were NPY-immunoreactive. 6% of VGAT boutons presynaptic to large lamina I projection neurons that lacked NK1rs contained NPY These results show that NPY-containing neurons make up a considerable proportion of the inhibitory interneurons in laminae I–III, and that their axons preferentially target certain classes of dorsal horn neuron. Since the majority of NPY-containing boutons in the superficial dorsal horn are not associated with the lamina III NK1r projection cells, we have estimated the contribution that they make to the GABAergic innervation of two other types of neuron: the large gephyrin-coated projection cells in lamina I and interneurons in the inner part of lamina II (IIi) that express protein kinase Cc (PKCc; Mori et al, 1990; Malmberg et al, 1997; Polgar et al, 1999a)

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