Abstract
Spinal lamina I is a key area for relaying and integrating information from nociceptive primary afferents with various other sources of inputs. Although lamina I projection neurons have been intensively studied, much less attention has been given to local-circuit neurons (LCNs), which form the majority of the lamina I neuronal population. In this work the infrared light-emitting diode oblique illumination technique was used to visualize and label LCNs, allowing reconstruction and analysis of their dendritic and extensive axonal trees. We show that the majority of lamina I neurons with locally branching axons fall into the multipolar (with ventrally protruding dendrites) and flattened (dendrites limited to lamina I) somatodendritic categories. Analysis of their axons revealed that the initial myelinated part gives rise to several unmyelinated small-diameter branches that have a high number of densely packed, large varicosities and an extensive rostrocaudal (two or three segments), mediolateral, and dorsoventral (reaching laminae III–IV) distribution. The extent of the axon and the occasional presence of long, solitary branches suggest that LCNs may also form short and long propriospinal connections. We also found that the distribution of axon varicosities and terminal field locations show substantial heterogeneity and that a substantial portion of LCNs is inhibitory. Our observations indicate that LCNs of lamina I form intersegmental as well as interlaminar connections and may govern large numbers of neurons, providing anatomical substrate for rostrocaudal “processing units” in the dorsal horn. J. Comp. Neurol. 521:2719–2741, 2013.
Highlights
Lamina I of the spinal cord is a key area for sensory information processing and pain transmission (Cervero and Tattersall, 1987; Christensen and Perl, 1970)
We found that the greatest extent of the axonal tree of local-circuit neurons (LCNs) is in the rostrocaudal direction, so we chose cells sectioned in the sagittal plane for reconstruction
With the exception of a few neurons, LCNs presented a tonic firing pattern, and, in 46% of the cases, neurons were rhythmically firing action potentials that persisted in the presence of a blocker of fast glutamatergic transmission, CNQX (10 lM; Sigma; see Li and Baccei, 2011)
Summary
Lamina I of the spinal cord is a key area for sensory information processing and pain transmission (Cervero and Tattersall, 1987; Christensen and Perl, 1970) It is a major target zone for the fine-caliber myelinated Adelta- and unmyelinated C-primary afferent fibers (Willis and Coggeshall, 1991) as well as for the descending systems that control its activity (Millan, 2002). The use of the infrared light-emitting diode (IR-LED) oblique illumination technique (Safronov et al, 2007; Szucs et al, 2009) in intact spinal cord preparations, in vitro, has proved to be a way to solve this problem This approach permits recording, labeling, and reconstruction of the complete dendritic and axonal trees of lamina I neurons, revealing distinct local axon-collateral patterns for projection neurons belonging to the anterolateral tract (ALT; Szucs et al, 2010). We sought to create the first detailed 3-D reconstructions of lamina I neurons that, in addition to being a valuable tool for computational neuroscience, would allow novel, spatially dependent morphometric measurements
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