Steady-State Levels of Monoamines in the Rat Lumbar Spinal Cord: Spatial Mapping and the Effect of Acute Spinal Cord Injury
Journal of Neurophysiology
Noga, Brian R., Alberto Pinzon, Riza P. Mesigil, and Ian D. Hentall. Steady-state levels of monoamines in the rat lumbar spinal cord: spatial mapping and the effect of acute spinal cord injury. . Monoamines in the spinal cord are important in the regulation of locomotor rhythms, nociception, and motor reflexes. To gain further insight into the control of these functions, the steady-state extracellular distribution of monoamines was mapped in the anesthetized rat's lumbar spinal cord. The effect
... of acute spinal cord lesions at sites selected for high resting levels was determined over ϳ1 h to estimate contributions to resting levels from tonic descending activity and to delineate chemical changes that may influence the degree of pathology and recovery after spinal injury. Measurements employed fast cyclic voltammetry with carbon fiber microelectrodes to give high spatial resolution. Monoamine oxidation currents, sampled at equal vertical spacings within each segment, were displayed as contours over the boundaries delineated by histologically reconstructed electrode tracks. Monoamine oxidation currents were found in well defined foci, often confined within a single lamina. Larger currents were typically found in the dorsal or ventral horns and in the lateral aspect of the intermediate zone. Cooling of the low-thoracic spinal cord led to a decrease in the oxidation current (to 71-85% of control) in dorsal and ventral horns. Subsequent lowthoracic transection produced a transient increase in signal in some animals followed by a longer lasting decrease to levels similar to or below that with cooling (to 17-86% of control values). We conclude that descending fibers tonically release high amounts of monoamines in localized regions of the dorsal and ventral horn of the lumbar spinal cord at rest. Lower amounts of monoamines were detected in medial intermediate zone areas, where strong release may be needed for descending activation of locomotor rhythms. . signaling inhibits hyperalgesia induced by spinal cord injury. Brain Res 963: 312-320, 2003. Hosoya Y, Okado N, Sugiura Y, and Kohno K. Coincidence of "ladder-like patterns" in distributions of monoaminergic terminals and sympathetic preganglionic neurons in the rat spinal cord. Exp Brain Res 86: 224 -228, 1991. Huang A, Noga BR, Carr PA, Fedirchuk B, and Jordan LM. Spinal cholinergic neurons activated during locomotion: immunohistochemical localization and electrophysiological characterization. J Neurophysiol 83: 3537-3547, 2000. Johnson DMG, Riesgo MI, Pinzon A, and Noga BR. Monoaminergic innervation of locomotor activated cells in cat spinal cord. Soc Neurosci Abstr 28: 65.15, 2002. Jones SL and Light AR. Serotonergic medullary raphespinal projection to the lumbar spinal cord in the rat: a retrograde immunohistochemical study. J Comp Neurol 322: 599 -610, 1992. Keita H, Henzel-Rouelle D, Dupont H, Desmonts JM, and Mantz J. Halothane and isoflurane increase spontaneous but reduce the N-methyl-Daspartate-evoked dopamine release in rat striatal slices: evidence for direct presynaptic effects. Anesthesiology 91: 1788 -1797, 1999. Kiehn O, Hultborn H, and Conway BA. Spinal locomotor activity in acutely spinalized cats induced by intrathecal application of nonadrenaline. Neurosci Lett 143: 243-246, 1992. Kjaerulff O and Kiehn O. Distribution of networks generating and coordinating locomotor activity in the neonatal rat spinal cord in vitro: a lesion study. J Neurosci 16: 5777-5794, 1996. Ko ML, King MA, Gordon TL, and Crisp T. The effects of aging on spinal neurochemistry in the rat. Brain Res Bull 42: 95-98, 1997. Kopin IJ. Catecholamine metabolism: basic aspects and clinical significance. Pharmacol Rev 37: 333-364, 1985. Li HS, Monhemius R, Simpson BA, and Roberts MHT. Supraspinal inhibition of nociceptive dorsal horn neurons in the anaesthetized rat: tonic or dynamic? J Physiol 506: 459 -469, 1998. Lisi TL, Westlund KN, and Sluka KA. Comparison of microdialysis and push-pull perfusion for retrieval of serotonin and norepinephrine in the spinal cord dorsal horn. J Neurosci Methods 126: 187-194, 2003. Liu D, Valadez V, Sorkin LS, and McAdoo DJ. Norepinephrine and serotonin release upon impact injury to rat spinal cord. J Neurotrauma 7: 219 -227, 1990. Magnusson T. Effect of chronic transection on dopamine, noradrenaline and 5-hydroxytryptamine in the rat spinal cord. Naunyn Schmiedebergs Arch Pharmacol 278: 13-22, 1973. Marcoux J and Rossignol S. Initiating or blocking locomotion in spinal cats by applying noradrenergic drugs to restricted lumbar spinal segments. J Neurosci 20: 8577-8585, 2000. Marlier L, Sandillon F, Poulat P, Rajaofetra N, Geffard M, and Privat A. Serotonin innervation of the dorsal horn of the rat spinal cord: light and electron microscopic immunocytochemical study. J Neurocytol 20: 310 -322, 1991. Martin RF, Jordan LM, and Willis WD. Differential projections of cat medullary raphe neurons demonstrated by retrograde labeling following spinal cord lesions. J Comp Neurol 182: 77-88, 1978. Matos FF, Rollema H, and Basbaum AI. Simultaneous measurement of extracellular morphine and serotonin in brain tissue and CSF by microdialysis in awake rats. J Neurochem 58: 1773-1781, 1992. Maxwell DJ, Leranth CS, and Verhofstad AA. Fine structure of serotonincontaining axons in the marginal zone of the rat spinal cord. Brain Res 266: 253-259, 1983. Maxwell L, Maxwell DJ, Neilson M, and Kerr R. A confocal microscopic survey of serotoninergic axons in the lumbar spinal cord of the rat: colocalization with glutamate decarbosylase and neuropeptides. Neuroscience 75: 471-480, 1996. Men D-S and Matsui Y. Peripheral nerve stimulation increases serotonin and dopamine metabolites in rat spinal cord. Brain Res Bull 33: 625-632, 1994. Men D-S, Matsui A, and Matsui Y. Somatosensory afferent inputs release 5-HT and NA from the spinal cord. Neurochem Res 21: 1515-1519, 1996. Millan MJ. The induction of pain: an integrative review.