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The Journal of Neuroscience, May 1, 2001, 21(9):3073-3084

Lack of Neurotrophin-4 Causes Selective Structural and Chemical Deficits in Sympathetic Ganglia and Their Preganglionic Innervation

Alexander Roosen¹, Andreas Schober¹, Jens Strelau¹, Martina Böttner¹, Jörg Faulhaber², Gerald Bendner¹, Sabrina L. McIlwrath⁴, Horst Seller², Heimo Ehmke³, Gary R. Lewin⁴, and Klaus Unsicker¹

¹ Department of Neuroanatomy and Interdisciplinary Center for Neuroscience and ² Department of Physiology, University of Heidelberg, D-69120 Heidelberg, Germany, ³ Department of Physiology, University of Hamburg, D-20251 Hamburg, Germany, and ⁴ Max-Delbrück-Center for Molecular Medicine, D-13122 Berlin-Buch, Germany

Neurotrophin-4 (NT-4) is perhaps the still most enigmatic member of the neurotrophin family. We show here that NT-4 is expressed in neurons of paravertebral and prevertebral sympathetic ganglia, i.e., the superior cervical (SCG), stellate (SG), and celiac (CG) ganglion. Mice deficient for NT-4 showed a significant reduction (20-30%) of preganglionic sympathetic neurons in the intermediolateral column (IML) of the thoracic spinal cord. In contrast, neuron numbers in the SCG, SG, and CG were unchanged. Numbers of axons in the thoracic sympathetic trunk (TST) connecting the SG with lower paravertebral ganglia were also reduced, whereas axon numbers in the cervical sympathetic trunk (CST) were unaltered. Axon losses in the TST were paralleled by losses of synaptic terminals on SG neurons visualized by electron microscopy. Furthermore, immunoreactivity for the synaptic vesicle antigen SV2 was clearly reduced in the SG and CG. Levels of catecholamines and tyrosine hydroxylase immunoreactivity were dramatically reduced in the SG and the CG but not in the SCG. Despite this severe phenotype in the sympathetic system, blood pressure levels were not reduced and displayed a pattern more typical of deficits in baroreceptor afferents. Numbers of IML neurons were unaltered at postnatal day 4, suggesting a postnatal requirement for their maintenance. In light of these and previous data, we hypothesize that NT-4 provided by postganglionic sympathetic neurons is required for establishing and/or maintaining synapses of IML neurons on postganglionic cells. Impairment of synaptic connectivity may consequently reduce impulse flow, causing a reduction in transmitter synthesis in postganglionic neurons.

Key words: preganglionic sympathetic neurons; intermediolateral column; superior cervical ganglion; stellate ganglion; celiac ganglion; synapses; catecholamines; brain-derived neurotrophic factor

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Copyright © 2001 Society for Neuroscience  0270-6474/01/2193073-12$05.00/0

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