Glutamate- and GABA-immunoreactive synapses on sympathetic preganglionic neurons caudal to a spinal cord transection in rats

• Published in: Neuroscience 1997-10, Vol.80 (4), p.1225-1235
• Main Authors: Llewellyn-Smith, I.J, Cassam, A.K, Krenz, N.R, Krassioukov, A.V, Weaver, L.C
• Format: Article
• Language: English
• Subjects: Adrenal Medulla - innervation; amino acids; Animals; autonomic dysreflexia; Axonal Transport; Biological and medical sciences; cholera toxin B subunit; Dendrites - physiology; Dendrites - ultrastructure; Fundamental and applied biological sciences. Psychology; gamma-Aminobutyric Acid - analysis; Ganglia, Sympathetic - physiology; Ganglia, Sympathetic - physiopathology; Glutamic Acid - analysis; immunocytochemistry; Male; Microscopy, Immunoelectron; Neurons - pathology; Neurons - physiology; Neurons - ultrastructure; Peripheral nervous system. Autonomic nervous system. Neuromuscular transmission. Ganglionic transmission. Electric organ; Rats; Rats, Wistar; retrograde tracing; Spinal Cord - physiology; Spinal Cord Injuries - pathology; Spinal Cord Injuries - physiopathology; spinal cord injury; Synapses - pathology; Synapses - physiology; Synapses - ultrastructure; Vertebrates: nervous system and sense organs
• ISSN: 0306-4522; 1873-7544
• DOI: 10.1016/S0306-4522(97)00155-3

Spinal cord injury destroys bulbospinal amino acid-containing pathways to sympathetic preganglionic neurons and severely disrupts blood pressure control, resulting in resting or postural hypotension and episodic hypertension. Almost all immunoreactivity for the excitatory amino acid l-glutamate has been reported to disappear from autonomic areas of the cord caudal to a transection, apparently depriving autonomic neurons of their major excitatory input. However, the magnitude of the neurogenic episodic hypertension after cord injury suggests that excitatory inputs to sympathetic preganglionic neurons must still be present. Moreover, the hypotension associated with high spinal injuries may reflect a enhanced role for inhibitory transmitters, such as GABA. This apparent contradiction regarding the presence of glutamate and lack of information about GABA prompted the present investigation. In rats seven days after spinal cord transection, we examined identified sympathetic preganglionic neurons caudal to the injury for the presence of synapses or direct contacts from varicosities that were immunoreactive for the amino acids, l-glutamate and GABA. Adrenal sympathetic preganglionic neurons were retrogradely labelled with cholera toxin B subunit and amino acid immunoreactivity was revealed with post-embedding immunogold labelling. In single ultrathin sections, 46% (98/212) of the synapses or direct contacts on adrenal sympathetic preganglionic neurons were immunoreactive for glutamate and 39% (83/214) were immunoreactive for GABA. Analysis of inputs with the physical disector yielded similar results for the two amino acids. The proportions of glutamatergic or GABAergic synapses on cell bodies and dendrites were similar. When alternate ultrathin sections were stained to reveal glutamate or GABA immunoreactivity, either one or the other amino acid occurred in 78.4% (116/148) of inputs; 4.1% (6/148) of inputs contained both amino acids and 17.5% (26/148) of inputs contained neither. These results demonstrate that nerve fibres immunoreactive for the neurotransmitter amino acids, glutamate and GABA, provide most of the input to sympathetic preganglionic neurons caudal to a spinal cord transection. Synapses containing glutamate and GABA could provide the anatomical substrate for the exaggerated sympathetic reflexes and the low sympathetic tone that result from spinal cord injury.