Contraction-sensitive skeletal muscle afferents inhibit arterial baroreceptor signalling in the nucleus of the solitary tract: role of intrinsic GABA interneurons

• Published in: Neuroscience 2003-01, Vol.119 (1), p.201-214
• Main Authors: Potts, J.T., Paton, J.F.R., Mitchell, J.H., Garry, M.G., Kline, G., Anguelov, P.T., Lee, S.M.
• Format: Article
• Language: English
• Subjects: Afferent Pathways - drug effects; Afferent Pathways - physiology; Animals; Arteries - physiology; Baroreflex - drug effects; Baroreflex - physiology; Bicuculline - pharmacology; Biological and medical sciences; Biotin - analogs & derivatives; Biotin - pharmacokinetics; blood pressure; Cell Count; Dextrans - pharmacokinetics; disinhibition; Dose-Response Relationship, Drug; Electric Stimulation; Electrocardiography; Enzyme Inhibitors - pharmacology; Evoked Potentials - drug effects; Evoked Potentials - physiology; exercise; Fundamental and applied biological sciences. Psychology; GABA; GABA Antagonists - pharmacology; Glutamate Decarboxylase - metabolism; Heart Rate - drug effects; Heart Rate - physiology; Immunohistochemistry; In Vitro Techniques; Isoenzymes - metabolism; Male; Muscle Contraction - drug effects; Muscle Contraction - physiology; Muscle, Skeletal - drug effects; Muscle, Skeletal - innervation; Muscle, Skeletal - physiology; neuronal signaling; Phrenic Nerve - physiology; Physical Stimulation; rat; Rats; Sodium Cyanide - pharmacology; Solitary Nucleus - cytology; Solitary Nucleus - physiology; Somesthesis and somesthetic pathways (proprioception, exteroception, nociception); interoception; electrolocation. Sensory receptors; Spinal Cord - cytology; Spinal Cord - metabolism; Vertebrates: nervous system and sense organs
• ISSN: 0306-4522; 1873-7544
• DOI: 10.1016/S0306-4522(02)00953-3

Arterial baroreceptor and skeletal muscle receptor afferents relay sensory information to the nucleus of the solitary tract (NTS) during exercise. Previous studies have suggested that skeletal muscle afferent input inhibits baroreflex function; however, detailed information on the role of muscle afferents and GABAergic mechanisms in the NTS is limited. Furthermore, identification of specific afferent modalities that activate GABAergic neurons in the NTS remains unknown. In the present study, we examined the neuroanatomical and physiological interactions between spinal dorsal horn cells that transmit contraction-sensitive input from skeletal muscle and GABAergic interneurons in the NTS. Biotinylated dextran amine (BDA, 10%, 25–100 nL) microinjection into dorsal horn of the cervical spinal cord was combined with glutamate decarboxylase (GAD) immunohistochemistry to visualize the nature of the relationship of BDA-labeled fibers in the NTS with GAD immunoreactivity (GAD-ir). BDA-labeled axons and terminal processes were localized in the medial, commissural, dorsomedial and dorsolateral subdivisions of the caudal NTS. Moreover, BDA-labeled fibers were observed in close proximity to GAD-ir structures throughout these regions of the NTS. The physiological interaction between skeletal muscle receptor and arterial baroreceptor afferents was investigated using an arterially perfused, decerebrate rat preparation. Activation of skeletal muscle afferents by electrically evoked twitch contraction of the forelimb attenuated baroreflex responsiveness (BR, calculated as the ratio of changes in heart rate to systemic pressure) from −1.5±0.3 bpm·mm Hg −1 to −0.1±0.1 bpm·mm Hg −1 (control versus contraction, P