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

Potts, Jeffrey T.; Paton, Julian F. R.; Mitchell, Jere H.; Garry, Mary G.; Kline, Greg; Anguelov, P.T.; Lee, S.M.

doi:10.1016/s0306-4522(02)00953-3

Cited by 77 publications

(75 citation statements)

References 51 publications

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“…On the other hand, the inhibition of the commNTS reduces splanchnic sympathetic nerve activity and, consequently, produces a marked fall in blood pressure in SHR, suggesting this subnucleus of the NTS is tonically active in SHR (41). Thereby, according to the previous reports, the intermediate and commissural NTS have different neurons that control the Muscle afferents release substance P in the NTS and activate GABAergic neurons (37,38). They seem to inhibit baroreflex neurons contributing to the resetting of baroreceptor reflex mechanism toward high blood pressure levels during exercise (38).…”

Section: Discussionmentioning

confidence: 88%

“…Thereby, according to the previous reports, the intermediate and commissural NTS have different neurons that control the Muscle afferents release substance P in the NTS and activate GABAergic neurons (37,38). They seem to inhibit baroreflex neurons contributing to the resetting of baroreceptor reflex mechanism toward high blood pressure levels during exercise (38). In contrast, our data suggest the GABAergic neurons in the commNTS seem to be most important for depressor responses, and moreover, they appear essential for the enhanced vasodilation in the hindlimb in rats submitted to exercise training.…”

Section: Discussionmentioning

confidence: 94%

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Exercise changes regional vascular control by commissural NTS in spontaneously hypertensive rats

Ogihara

Schoorlemmer

Levada

et al. 2010

American Journal of Physiology-Regulatory, Integrative and Comp

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Ogihara CA, Schoorlemmer GHM, Levada AC, Pithon-Curi TC, Curi R, Lopes OU, Colombari E, Sato MA. Exercise changes regional vascular control by commissural NTS in spontaneously hypertensive rats. Am J Physiol Regul Integr Comp Physiol 299: R291-R297, 2010. First published April 21, 2010 doi:10.1152/ajpregu.00055.2009.-Inhibition of the commissural nucleus of the solitary tract (commNTS) induces a fall in sympathetic nerve activity and blood pressure in spontaneously hypertensive rats (SHR), which suggests that this subnucleus of the NTS is a source of sympathoexcitation. Exercise training reduces sympathetic activity and arterial pressure. The purpose of the present study was to investigate whether the swimming exercise can modify the regional vascular responses evoked by inhibition of the commNTS neurons in SHR and normotensive Wistar-Kyoto (WKY) rats. Exercise consisted of swimming, 1 h/day, 5 days/wk for 6 wks, with a load of 2% of the body weight. The day after the last exercise session, the rats were anesthetized with intravenous ␣-chloralose, tracheostomized, and artificially ventilated. The femoral artery was cannulated for mean arterial pressure (MAP) and heart rate recordings, and Doppler flow probes were placed around the lower abdominal aorta and superior mesenteric artery. Microinjection of 50 mM GABA into the commNTS caused similar reductions in MAP in swimming and sedentary SHR (Ϫ25 Ϯ 6 and Ϫ30 Ϯ 5 mmHg, respectively), but hindlimb vascular conductance increased twofold in exercised vs. sedentary SHR (54 Ϯ 8 vs. 24 Ϯ 5%). GABA into the commNTS caused smaller reductions in MAP in swimming and sedentary WKY rats (Ϫ20 Ϯ 4 and Ϫ16 Ϯ 2 mmHg). Hindlimb conductance increased fourfold in exercised vs. sedentary WKY rats (75 Ϯ 2% vs. 19 Ϯ 3%). Therefore, our data suggest that the swimming exercise induced changes in commNTS neurons, as shown by a greater enhancement of hindlimb vasodilatation in WKY vs. SHR rats in response to GABAergic inhibition of these neurons.GABA; cardiovascular; citrate synthase THE NUCLEUS OF THE SOLITARY tract (NTS) is the primary site in the central nervous system that receives the afferents arising from arterial baro-and chemoreceptors (10, 15). The intermediate NTS receives inputs particularly from arterial baroreceptors, but some of these afferents achieve the commNTS (10, 16). The commNTS also receives inputs from arterial chemoreceptors, and seems to be highly sensitive to carotid chemoreceptor stimulation (8, 9, 11).The possible role of the commNTS as a source of sympathoexcitation was first shown by Nelson et al. (33), which demonstrated that nanoliter injections of L-glutamate into the commNTS evoke elevations in heart rate and arterial pressure mediated by the sympathetic nervous system. Electrolytic lesions or chemical inhibition of the commNTS have been shown to markedly decrease the splanchnic sympathetic nerve activity and arterial pressure in spontaneously hypertensive rats (SHR), which suggested that this subnucleus of the NTS contains neurons tonically active in S...

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Section: Discussionmentioning

confidence: 88%

Section: Discussionmentioning

confidence: 94%

Exercise changes regional vascular control by commissural NTS in spontaneously hypertensive rats

Ogihara

Schoorlemmer

Levada

et al. 2010

American Journal of Physiology-Regulatory, Integrative and Comp

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“…The DMH directly innervates the nTS (Fontes et al, 2001), and electrical or chemical (see review (McDowall et al, 2006)) stimulation of the DMH decreases the sensitivity of the baroreflex through a GABAergic mechanism in the nTS/DMV (Jordan et al, 1988). This circuit represents an adaptive means of inhibiting the baroreflex during 'fight or flight' responses and exercise (Potts et al, 2003). The nTS contains numerous GABAergic neurons (Fong et al, 2005) which could be dampening parasympathetic activity by inhibiting acetylcholinergic vagal preganglionic neurons.…”

Section: Pathways For Lactate-induced Panic-like Responsesmentioning

confidence: 99%

Neural Pathways Underlying Lactate-Induced Panic

Johnson

Truitt

Fitz

et al. 2007

Neuropsychopharmacol

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Panic disorder is a severe anxiety disorder characterized by susceptibility to induction of panic attacks by subthreshold interoceptive stimuli such as 0.5 M sodium lactate infusions. Although studied for four decades, the mechanism of lactate sensitivity in panic disorder has not been understood. The dorsomedial hypothalamus/perifornical region (DMH/PeF) coordinates rapid mobilization of behavioral, autonomic, respiratory and endocrine responses to stress, and rats with disrupted GABA inhibition in the DMH/PeF exhibit panic-like responses to lactate, similar to panic disorder patients. Utilizing a variety of anatomical and pharmacological methods, we provide evidence that lactate, via osmosensitive periventricular pathways, activates neurons in the compromised DMH/PeF, which relays this signal to forebrain limbic structures such as the bed nucleus of the stria terminalis to mediate anxiety responses, and specific brainstem sympathetic and parasympathetic pathways to mediate the respiratory and cardiovascular components of the panic-like response. Acutely restoring local GABAergic tone in the DMH/PeF blocked lactate-induced panic-like responses. Autonomic panic-like responses appear to be a result of DMH/PeF-mediated mobilization of sympathetic responses (verified with atenolol) and resetting of the parasympathetically mediated baroreflex. Based on our findings, DMH/PeF efferent targets such as the C1 adrenergic neurons, paraventricular hypothalamus, and the central amygdala are implicated in sympathetic mobilization; the nucleus of the solitary tract is implicated in baroreflex resetting; and the parabrachial nucleus is implicated in respiratory responses. These results elucidate neural circuits underlying lactate-induced panic-like responses and the involvement of both sympathetic and parasympathetic systems.

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“…A prime example of such interaction is the somatosympathetic reflex, in which stimulation of thinly myelinated group III (A␦) and unmyelinated group IV (C-fiber) limb muscle afferent fibers can reflexly increase cardiorespiratory output (Potts et al, 2000(Potts et al, , 2003Wilson, 2000). These reflexes are mediated via sensory afferent input to the spinal cord, which is then relayed to the nucleus tractus solitarius (NTS), a brainstem site for cardiorespiratory integration (Potts et al, 2003).…”

Section: Introductionmentioning

confidence: 99%

The Neurochemically Diverse Intermedius Nucleus of the Medulla as a Source of Excitatory and Inhibitory Synaptic Input to the Nucleus Tractus Solitarii

Edwards¹,

Dallas²,

Poole³

et al. 2007

J. Neurosci.

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Sensory afferent signals from neck muscles have been postulated to influence central cardiorespiratory control as components of postural reflexes, but neuronal pathways for this action have not been identified. The intermedius nucleus of the medulla (InM) is a target of neck muscle spindle afferents and is ideally located to influence such reflexes but is poorly investigated. To aid identification of the nucleus, we initially produced three-dimensional reconstructions of the InM in both mouse and rat. Neurochemical analysis including transgenic reporter mice expressing green fluorescent protein in GABA-synthesizing neurons, immunohistochemistry, and in situ hybridization revealed that the InM is neurochemically diverse, containing GABAegric and glutamatergic neurons with some degree of colocalization with parvalbumin, neuronal nitric oxide synthase, and calretinin. Projections from the InM to the nucleus tractus solitarius (NTS) were studied electrophysiologically in rat brainstem slices. Electrical stimulation of the NTS resulted in antidromically activated action potentials within InM neurons. In addition, electrical stimulation of the InM resulted in EPSPs that were mediated by excitatory amino acids and IPSPs mediated solely by GABA A receptors or by GABA A and glycine receptors. Chemical stimulation of the InM resulted in (1) a depolarization of NTS neurons that were blocked by NBQX (2,3-dioxo-6-nitro-1,2,3,4-tetrahydrobenzo[f ]quinoxaline-7-sulfonoamide) or kynurenic acid and (2) a hyperpolarization of NTS neurons that were blocked by bicuculline. Thus, the InM contains neurochemically diverse neurons and sends both excitatory and inhibitory projections to the NTS. These data provide a novel pathway that may underlie possible reflex changes in autonomic variables after neck muscle spindle afferent activation.

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

Cited by 77 publications

References 51 publications

Exercise changes regional vascular control by commissural NTS in spontaneously hypertensive rats

Exercise changes regional vascular control by commissural NTS in spontaneously hypertensive rats

Neural Pathways Underlying Lactate-Induced Panic

The Neurochemically Diverse Intermedius Nucleus of the Medulla as a Source of Excitatory and Inhibitory Synaptic Input to the Nucleus Tractus Solitarii

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