Elsevier

Neuroscience

Volume 110, Issue 2, 12 March 2002, Pages 319-328
Neuroscience

Nociceptive afferents selectively modulate the cardiac component of the peripheral chemoreceptor reflex via actions within the solitary tract nucleus

https://doi.org/10.1016/S0306-4522(01)00585-1Get rights and content

Abstract

Our previous findings showed that the nucleus of the solitary tract (NTS) mediated part of the tachycardia evoked during somatic noxious stimulation. Here, we investigated the interaction between somatic nociceptor- and peripheral chemoreceptor-evoked cardiac changes. We sought to determine whether this interaction occurred within the NTS, the primary site of termination of chemoreceptor afferents. In a working heart–brainstem preparation of rat, mechanical noxious activation of a forelimb evoked a tachycardia of 17.5±3 (mean±S.E.M.) b.p.m., whereas sodium cyanide (7–30 μg) stimulation of peripheral chemoreceptors produced a sub-maximal bradycardia of −140±15 b.p.m. During nociceptor stimulation the sodium cyanide-evoked bradycardia was attenuated to −42.6±12 b.p.m. but could be prevented by a multiple bilateral NTS microinjection of bicuculline (i.e. −173±18 b.p.m.). Furthermore, the activity of NTS neurones responding to peripheral chemoreceptor stimulation increased from 2.8±1.3 to 9.4±1.9 Hz during sodium cyanide injection (n=7; P<0.01). The latter response was attenuated reversibly to 2.9±0.9 Hz during simultaneous stimulation of the brachial nerve. Pressure ejection of bicuculline abolished this inhibitory action of brachial-nerve stimulation on the chemoreceptor-evoked excitatory synaptic response.

We conclude that somatic noxious stimulation attenuates the chemoreceptor reflex-evoked bradycardia via a GABAAergic mechanism in the NTS.

Section snippets

The working heart–brainstem preparation (WHBP)

The experimental procedures were approved by the Home Office. Sprague–Dawley rats (University of Bristol colony; 75–150 g male/female) were anaesthetised deeply in a saturated environment of halothane, and the WHBP prepared according to the original description by Paton (1996). Every effort was made to minimise the number of animals used. Prior to surgery, the level of anaesthesia was assessed as deep by a complete absence of withdrawal reflexes following a pinch to a paw or the tail. The rat

Control values

In 13 WHBP the mean HR and PNA cycle length were 279±8.4 b.p.m. and 3.6±0.3 s respectively.

Peripheral chemoreceptor reflex and effect of noxious stimulation

Aortic injection of CN to stimulate peripheral chemoreceptors elicited a reflex bradycardia (−121±12 b.p.m.) and decreased PNA cycle length (Table 1 and Fig. 1; n=13; P<0.01). In these preparations, mechanical noxious stimulation of either forelimb elicited a tachycardia (17.5±3 b.p.m.) and decreased PNA cycle length (Table 1 and Fig. 1; n=13; P<0.01); this is quantitatively similar to our recent report (

Discussion

Our results show that the reflex bradycardia following stimulation of peripheral chemoreceptors is attenuated by activation of forelimb nociceptors. This attenuation occurs at the level of the NTS and involves a GABAAergic mechanism. Furthermore, electrical stimulation of somatic afferents in the brachial nerve (to include Aδ and C fibres) can depress the synaptic response of some NTS neurones activated orthodromically by peripheral chemoreceptors. The latter is also mediated by GABAA

Acknowledgements

We thank Tony MacDonald for building the strain gauge used to measure forces generated during mechanical noxious stimulation. P.B. is supported by a University of Bristol postgraduate scholarship. The work was supported by the British Heart Foundation (BS/93003).

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