Descriptive and functional neuroanatomy of locus coeruleus-noradrenaline-containing neurons involvement in bradykinin-induced antinociception on principal sensory trigeminal nucleus

Couto, Lucélio Bernardes; Moroni, Cristian Rogério; Ferreira, César Augusto; Elias-Filho, D.H.; Parada, Carlos Amílcar; Pelá, Irene Rosemir; Coimbra, Norberto Cysne

doi:10.1016/j.jchemneu.2006.03.003

Cited by 45 publications

(49 citation statements)

References 130 publications

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“…The locus coeruleus is the main source of noradrenaline production in the brain with connections to cortical structures and to the spinal cord dorsal horn [42]. This nucleus also inhibits nociceptive processing in the sensory trigeminal nucleus and Sp5 [18], similar to raphe nuclei. In addition, locus coeruleus could be involved in vascular regulation of migraine through direct projections to both intra- and extra-cranial vasculature [39].…”

Section: Discussionmentioning

confidence: 99%

Modulation of brainstem activity and connectivity by respiratory-gated auricular vagal afferent nerve stimulation in migraine patients

García

Lin

Lee

et al. 2017

Pain

107

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Migraine pathophysiology includes altered brainstem excitability, and recent neuromodulatory approaches aimed at controlling migraine episodes have targeted key brainstem relay and modulatory nuclei. In this study, we evaluated the impact of respiratory-gated auricular vagal afferent nerve stimulation (RAVANS), a novel neuromodulatory intervention based on an existing transcutaneous Vagus Nerve Stimulation approach, in the modulation of brainstem activity and connectivity in migraine patients. We applied 3T-functional magnetic resonance imaging with improved in-plane spatial resolution (2.62×2.62 mm) in episodic migraine (interictal) and age- and sex-matched healthy controls to evaluate brain response to RAVANS (gated to either inhalation or exhalation) and sham stimulation. We further investigated RAVANS modulation of tactile trigeminal sensory afference response in the brainstem using air-puff stimulation directed to the forehead during functional magnetic resonance imaging. Compared to sham and inhalatory-gated RAVANS (iRAVANS), exhalatory-gated RAVANS (eRAVANS) activated an ipsilateral pontomedullary region consistent with nucleus tractus solitarii (NTS). During eRAVANS, NTS connectivity was increased to anterior insula and anterior mid-cingulate cortex, compared to both sham and iRAVANS, in migraine patients. Increased connectivity was inversely correlated with relative time to the next migraine attack, suggesting clinical relevance to this change in connectivity. Post-stimulation effects were also noted immediately following eRAVANS, as we found increased activation in putative pontine serotonergic (i.e. nucleus raphe centralis) and noradrenergic (i.e. locus coeruleus) nuclei in response to trigeminal sensory afference. Regulation of activity and connectivity of brainstem and cortical regions involved in serotonergic and noradrenergic regulation and pain modulation may constitute an underlying mechanism supporting beneficial clinical outcomes for eRAVANS applied for episodic migraine.

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Section: Discussionmentioning

confidence: 99%

Modulation of brainstem activity and connectivity by respiratory-gated auricular vagal afferent nerve stimulation in migraine patients

García

Lin

Lee

et al. 2017

Pain

107

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“…It has been shown that the SpV receives input from sites involved in pain modulation. For example, it has been reported that the locus coeruleus (a noradrenergic region involved in endogenous pain modulation) projects to-and can modulate-the activity of neurons in the rostral SpV complex, particularly SpVo and Vp [Couto et al, 2006;Sasa et al, 1974]. Furthermore, brainstem regions that form part of the serotinergic endogenous analgesic system, namely the nucleus raphe magnus, send projections to the caudal regions of SpV, specifically SpVc and SpVi, and these connections have been shown to modulate the response of SpV neurons during acute noxious stimuli [Basbaum and Fields, 1984].…”

Section: Discussionmentioning

confidence: 99%

Differential activation of the human trigeminal nuclear complex by noxious and non‐noxious orofacial stimulation

Nash¹,

Macefield²,

Klineberg³

et al. 2009

Human Brain Mapping

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There is good evidence from animal studies for segregation in the processing of non-nociceptive and nociceptive information within the trigeminal brainstem sensory nuclear complex. However, it remains unknown whether a similar segregation occurs in humans, and a recent tract tracing study suggests that this segregation may not exist. We used functional magnetic resonance imaging (fMRI) to define and compare activity patterns of the trigeminal brainstem nuclear complex during non-noxious and noxious cutaneous and non-noxious and noxious muscle orofacial stimulation in humans. We found that during cutaneous pain, signal intensity increased within the entire rostrocaudal extent of the spinal trigeminal nucleus (SpV), encompassing the ipsilateral oralis (SpVo), interpolaris (SpVi) and caudalis (SpVc) subdivisions. In contrast, muscle pain did not activate SpVi, but instead activated a discrete region of the ipsilateral SpVo and SpVc. Further, muscle noxious stimulation activated a region of the ipsilateral lateral pons in the region of the trigeminal principal sensory nucleus (Vp). Innocuous orofacial stimulation (lip brushing) also evoked a significant increase in signal intensity in the ipsilateral Vp; however, non-noxious muscle stimulation showed no increase in signal in this area. The data reveal that orofacial cutaneous and muscle nociceptive information and innocuous cutaneous stimulation are differentially represented within the trigeminal nuclear complex. It is well established that cutaneous and muscle noxious stimuli evoke different perceptual, behavioural and cardiovascular changes. We speculate that the differential activation evoked by cutaneous and muscle noxious stimuli within the trigeminal sensory complex may contribute to the neural basis for these differences.

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“…Another major action of the serotonergic projection to the spinal cord is the suppression of nociception [66, 113, 239], achieved through the release of serotonin in the dorsal spinal cord [135, 162, 188, 297]. Interestingly, α 1 - and α 2 -adrenoceptors have been found to be co-localised on raphe magnus neurones involved in the inhibition of nociception [34].…”

Section: Output Functions Of the Locus Coeruleusmentioning

confidence: 99%

“…In contrast to the sparse innervation of the trigeminal motor nucleus, the LC densely innervates the neurones of the trigeminal sensory nucleus [66, 197, 261, 321] and this pathway is likely to be involved in the antinociceptive function of the LC [47, 66, 367]. Indeed, electrical stimulation of the LC has been found to inhibit the neurones of the sensory trigeminal nucleus involved in pain perception [230, 312, 314, 367].…”

Section: Output Functions Of the Locus Coeruleusmentioning

confidence: 99%

Functional Neuroanatomy of the Noradrenergic Locus Coeruleus: Its Roles in the Regulation of Arousal and Autonomic Function Part I: Principles of Functional Organisation

Samuels

Szabadi²

2008

623

510

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The locus coeruleus (LC) is the major noradrenergic nucleus of the brain, giving rise to fibres innervating extensive areas throughout the neuraxis. Recent advances in neuroscience have resulted in the unravelling of the neuronal circuits controlling a number of physiological functions in which the LC plays a central role. Two such functions are the regulation of arousal and autonomic activity, which are inseparably linked largely via the involvement of the LC. The LC is a major wakefulness-promoting nucleus, resulting from dense excitatory projections to the majority of the cerebral cortex, cholinergic neurones of the basal forebrain, cortically-projecting neurones of the thalamus, serotoninergic neurones of the dorsal raphe and cholinergic neurones of the pedunculopontine and laterodorsal tegmental nucleus, and substantial inhibitory projections to sleep-promoting GABAergic neurones of the basal forebrain and ventrolateral preoptic area. Activation of the LC thus results in the enhancement of alertness through the innervation of these varied nuclei. The importance of the LC in controlling autonomic function results from both direct projections to the spinal cord and projections to autonomic nuclei including the dorsal motor nucleus of the vagus, the nucleus ambiguus, the rostroventrolateral medulla, the Edinger-Westphal nucleus, the caudal raphe, the salivatory nuclei, the paraventricular nucleus, and the amygdala. LC activation produces an increase in sympathetic activity and a decrease in parasympathetic activity via these projections. Alterations in LC activity therefore result in complex patterns of neuronal activity throughout the brain, observed as changes in measures of arousal and autonomic function.

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Descriptive and functional neuroanatomy of locus coeruleus-noradrenaline-containing neurons involvement in bradykinin-induced antinociception on principal sensory trigeminal nucleus

Cited by 45 publications

References 130 publications

Modulation of brainstem activity and connectivity by respiratory-gated auricular vagal afferent nerve stimulation in migraine patients

Modulation of brainstem activity and connectivity by respiratory-gated auricular vagal afferent nerve stimulation in migraine patients

Differential activation of the human trigeminal nuclear complex by noxious and non‐noxious orofacial stimulation

Functional Neuroanatomy of the Noradrenergic Locus Coeruleus: Its Roles in the Regulation of Arousal and Autonomic Function Part I: Principles of Functional Organisation

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