The ins and outs of the caudal nucleus of the solitary tract: An overview of cellular populations and anatomical connections

Holt, Marie K.

doi:10.1111/jne.13132

Cited by 19 publications

(16 citation statements)

References 221 publications

(294 reference statements)

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“…However, the similarity between contra- and ipsilateral evoked NE transients s suggests that the noradrenergic response reflects a general aversiveness of sensory inputs, rather than spatial or modality specific information. This functional observation is consistent with anatomical studies demonstrating bilateral projections from dorsal horn neurons to the NTS (Menetrey and Basbaum, 1987; Holt et al, 2019; Holt, 2022).…”

Section: Discussionsupporting

confidence: 91%

“…Although A2 neurons primarily project to the ipsilateral parabrachial nucleus (Milner et al, 1986), robust NE release was measured in response to noxious stimuli—thermal or mechanical—applied ipsilateral or contralateral to the recorded side. This functional observation is consistent with anatomical studies demonstrating bilateral projections from dorsal horn neurons to the NTS (Menetrey and Basbaum, 1987; Holt et al, 2019; Holt, 2022), and suggests that the noradrenergic response reflects a general aversiveness of sensory inputs, rather than spatial or modality specific information.…”

Section: Discussionsupporting

confidence: 88%

“…The majority of A2 neurons receive monosynaptic excitatory input from the solitary tract (Appleyard et al, 2007) and respond to a wide range of interoceptive and aversive signals (Rinaman, 2011). Caudal NTS neurons also receive direct projections from medullary and dorsal horn neurons, and this overlap has been postulated to aid integration of somatosensory and interoceptive stimuli (Menetrey and Basbaum, 1987; Holt et al, 2019; Holt, 2022). Projections from the caudal NTS, including A2, preferentially target the lateral regions of the parabrachial nucleus (Herbert et al, 1990), including those that participate in nociception and in encoding aversiveness of noxious or stressful stimuli (Palmiter, 2018; Uddin et al, 2018; Bowen et al, 2020; Raver et al, 2020).…”

Section: Discussionmentioning

confidence: 99%

“…NE innervation of the parabrachial nucleus largely originates from the A2 cell group of the NTS, with a comparatively minor projection arising from the anatomically adjacent locus coeruleus (Milner et al, 1986). NTS neurons receive direct projections from medullary and dorsal horn neurons and solitary tract afferents, and this overlap has been postulated to aid integration of somatosensory and interoceptive stimuli (Menetrey and Basbaum, 1987; Appleyard et al, 2007; Holt et al, 2019; Holt, 2022). Projections from the cNTS, including A2 neurons, preferentially target the lateral regions of the parabrachial nucleus (Herbert et al, 1990), a hub for processing aversive stimuli (Palmiter, 2018; Uddin et al, 2018; Bowen et al, 2020; Raver et al, 2020).…”

Section: Discussionmentioning

confidence: 99%

“…NE input to PB arises from multiple cell groups, including the locus coeruleus (A6), but the single largest source is the A2 cell group in the caudal nucleus of the solitary tract (cNTS) (Milner et al, 1986). Neurons in the cNTS are responsive to stress (Rinaman, 2011) and receive exteroceptive input from medullary and spinal dorsal horn neurons (Menetrey and Basbaum, 1987), and interoceptive inputs from the vagus and glossopharyngeal nerves and blood borne signaling molecules (Holt, 2022). Thus, the aversiveness of noxious stimuli may be regulated by the convergence of multimodal inputs within cNTS and its dense noradrenergic projections to PB.…”

Section: Introductionmentioning

confidence: 99%

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Noradrenergic input from nucleus of the solitary tract regulates parabrachial activity in mice

Onwukwe

Smith

et al. 2022

Preprint

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The parabrachial complex (PB) is critically involved in aversive processes, including pain. We have reported that chronic pain is associated with amplified activity of PB neurons in rodent models of neuropathic pain. Here we demonstrate that catecholaminergic input from the caudal nucleus of the solitary tract (cNTScat)—a stress responsive region that integrates intero– and exteroceptive signals– causes amplification of PB activity and their sensory afferents. Using a virally mediated expression of a norepinephrine (NE) sensor, NE2h, and fiber photometry in anesthetized mice, noxious mechanical and thermal stimuli caused prolonged NE transients in PB that far outlast the noxious stimulus. Similar NE transients in PB were evoked by focal stimulation of the superficial cNTS, a region that contains the noradrenergic A2 cell group that projects densely upon PB. In vitro, optical stimulation of cNTScat terminals depolarized PB neurons and increased their frequency of spontaneous excitatory synaptic inputs. A dual opsin approach showed that sensory afferents from the caudal spinal trigeminal nucleus (SpVc) are potentiated by cNTScat terminal activation. This potentiation was coupled with a decrease in the paired pulse ratio, consistent with an cNTScat mediated increase in the probability of release at SpVc synapses. Together, these data suggest that A2 neurons of the cNTS generate long lasting NE transients in PB which increase excitability and potentiate responses of PB neurons to sensory inputs. These reveal a mechanism through which stressors from multiple modalities may potentiate the aversiveness of nociceptive stimuli.

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Section: Discussionsupporting

confidence: 91%

Section: Discussionsupporting

confidence: 88%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Noradrenergic input from nucleus of the solitary tract regulates parabrachial activity in mice

Onwukwe

Smith

et al. 2022

Preprint

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SubSol-HIe is an AMPK-dependent hypoxia-responsive subnucleus of the nucleus tractus solitarius that coordinates the hypoxic ventilatory response and protects against apnoea in mice

MacMillan,

Burns,

O’Halloran

et al. 2024

Pflugers Arch - Eur J Physiol

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Functional magnetic resonance imaging (fMRI) suggests that the hypoxic ventilatory response is facilitated by the AMP-activated protein kinase (AMPK), not at the carotid bodies, but within a subnucleus (Bregma -7.5 to -7.1 mm) of the nucleus tractus solitarius that exhibits right-sided bilateral asymmetry. Here, we map this subnucleus using cFos expression as a surrogate for neuronal activation and mice in which the genes encoding the AMPK-α1 (Prkaa1) and AMPK-α2 (Prkaa2) catalytic subunits were deleted in catecholaminergic cells by Cre expression via the tyrosine hydroxylase promoter. Comparative analysis of brainstem sections, relative to controls, revealed that AMPK-α1/α2 deletion inhibited, with right-sided bilateral asymmetry, cFos expression in and thus activation of a neuronal cluster that partially spanned three interconnected anatomical nuclei adjacent to the area postrema: SolDL (Bregma -7.44 mm to -7.48 mm), SolDM (Bregma -7.44 mm to -7.48 mm) and SubP (Bregma -7.48 mm to -7.56 mm). This approximates the volume identified by fMRI. Moreover, these nuclei are known to be in receipt of carotid body afferent inputs, and catecholaminergic neurons of SubP and SolDL innervate aspects of the ventrolateral medulla responsible for respiratory rhythmogenesis. Accordingly, AMPK-α1/α2 deletion attenuated hypoxia-evoked increases in minute ventilation (normalised to metabolism), reductions in expiration time, and increases sigh frequency, but increased apnoea frequency during hypoxia. The metabolic response to hypoxia in AMPK-α1/α2 knockout mice and the brainstem and spinal cord catecholamine levels were equivalent to controls. We conclude that within the brainstem an AMPK-dependent, hypoxia-responsive subnucleus partially spans SubP, SolDM and SolDL, namely SubSol-HIe, and is critical to coordination of active expiration, the hypoxic ventilatory response and defence against apnoea.

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Whole-brain monosynaptic inputs and outputs of leptin receptor b neurons of the nucleus tractus solitarii in mice

Sun,

Zhu,

Wang

et al. 2023

Brain Research Bulletin

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The ins and outs of the caudal nucleus of the solitary tract: An overview of cellular populations and anatomical connections

Cited by 19 publications

References 221 publications

Noradrenergic input from nucleus of the solitary tract regulates parabrachial activity in mice

Noradrenergic input from nucleus of the solitary tract regulates parabrachial activity in mice

SubSol-HIe is an AMPK-dependent hypoxia-responsive subnucleus of the nucleus tractus solitarius that coordinates the hypoxic ventilatory response and protects against apnoea in mice

Whole-brain monosynaptic inputs and outputs of leptin receptor b neurons of the nucleus tractus solitarii in mice

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