TRPV1-Lineage Somatosensory Fibers Communicate with Taste Neurons in the Mouse Parabrachial Nucleus

Li, Jinrong; Ali, Md Sams Sazzad; Lemon, Christian H.

doi:10.1523/jneurosci.0927-21.2021

Cited by 10 publications

(9 citation statements)

References 76 publications

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“…Consistent with this, studies have shown PbN neurons are activated by a variety of danger signals and this activation contributes to behavioral responses to threat in a cell-type and circuit-specific manner (14,31,(56)(57)(58)(59)(60)(61)(62)(63)(64). PbN neurons that express Calcitonin gene-related peptide (CGRP) and project to the CeA, for example, have been shown to modulate escape responses to noxious heat and contribute to threat memory (31).…”

Section: Protective and Maladaptive Functions Of The Pbn→cea In Respo...mentioning

confidence: 77%

The parabrachial to central amygdala circuit is a key mediator of injury-induced pain sensitization

Torres-Rodriguez

Wilson

Singh

et al. 2023

Preprint

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The spino-ponto-amygdaloid pathway is a major ascending circuit relaying nociceptive information from the spinal cord to the brain. Potentiation of excitatory synaptic transmission in the parabrachial nucleus (PbN) to central amygdala (CeA) pathway has been reported in rodent models of persistent pain. At the behavioral level, the PbN→CeA pathway has been proposed to serve as a general alarm system to potential threats that modulates pain-related escape behaviors, affective-motivational (but not somatosensory) responses to painful stimuli, aversion, and threat memory. Increased sensitivity to previously innocuous somatosensory stimulation is a hallmark of chronic pain. Whether the PbN→CeA circuit contributes to heightened sensitivity to somatosensory stimulation following an injury, however, remains unknown. Here, we demonstrate that activation of CeA-projecting PbN neurons contributes to injury-induced behavioral hypersensitivity but not baseline nociception in male and female mice. Using optogenetic assisted circuit mapping, we confirmed a functional excitatory projection from PbN→CeA that is independent of the genetic or firing identity of CeA cells. We then showed that peripheral noxious stimulation increases the expression of the neuronal activity marker c-Fos in CeA-projecting PbN neurons and chemogenetic inactivation of these cells reduces behavioral hypersensitivity in models of neuropathic and inflammatory pain without affecting baseline nociception. Lastly, we show that chemogenetic activation of CeA-projecting PbN neurons is sufficient to induce bilateral hypersensitivity without injury. Together, our results demonstrate that the PbN→CeA pathway is a key modulator pain-related behaviors that can amplify responses to somatosensory stimulation in pathological states without affecting nociception under normal physiological conditions.

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Section: Protective and Maladaptive Functions Of The Pbn→cea In Respo...mentioning

confidence: 77%

The parabrachial to central amygdala circuit is a key mediator of injury-induced pain sensitization

Torres-Rodriguez

Wilson

Singh

et al. 2023

Preprint

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“…NNMF is a matrix decomposition technique that can identify a small number of additive data features that compose patterns in a data set and can be used to classify data points (Lee and Seung, 1999; Brunet et al, 2004). We previously described use of this technique for classification of trigeminal-integrative neurons in the brain based on orosensory tuning (Li et al, 2022) and we followed that approach here. In brief, NNMF reduced a matrix of stimulus responses by individual cells to two non-negative, lower-dimensional matrices.…”

Section: Methodsmentioning

confidence: 99%

“…We discarded runs which converged to a rank lower than k , which was infrequent. The final k used to determine the number of cellular clusters present in the data was the largest k that resulted in the highest percentage of runs that repeatedly placed any given pair of neurons into the same or different cluster, evaluated using visual and quantitative methods (Brunet et al, 2004; Li et al, 2022). For the present analysis, the best k was found to be 2, indicating there were two major groups of TRPM8-KO/wild-type Vc cells based on thermal tuning.…”

Section: Methodsmentioning

confidence: 99%

“…We previously described use of this technique for classification of trigeminal-integrative neurons in the brain based on orosensory tuning (Li et al, 2022) and we followed that approach here. In brief, NNMF reduced a matrix of stimulus responses by individual cells to two non-negative, lower-dimensional matrices.…”

Section: Analysis Of Vc Neurons In Trpm8-ko and Wild-type Micementioning

confidence: 99%

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Diverse thermosensory receptors and neurons mediate the neural coding of oral cooling in the mouse trigeminothalamic tract

Lemon

2022

Preprint

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Different sets of peripheral and medullary trigeminal neurons respond across a cooling gradient applied to intraoral skin. Here we applied electrophysiology to anesthetized mice to study if different types of cool-driven trigeminothalamic neurons convey oral cooling information to the thalamus. We monitored spiking responses to oral stimulation with cold (≤13°C), cool (21°C to 28°C), neutral (35°C), and warm/hot (≥40°C) water in single trigeminal nucleus caudalis (Vc) neurons physiologically tested for projections to the thalamus. We also recorded oral thermal responses from Vc neurons in mice gene deficient for the cooling and menthol receptor TRPM8 to study afferent mechanisms of central oral thermosensory activity. We found that thalamic-projecting Vc neurons that respond to oral cooling comprise heterogeneous cell types. These cell types showed unique temporal response kinetics across cool and cold temperatures, with tuning to select ranges of a cooling gradient. The combined thermal activity of multiple, differently tuned types of trigeminothalamic cooling neurons offered greater contrast between cold, cool, and warm temperatures in multivariate analysis than the responses of the individual neural types alone, agreeing with a neural population code for cooling information. Compared to control, TRPM8 deficient mice demonstrated a loss of Vc neurons tuned to mild oral cooling, but maintained Vc cells responsive to intense cold. Notably, distinctions between Vc population responses to mild cool and warm temperatures were impaired in TRPM8 deficient mice, suggesting a role for TRPM8 in oral warmth recognition. Diverse receptors and neurons mediate oral cooling signals carried by the trigeminothalamic pathway.

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“…In mice, ascending projections from trigeminal neurons reach the parabrachial nucleus (PB). Trigeminal fibers use TRPV1 and TRPA1 to play a role in thermosensation and pain communication with parabrachial taste neurons (Li et al, 2021;Rhyu et al, 2021). In summary, mammals' somatosensory cortical regions (S1, S2, and PV) have integrated with the motor cortex and visual, auditory, vestibular, taste, and olfactory cortical areas.…”

Section: Somatosensory-taste Interactionsmentioning

confidence: 99%

Neurosensory development of the four brainstem-projecting sensory systems and their integration in the telencephalon

Fritzsch

Elliott

Yamoah

2022

Front. Neural Circuits

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Somatosensory, taste, vestibular, and auditory information is first processed in the brainstem. From the brainstem, the respective information is relayed to specific regions within the cortex, where these inputs are further processed and integrated with other sensory systems to provide a comprehensive sensory experience. We provide the organization, genetics, and various neuronal connections of four sensory systems: trigeminal, taste, vestibular, and auditory systems. The development of trigeminal fibers is comparable to many sensory systems, for they project mostly contralaterally from the brainstem or spinal cord to the telencephalon. Taste bud information is primarily projected ipsilaterally through the thalamus to reach the insula. The vestibular fibers develop bilateral connections that eventually reach multiple areas of the cortex to provide a complex map. The auditory fibers project in a tonotopic contour to the auditory cortex. The spatial and tonotopic organization of trigeminal and auditory neuron projections are distinct from the taste and vestibular systems. The individual sensory projections within the cortex provide multi-sensory integration in the telencephalon that depends on context-dependent tertiary connections to integrate other cortical sensory systems across the four modalities.

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TRPV1-Lineage Somatosensory Fibers Communicate with Taste Neurons in the Mouse Parabrachial Nucleus

Cited by 10 publications

References 76 publications

The parabrachial to central amygdala circuit is a key mediator of injury-induced pain sensitization

The parabrachial to central amygdala circuit is a key mediator of injury-induced pain sensitization

Diverse thermosensory receptors and neurons mediate the neural coding of oral cooling in the mouse trigeminothalamic tract

Neurosensory development of the four brainstem-projecting sensory systems and their integration in the telencephalon

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