Itch perception is reflected by neuronal ignition in the primary somatosensory cortex

Chen, Xiaojun; Liu, Yanhe; Xu, Ning-long; Sun, Yan-Gang

doi:10.1093/nsr/nwab218

Cited by 7 publications

(3 citation statements)

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“…Optogenetic activation of cervical spinal GRPR 1 neurons induced laser frequency-dependent scratching behavior (Fig. 5A-F), indicating that optogenetic manipulation of spinal GRPR 1 neurons successfully induced the itch sensation, consistent with recent studies (Liu et al, 2019;Chen et al, 2022). Next, we wondered how to separate the itch sensation and itch relief.…”

Section: Dynamics Of Dopamine Signals In the Nac Lash Under Different...supporting

confidence: 82%

“…Nevertheless, the dopamine release in the NAc LaSh at the onset of itch stimulation likely represents the motivational component. Although we cannot exclude the possibility that activation of spinal GRPR 1 neurons could elicit other sensations, it is conceivable that pruritic input should be dominant during optogenetic activation of spinal GRPR 1 neurons (Liu et al, 2019;Chen et al, 2022). Thus, the evidence provided in this study together with previous studies suggests that dopaminergic signals have a role in both the motivation and reward components of itch.…”

Section: Discussionmentioning

confidence: 46%

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Distinct Roles of Dopamine Receptor Subtypes in the Nucleus Accumbens during Itch Signal Processing

2022

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Ventral tegmental area (VTA) dopaminergic neurons, which are well known for their central roles in reward and motivation-related behaviors, have been shown to participate in itch processing via their projection to the nucleus accumbens (NAc). However, the functional roles of different dopamine receptor subtypes in subregions of the NAc during itch processing remain unknown. With pharmacological approaches, we found that the blockade of dopamine D1 receptors (D1R), but not dopamine D2 receptors (D2R), in the lateral shell (LaSh) of the NAc impaired pruritogen-induced scratching behavior in male mice. In contrast, pharmacological activation of D2R in both the LaSh and medial shell (MeSh) of the NAc attenuated the scratching behavior induced by pruritogens. Consistently, we found that dopamine release, as detected by a dopamine sensor, was elevated in the LaSh rather than the MeSh of the NAc at the onset of scratching behavior. Furthermore, the elevation of dopamine release in the LaSh of the NAc persisted even though itch-relieving behavior was blocked, suggesting that the dopamine signal in the NAc LaSh represents a motivational component of itch processing. Our study revealed different dynamics of dopamine release that target neurons expressing two dopamine receptors subtypes within different subregions of the NAc, and emphasized that D1R in the LaSh of the NAc is important in itch signal processing.SIGNIFICANCE STATEMENTDopamine has been implicated in itch signal processing. However, the mechanism underlying the functional role of dopamine in itch processing remains largely unknown. Here, we examined the role of dopamine D1 receptor (D1R) and D2R in the nucleus accumbens (NAc) shell during pruritogen-induced scratching behavior. We demonstrated that D1R in the NAc lateral shell (LaSh) play an important role in motivating itch-induced scratching behavior, while activation of D2R would terminate scratching behavior. Our study revealed the diverse functional roles of dopamine signals in the NAc shell during itch processing.

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Section: Dynamics Of Dopamine Signals In the Nac Lash Under Different...supporting

confidence: 82%

Section: Discussionmentioning

confidence: 46%

Distinct Roles of Dopamine Receptor Subtypes in the Nucleus Accumbens during Itch Signal Processing

2022

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“…Perception of sensation is generated at the brain level, and processing of somatosensory information involves multiple brain regions [ 13 , 14 ]. Primary somatosensory cortex (S1) plays a crucial role in the perception and discrimination of somatosensory information, including touch, itch, and pain [ 15 - 17 ]. Recent studies have shown that S1 encodes the sub-modality of somatic sensations using multiplexed strategies [ 18 , 19 ].…”

Section: Introductionmentioning

confidence: 99%

Multiplexed Representation of Itch and Pain and Their Interaction in the Primary Somatosensory Cortex

et al. 2022

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Itch and pain are distinct sensations that share anatomically similar pathways: from the periphery to the brain. Over the last decades, several itchspecific neural pathways and molecular markers have been identified at the peripheral and spinal cord levels. Although the perception of sensation is ultimately generated at the brain level, how the brain separately processes the signals is unclear. The primary somatosensory cortex (S1) plays a crucial role in the perception of somatosensory information, including touch, itch, and pain. In this study, we investigated how S1 neurons represent itch and pain differently. First, we established a spontaneous itch and pain mouse model. Spontaneous itch or pain was induced by intradermal treatment with 5-HT or capsaicin on the lateral neck and confirmed by a selective increase in scratching or wiping-like behavior, respectively. Next, in vivo two-photon calcium imaging was performed in awake mice after four different treatments, including 5-HT, capsaicin, and each vehicle. By comparing the calcium activity acquired during different sessions, we distinguished the cells responsive to itch or pain sensations. Of the total responsive cells, 11% were both responsive, and their activity in the pain session was slightly higher than that in the itch session. Itch-and painpreferred cells accounted for 28.4% and 60.6%, respectively, and the preferred cells showed the lowest activity in their counter sessions. Therefore, our results suggest that S1 uses a multiplexed coding strategy to encode itch and pain, and S1 neurons represent the interaction between itch and pain.

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The Anterior Insula and its Projection to the Prelimbic Cortex are Involved in the Regulation of 5-HT-Induced Itch

Yao

et al. 2023

Neurosci. Bull.

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Itch is an unpleasant sensation that urges people and animals to scratch. Neuroimaging studies on itch have yielded extensive correlations with diverse cortical and subcortical regions, including the insular lobe. However, the role and functional specificity of the insular cortex (IC) and its subdivisions in itch mediation remains unclear. Here, we demonstrated by immunohistochemistry and fiber photometry tests, that neurons in both the anterior insular cortex (AIC) and the posterior insular cortex (PIC) are activated during acute itch processes. Pharmacogenetic experiments revealed that nonselective inhibition of global AIC neurons, or selective inhibition of the activity of glutaminergic neurons in the AIC, reduced the scratching behaviors induced by intradermal injection of 5-hydroxytryptamine (5-HT), but not those induced by compound 48/80. However, both nonselective inhibition of global PIC neurons and selective inhibition of glutaminergic neurons in the PIC failed to affect the itching-scratching behaviors induced by either 5-HT or compound 48/80. In addition, pharmacogenetic inhibition of AIC glutaminergic neurons effectively blocked itch-associated conditioned place aversion behavior, and inhibition of AIC glutaminergic neurons projecting to the prelimbic cortex significantly suppressed 5-HT-evoked scratching. These findings provide preliminary evidence that the AIC is involved, at least partially via aversive emotion mediation, in the regulation of 5-HT-, but not compound 48/80-induced itch.

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Itch perception is reflected by neuronal ignition in the primary somatosensory cortex

Cited by 7 publications

References 50 publications

Distinct Roles of Dopamine Receptor Subtypes in the Nucleus Accumbens during Itch Signal Processing

Distinct Roles of Dopamine Receptor Subtypes in the Nucleus Accumbens during Itch Signal Processing

Multiplexed Representation of Itch and Pain and Their Interaction in the Primary Somatosensory Cortex

The Anterior Insula and its Projection to the Prelimbic Cortex are Involved in the Regulation of 5-HT-Induced Itch

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