Multiplexed Representation of Itch and Mechanical and Thermal Sensation in the Primary Somatosensory Cortex

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

doi:10.1523/jneurosci.1445-21.2021

Cited by 18 publications

(10 citation statements)

References 51 publications

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“…d , Bar graph showing the percentage of pIC and S1 neurons responding to thermal only and also to tactile stimulation (pIC, 506 neurons thermal only, 18 neurons thermal and tactile; S1, 345 neurons thermal only, 49 neurons thermal and tactile). The overall number and proportion of thermal and tactile neurons in S1 presented here differs from a previous report 50 . This might depend on the body part studied, stimulus design and recording conditions.…”

Section: Extended Data Figures and Tablescontrasting

confidence: 99%

The cellular coding of temperature in the mammalian cortex

Vestergaard

Carta

Güney

et al. 2023

Nature

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Temperature is a fundamental sensory modality separate from touch, with dedicated receptor channels and primary afferent neurons for cool and warm1–3. Unlike for other modalities, however, the cortical encoding of temperature remains unknown, with very few cortical neurons reported that respond to non-painful temperature, and the presence of a ‘thermal cortex’ is debated4–8. Here, using widefield and two-photon calcium imaging in the mouse forepaw system, we identify cortical neurons that respond to cooling and/or warming with distinct spatial and temporal response properties. We observed a representation of cool, but not warm, in the primary somatosensory cortex, but cool and warm in the posterior insular cortex (pIC). The representation of thermal information in pIC is robust and somatotopically arranged, and reversible manipulations show a profound impact on thermal perception. Despite being positioned along the same one-dimensional sensory axis, the encoding of cool and that of warm are distinct, both in highly and broadly tuned neurons. Together, our results show that pIC contains the primary cortical representation of skin temperature and may help explain how the thermal system generates sensations of cool and warm.

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Section: Extended Data Figures and Tablescontrasting

confidence: 99%

The cellular coding of temperature in the mammalian cortex

Vestergaard

Carta

Güney

et al. 2023

Nature

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“…The coding strategy explains that the sensory system processes distinct sensations by both specific cell populations and converged cell populations [ 19 , 33 ]. These coding strategies were found at the supraspinal level, including S1 [ 18 , 19 , 34 ]. When we classified the preferred cells, we disregarded the activities of counter pair.…”

Section: Resultsmentioning

confidence: 99%

“…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 ]. In other reports, the activation of the S1 layer 5 neurons projecting to the spinal cord decreased itch; meanwhile, activation of these neurons could facilitate mechanical allodynia.…”

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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“…Moreover, a substantial proportion of itch-responsive neurons showed progressively increased activity after scratching onset, suggesting that these itch-responsive neurons also responded to other somatosensory inputs associated with the scratching behavior [ 9 , 28 ]. Moreover, S1 could also adopt a population coding mechanism to selectively process itch information as suggested by a recent study [ 46 ]. Due to the close relationship between itch and pain, it is interesting to examine whether these two submodalities could activate distinct neuron populations in S1, and further experiments are warranted to directly test this.…”

Section: Discussionmentioning

confidence: 99%

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

Chen

Liu

et al. 2021

National Science Review

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Multiple cortical areas including primary somatosensory cortex (S1) are activated during itch signal processing, yet cortical representation of itch perception remains unknown. Using a novel miniature two-photon microscopic imaging in free-moving mice, we investigated the coding of itch perception in S1. We found that pharmacological inactivation of S1 abolished itch-induced scratching behavior, and the itch-induced scratching behavior could be well predicted by the activity of a fraction of layer 2/3 pyramidal neurons, suggesting that a subpopulation of S1 pyramidal neurons encoded itch perception, as indicated by immediate subsequent scratching behaviors. With a newly-established optogenetics-based paradigm that allows precisely-controlled pruritic stimulation, we found that a small fraction of S1 neurons exhibited ignition-like pattern at the detection threshold of itch perception. Our study revealed the neural mechanism underlying itch perceptual coding in S1, thus paving the way for studying cortical representation of itch perception at the single-neuron level in freely moving animals.

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Multiplexed Representation of Itch and Mechanical and Thermal Sensation in the Primary Somatosensory Cortex

Cited by 18 publications

References 51 publications

The cellular coding of temperature in the mammalian cortex

The cellular coding of temperature in the mammalian cortex

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

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

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