The cellular coding of temperature in the mammalian cortex

被引:24
作者
Vestergaard, M. [1 ,2 ]
Carta, M. [1 ,2 ,3 ]
Gueney, G. [1 ,2 ,4 ]
Poulet, J. F. A. [1 ,2 ]
机构
[1] Max Delbruck Ctr Mol Med Helmholtz Assoc MDC, Berlin, Germany
[2] Charite Univ Med Berlin, Neurosci Res Ctr, Berlin, Germany
[3] Univ Bordeaux, CNRS, IINS, UMR 5297, Bordeaux, France
[4] Humboldt Univ, Inst Biol, Berlin, Germany
关键词
RESPONSE CHARACTERISTICS; INSULAR CORTEX; INNERVATING PALMAR; DIGITAL SKIN; NEURONS; COLD; REPRESENTATION; MONKEY; TASTE; PAIN;
D O I
10.1038/s41586-023-05705-5
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
Temperature is a fundamental sensory modality separate from touch, with dedicated receptor channels and primary afferent neurons for cool and warm(1-3). 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 debated(4-8). 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.
引用
收藏
页码:725 / +
页数:24
相关论文
共 50 条
[1]   Spinothalamic lamina I neurones selectively responsive to cutaneous warming in cats [J].
Andrew, D ;
Craig, AD .
JOURNAL OF PHYSIOLOGY-LONDON, 2001, 537 (02) :489-495
[2]   TrpM8-mediated somatosensation in mouse neocortex [J].
Beukema, Patrick ;
Cecil, Katherine L. ;
Peterson, Elena ;
Mann, Victor R. ;
Matsushita, Megumi ;
Takashima, Yoshio ;
Navlakha, Saket ;
Barth, Alison L. .
JOURNAL OF COMPARATIVE NEUROLOGY, 2018, 526 (09) :1444-1456
[3]   Isolated insular infarction eliminates contralateral cold, cold pain, and pinprick perception [J].
Birklein, F ;
Rolke, R ;
Müller-Forell, W .
NEUROLOGY, 2005, 65 (09) :1381-1381
[4]  
Blix Magnus., 1882, Uppsala Lakfor. Forh, P87
[5]   Brain-wide connectivity map of mouse thermosensory cortices [J].
Bokiniec, Phillip ;
Whitmire, Clarissa J. ;
Leva, Tobias M. ;
Poulet, James F. A. .
CEREBRAL CORTEX, 2023, 33 (08) :4870-4885
[6]   The neural circuits of thermal perception [J].
Bokiniec, Phillip ;
Zampieri, Niccolo ;
Lewin, Gary R. ;
Poulet, James F. A. .
CURRENT OPINION IN NEUROBIOLOGY, 2018, 52 :98-106
[7]  
Chen K, 2021, CURR BIOL, V31, P247, DOI [10.1016/j.cub.2020.10.014, 10.1016/j.cub.2020.11.038]
[8]   Ultrasensitive fluorescent proteins for imaging neuronal activity [J].
Chen, Tsai-Wen ;
Wardill, Trevor J. ;
Sun, Yi ;
Pulver, Stefan R. ;
Renninger, Sabine L. ;
Baohan, Amy ;
Schreiter, Eric R. ;
Kerr, Rex A. ;
Orger, Michael B. ;
Jayaraman, Vivek ;
Looger, Loren L. ;
Svoboda, Karel ;
Kim, Douglas S. .
NATURE, 2013, 499 (7458) :295-+
[9]   Multiplexed Representation of Itch and Mechanical and Thermal Sensation in the Primary Somatosensory Cortex [J].
Chen, Xiao-Jun ;
Liu, Yan-He ;
Xu, Ning-Long ;
Sun, Yan-Gang .
JOURNAL OF NEUROSCIENCE, 2021, 41 (50) :10330-10340
[10]   A Gustotopic Map of Taste Qualities in the Mammalian Brain [J].
Chen, Xiaoke ;
Gabitto, Mariano ;
Peng, Yueqing ;
Ryba, Nicholas J. P. ;
Zuker, Charles S. .
SCIENCE, 2011, 333 (6047) :1262-1266