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Peer-reviewedCC BYPLOS Biology

Distinct millisecond-scale click-train patterns evoke discriminable behavioral and neural responses in humans and rats

  • Yuying Zhai1,2,3,4,5
  • Peirun Song1,2,3
  • Ana Belén Lao-Rodríguez6,7,8
  • Xinyu Du2
  • Haoxuan Xu4,5
  • Hangting Ye2
  • Xuehui Bao4
  • Ishrat Mehmood4
  • Nayaab Shahir Pandit4
  • Cheng Chang2
  • Zhouyou Dai2
  • Zhiyi Tu1
7 more authors
  • Pei Chen1
  • Tingting Zhang1
  • Lingling Zhang1
  • Xuan Zhao1
  • David Pérez-González6,7,9
  • Manuel S Malmierca6,7,8
  • Xiongjie Yu2,3,4,5
9 affiliations
  1. 1Department of Anesthesiology, Shanghai Tenth People's Hospital, Tongji University School of Medicine, Shanghai, China.
  2. 2Department of Anesthesia, Women's Hospital, Zhejiang University School of Medicine, Hangzhou, China.
  3. 3Zhejiang Provincial Key Laboratory of Precision Diagnosis and Therapy for Major Gynecological Diseases, Women's Hospital, Zhejiang University School of Medicine, Hangzhou, China.
  4. 4College of Biomedical Engineering and Instrument Science, Zhejiang University, Hangzhou, China.
  5. 5Key Laboratory for Biomedical Engineering of Ministry of Education, Zhejiang University, Hangzhou, China.
  6. 6Cognitive and Auditory Neuroscience Laboratory (Lab 1), Institute of Neuroscience of Castilla y León (INCYL), University of Salamanca, Salamanca, Spain.
  7. 7Institute for Biomedical Research of Salamanca (IBSAL), University of Salamanca, Salamanca, Spain.
  8. 8Department of Cell Biology and Pathology, Faculty of Medicine, University of Salamanca, Salamanca, Spain.
  9. 9Department of Basic Psychology, Psychobiology and Methodology of Behavioral Sciences, Faculty of Psychology, University of Salamanca, Salamanca, Spain.
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Abstract

Natural sounds are shaped by both spectral content and temporal patterning. Here we ask whether click trains with the same mean inter-click interval, but different millisecond-scale temporal patterns evoke distinct behavioral and neural responses. Human listeners discriminated several such click-train patterns, and human EEG revealed context-dependent deviance-related responses. Awake rats showed analogous cortical response differences at the ECoG level. Along the IC–MGB–A1 pathway, unit recordings revealed weak oddball/context sensitivity in IC, intermediate sensitivity in MGB, and stronger stimulus-specific adaptation in A1. Reversible inactivation of the auditory cortex reduced MGB sensitivity, indicating a contribution of corticothalamic feedback. Further A1 layer analyses showed stronger effects in supragranular than deep cortical layers. Together, these results show that distinct click-train temporal patterns are differentially represented across the auditory system, with stronger sensitivity emerging in higher auditory structures.

Natural sounds contain both spectral and temporal information, but how millisecond-scale temporal patterns are represented across the auditory system is unclear. This study shows that distinct click-train patterns evoke discriminable behavioral and neural responses, with sensitivity increasing from midbrain to cortex and shaped by corticothalamic feedback and cortical hierarchy.

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Cite

BibTeXRIS
BibTeX
@article{zhai2026distinct,
  title = {{Distinct millisecond-scale click-train patterns evoke discriminable behavioral and neural responses in humans and rats}},
  author = {Yuying Zhai and Peirun Song and Ana Belén Lao-Rodríguez and Xinyu Du and Haoxuan Xu and Hangting Ye and Xuehui Bao and Ishrat Mehmood and Nayaab Shahir Pandit and Cheng Chang and Zhouyou Dai and Zhiyi Tu and Pei Chen and Tingting Zhang and Lingling Zhang and Xuan Zhao and David Pérez-González and Manuel S Malmierca and Xiongjie Yu},
  journal = {PLOS Biology},
  year = {2026},
  month = oct,
  doi = {10.1371/journal.pbio.3004046},
  url = {https://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.3004046},
  note = {CC BY},
}
RIS
TY  - JOUR
TI  - Distinct millisecond-scale click-train patterns evoke discriminable behavioral and neural responses in humans and rats
AU  - Yuying Zhai
AU  - Peirun Song
AU  - Ana Belén Lao-Rodríguez
AU  - Xinyu Du
AU  - Haoxuan Xu
AU  - Hangting Ye
AU  - Xuehui Bao
AU  - Ishrat Mehmood
AU  - Nayaab Shahir Pandit
AU  - Cheng Chang
AU  - Zhouyou Dai
AU  - Zhiyi Tu
AU  - Pei Chen
AU  - Tingting Zhang
AU  - Lingling Zhang
AU  - Xuan Zhao
AU  - David Pérez-González
AU  - Manuel S Malmierca
AU  - Xiongjie Yu
PY  - 2026
DA  - 2026/10/08
JO  - PLOS Biology
DO  - 10.1371/journal.pbio.3004046
UR  - https://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.3004046
AB  - Natural sounds are shaped by both spectral content and temporal patterning. Here we ask whether click trains with the same mean inter-click interval, but different millisecond-scale temporal patterns evoke distinct behavioral and neural responses. Human listeners discriminated several such click-train patterns, and human EEG revealed context-dependent deviance-related responses. Awake rats showed analogous cortical response differences at the ECoG level. Along the IC–MGB–A1 pathway, unit recordings revealed weak oddball/context sensitivity in IC, intermediate sensitivity in MGB, and stronger stimulus-specific adaptation in A1. Reversible inactivation of the auditory cortex reduced MGB sensitivity, indicating a contribution of corticothalamic feedback. Further A1 layer analyses showed stronger effects in supragranular than deep cortical layers. Together, these results show that distinct click-train temporal patterns are differentially represented across the auditory system, with stronger sensitivity emerging in higher auditory structures.  Natural sounds contain both spectral and temporal information, but how millisecond-scale temporal patterns are represented across the auditory system is unclear. This study shows that distinct click-train patterns evoke discriminable behavioral and neural responses, with sensitivity increasing from midbrain to cortex and shaped by corticothalamic feedback and cortical hierarchy.
SN  - 1545-7885
SN  - 1544-9173
ER  -