Synaptic Dysfunction in the Anterior Cingulate Cortex Underlies Pain‐Anxiety Comorbidity in a Mandibular Asymmetry Mouse Model
Structural craniofacial abnormalities, particularly mandibular asymmetry (MA), are increasingly recognized as key drivers of orofacial pain and emotional comorbidities, although the underlying neural mechanisms remain unclear. This study aims to develop a preclinical MA model to investigate the dynamic interplay between craniofacial structural defects and neurobehavioral dysfunction. Longitudinal behavioral phenotyping including von Frey filaments test as well as open field and elevated plus maze tests reveals progressive sensory hypersensitivity and anxiety-like behaviors, with computational ethology revealing subtle but consistent alterations in the naturalistic behaviors. Whole-brain activity mapping reveal hyperactivation in the anterior cingulate cortex (ACC), whereas multi-omics profiling reveal cell type-specific transcriptional changes and synaptic reorganization within this region. Functional investigation including sparse labeling, electrophysiology, western blotting, and chemogenetics demonstrate that the ACC modulation regulated both pain and anxiety. These findings establish a causal association between structural craniofacial defects and maladaptive neural circuit remodeling, with the ACC emerging as a critical therapeutic target. The study provides a comprehensive framework for understanding how anatomical abnormalities translate into persistent neurological dysfunction and offers new avenues for mechanistically informed intervention.
Authors
- Haoxiang Xiao (ORCID: https://orcid.org/0000-0003-4948-6139)
- Zuolin Jin (ORCID: https://orcid.org/0000-0002-8342-9886)
- Jialin Si
- Zhaoyichun Zhang (ORCID: https://orcid.org/0000-0002-0972-2566)
- Shiquan Sun (ORCID: https://orcid.org/0000-0002-9150-6992)
- Xiaohua Chen
- Jin Ning (ORCID: https://orcid.org/0000-0002-8551-7038)
- Yanran Zhang (ORCID: https://orcid.org/0000-0001-7001-8079)
- Yuanyuan Zhu
- Guaiguai Ma
- Honghui Mao (ORCID: https://orcid.org/0000-0002-5625-3715)
- Meng Nian (ORCID: https://orcid.org/0009-0007-1159-4974)
- Haifeng Zhang (ORCID: https://orcid.org/0000-0003-0227-9861)
- Jing Huang (ORCID: https://orcid.org/0000-0003-0697-4968)
- Shengxi Wu (ORCID: https://orcid.org/0000-0002-3210-9567)
- Shibin Yu (ORCID: https://orcid.org/0000-0001-8428-1249)
- Yifan Lu (ORCID: https://orcid.org/0000-0003-4461-0698)
- Qian Liu (ORCID: https://orcid.org/0000-0002-7858-7089)
- Feng He
- Ze Fan
Institutions
- National Clinical Research (US)
- Xi'an Jiaotong University (CN)
- Air Force Medical University (CN)
Publication Details
- Journal
- Advanced Science
- Published
- 2025-09-24
- DOI
- https://doi.org/10.1002/advs.202509509
- Citations
- 1
- Primary Topic
- Pain Mechanisms and Treatments
- Type
- article
- Field-Weighted Citation Impact
- 1.16
Funders
- National Natural Science Foundation of China
- Fourth Military Medical University