Destrebecq Virginie, Rovai Antonin, Trotta Nicola, de Tiège Xavier, Naeije Gilles
Department of Neurology, CUB Hôpital Erasme, Hôpital Universitaire de Bruxelles (H.U.B.), Université Libre de Bruxelles (ULB), Brussels, Belgium.
Laboratoire de Neuroanatomie et Neuroimagerie translationnelles (LN T), UNI - ULB Neuroscience Institute, Université Libre de Bruxelles (ULB), Brussels, Belgium.
Imaging Neurosci (Camb). 2025 Jun 4;3. doi: 10.1162/imag_a_00572. eCollection 2025.
According to the predictive coding theory, the brain predicts future sensory inputs based on previous experiences. When there is a mismatch between the expected and the actual stimulus, a mismatch response is transmitted from low to high cortical levels to adapt the predictive model. An important cortical area for somatosensory mismatch responses is the secondary somatosensory (S2) cortex, which has reciprocal connections with the cerebellum. This study aims to characterize the role of the cortico-cerebellar interactions in the modulation of S2 cortex responses according to the predictability of afferent tactile and proprioceptive somatosensory inputs. We enrolled 20 right-handed healthy adults who underwent three functional magnetic resonance imaging (fMRI) runs (6 min each, block-design) consisting of twelve 30-s alternating blocks (10 brain volumes/block, 120 brain volumes/session) of tactile oddball paradigms. The fMRI signals within the contralateral S1 (cS1), ipsilateral S2 (iS2), and contralateral S2 (cS2) cortices; within the cortical areas involved in multimodal sensory mismatch detection (i.e., the right anterior insula (AIns), temporoparietal junction (TPJ), middle frontal gyrus (MFG), and supplementary motor are/anterior cingular cortex (SMA/ACC)); and within the ipsilateral cerebellar lobule 8 (iCL8) and 6 (iCL6) were extracted using region-of-interest (ROI) analyses and compared using ANOVA. The modulation of cortico-cerebellar functional connectivity by afferent stimuli predictability was studied using psychophysiological interaction (PPI) analyses. Predictable tactile stimuli were associated with significantly lower fMRI signals within cS1 and bilateral S2 cortices, and the right AIns, TPJ, and MFG compared to random tactile stimuli. PPI analyses showed that predictable tactile stimuli were associated with a significant increase in the functional connectivity (negative correlation) between cS2 cortex and iCL8 BOLD levels, with no significant correlation during random tactile stimulation. This effect, identified by the PPI analyses, occurred solely between the cerebellum and cS2 cortex and not with the other cortical mismatch areas. This study provides evidence for a cerebello-cortical interplay between iCL8 and the cS2 cortex in tactile somatosensory mismatch responses. The lower BOLD response in the S2 cortex observed for predictable tactile stimuli is likely mediated by an inhibitory influence of the cerebellum on the somatosensory cortex when tactile inputs are predictable.
根据预测编码理论，大脑基于先前的经验预测未来的感觉输入。当预期刺激与实际刺激之间存在不匹配时，不匹配反应会从低级皮质水平传递到高级皮质水平，以调整预测模型。躯体感觉不匹配反应的一个重要皮质区域是次级躯体感觉（S2）皮质，它与小脑有相互连接。本研究旨在根据传入触觉和本体感觉躯体感觉输入的可预测性，描述皮质-小脑相互作用在调节S2皮质反应中的作用。我们招募了20名右利手健康成年人，他们接受了三次功能磁共振成像（fMRI）扫描（每次6分钟，组块设计），包括12个30秒的交替组块（每个组块10个脑容积，每次扫描120个脑容积）的触觉oddball范式。使用感兴趣区域（ROI）分析提取对侧S1（cS1）、同侧S2（iS2）和对侧S2（cS2）皮质内；参与多模态感觉不匹配检测的皮质区域（即右侧前脑岛（AIns）、颞顶交界区（TPJ）、额中回（MFG）和辅助运动区/前扣带回皮质（SMA/ACC））内；以及同侧小脑小叶8（iCL8）和6（iCL6）内的fMRI信号，并使用方差分析进行比较。使用心理生理相互作用（PPI）分析研究传入刺激可预测性对皮质-小脑功能连接的调节作用。与随机触觉刺激相比，可预测的触觉刺激与cS1、双侧S2皮质以及右侧AIns、TPJ和MFG内的fMRI信号显著降低有关。PPI分析表明，可预测的触觉刺激与cS2皮质和iCL8血氧水平依赖（BOLD）信号之间的功能连接显著增加（负相关），在随机触觉刺激期间无显著相关性。PPI分析确定的这种效应仅发生在小脑和cS2皮质之间，与其他皮质不匹配区域无关。本研究为iCL8和cS2皮质在触觉躯体感觉不匹配反应中的小脑-皮质相互作用提供了证据。当触觉输入可预测时，在S2皮质中观察到的可预测触觉刺激的较低BOLD反应可能是由小脑对躯体感觉皮质的抑制作用介导的。
