Brain and Mind Institute, Western University, London, Ontario, N6A 3K7, Canada
Brain and Mind Institute, Western University, London, Ontario, N6A 3K7, Canada.
J Neurosci. 2022 Jun 29;42(26):5173-5185. doi: 10.1523/JNEUROSCI.2152-21.2022. Epub 2022 May 23.
The integration of somatosensory signals across fingers is essential for dexterous object manipulation. Previous experiments suggest that this integration occurs in neural populations in the primary somatosensory cortex (S1). However, the integration process has not been fully characterized, as previous studies have mainly used 2-finger stimulation paradigms. Here, we addressed this gap by stimulating all 31 single- and multifinger combinations. We measured population-wide activity patterns evoked during finger stimulation in human S1 and primary motor cortex (M1) using 7T fMRI in female and male participants. Using multivariate fMRI analyses, we found clear evidence of unique nonlinear interactions between fingers. In Brodmann area (BA) 3b, interactions predominantly occurred between pairs of neighboring fingers. In BA 2, however, we found equally strong interactions between spatially distant fingers, as well as interactions between finger triplets and quadruplets. We additionally observed strong interactions in the hand area of M1. In both M1 and S1, these nonlinear interactions did not reflect a general suppression of overall activity, suggesting instead that the interactions we observed reflect rich, nonlinear integration of sensory inputs from the fingers. We suggest that this nonlinear finger integration allows for a highly flexible mapping from finger sensory inputs to motor responses that facilitates dexterous object manipulation. Processing of somatosensory information in primary somatosensory cortex (S1) is essential for dexterous object manipulation. To successfully handle an object, the sensorimotor system needs to detect complex patterns of haptic information, which requires the nonlinear integration of sensory inputs across multiple fingers. Using multivariate fMRI analyses, we characterized brain activity patterns evoked by stimulating all single- and multifinger combinations. We report that progressively stronger multifinger interactions emerge in posterior S1 and in the primary motor cortex (M1), with interactions arising between inputs from neighboring and spatially distant fingers. Our results suggest that S1 and M1 provide the neural substrate necessary to support a flexible mapping from sensory inputs to motor responses of the hand.
感觉信号在手指间的整合对于灵巧的物体操作至关重要。先前的实验表明,这种整合发生在初级体感皮层(S1)的神经群体中。然而,由于先前的研究主要使用 2 指刺激范式,因此尚未完全描述整合过程。在这里,我们通过刺激所有 31 个单指和多指组合来解决这一差距。我们使用 7T fMRI 在女性和男性参与者中测量了手指刺激期间在 S1 和初级运动皮层(M1)中引发的全人群活动模式。使用多元 fMRI 分析,我们发现手指之间存在明显的独特非线性相互作用的证据。在 Brodmann 区(BA)3b 中,相互作用主要发生在相邻的两个手指之间。然而,在 BA 2 中,我们发现空间上遥远的手指之间以及手指三指和四指组合之间同样存在强烈的相互作用。我们还观察到 M1 手部区域的强烈相互作用。在 M1 和 S1 中,这些非线性相互作用都没有反映出整体活动的普遍抑制,这表明我们观察到的相互作用反映了来自手指的感觉输入的丰富、非线性整合。我们认为,这种非线性手指整合允许从手指感觉输入到运动反应的高度灵活的映射,从而促进灵巧的物体操作。初级体感皮层(S1)中的体感信息处理对于灵巧的物体操作至关重要。为了成功地处理一个物体,感觉运动系统需要检测复杂的触觉信息模式,这需要多个手指的感觉输入进行非线性整合。我们使用多元 fMRI 分析来描述刺激所有单指和多指组合时引发的大脑活动模式。我们报告说,在后 S1 和初级运动皮层(M1)中出现了逐渐增强的多指相互作用,这些相互作用出现在来自相邻和空间上遥远的手指的输入之间。我们的结果表明,S1 和 M1 提供了支持从感觉输入到手部运动反应的灵活映射的必要神经基础。