Institute of Psychology, Polish Academy of Sciences, Warsaw, 00-378, Poland
Visual & Cognitive Neuroscience Lab, Department of Psychology, University of Fribourg, Fribourg, 1700, Switzerland.
J Neurosci. 2023 Nov 15;43(46):7868-7878. doi: 10.1523/JNEUROSCI.0376-23.2023. Epub 2023 Oct 2.
Motor actions, such as reaching or grasping, can be decoded from fMRI activity of early visual cortex (EVC) in sighted humans. This effect can depend on vision or visual imagery, or alternatively, could be driven by mechanisms independent of visual experience. Here, we show that the actions of reaching in different directions can be reliably decoded from fMRI activity of EVC in congenitally blind humans (both sexes). Thus, neither visual experience nor visual imagery is necessary for EVC to represent action-related information. We also demonstrate that, within EVC of blind humans, the accuracy of reach direction decoding is highest in areas typically representing foveal vision and gradually decreases in areas typically representing peripheral vision. We propose that this might indicate the existence of a predictive, hard-wired mechanism of aligning action and visual spaces. This mechanism might send action-related information primarily to the high-resolution foveal visual areas, which are critical for guiding and online correction of motor actions. Finally, we show that, beyond EVC, the decoding of reach direction in blind humans is most accurate in dorsal stream areas known to be critical for visuo-spatial and visuo-motor integration in the sighted. Thus, these areas can develop space and action representations even in the lifelong absence of vision. Overall, our findings in congenitally blind humans match previous research on the action system in the sighted, and suggest that the development of action representations in the human brain might be largely independent of visual experience. Early visual cortex (EVC) was traditionally thought to process only visual signals from the retina. Recent studies proved this account incomplete, and showed EVC involvement in many activities not directly related to incoming visual information, such as memory, sound, or action processing. Is EVC involved in these activities because of visual imagery? Here, we show robust reach direction representation in EVC of humans born blind. This demonstrates that EVC can represent actions independently of vision and visual imagery. Beyond EVC, we found that reach direction representation in blind humans is strongest in dorsal brain areas, critical for action processing in the sighted. This suggests that the development of action representations in the human brain is largely independent of visual experience.
运动动作,如伸手或抓握,可以从有视力的人的早期视觉皮层(EVC)的 fMRI 活动中解码出来。这种效应可能依赖于视觉或视觉意象,或者也可能由独立于视觉经验的机制驱动。在这里,我们表明,在先天性失明的人中,可以从 EVC 的 fMRI 活动中可靠地解码出不同方向的伸手动作(无论性别)。因此,EVC 代表与动作相关的信息既不需要视觉经验也不需要视觉意象。我们还证明,在盲人群体的 EVC 中,手部运动方向解码的准确性在代表中央凹视觉的区域最高,而在代表周边视觉的区域则逐渐降低。我们提出,这可能表明存在一种预测性的、硬连线的动作与视觉空间对齐机制。这种机制可能会将与动作相关的信息主要发送到高分辨率的中央凹视觉区域,这对于指导和在线纠正运动动作至关重要。最后,我们表明,在 EVC 之外,盲人群体的手部运动方向解码在已知对有视力者的视空间和视动整合至关重要的背侧流区域中最为准确。因此,即使在没有视觉的情况下,这些区域也可以发展出空间和动作的表示。总的来说,我们在先天性失明者中的发现与有视力者的动作系统的先前研究相匹配,并表明人类大脑中动作表示的发展在很大程度上可能独立于视觉经验。早期视觉皮层(EVC)传统上被认为仅处理来自视网膜的视觉信号。最近的研究证明了这种说法不完整,并表明 EVC 参与了许多与传入视觉信息无关的活动,例如记忆、声音或动作处理。EVC 参与这些活动是因为视觉意象吗?在这里,我们表明,在天生失明的人的 EVC 中存在强大的伸手方向表示。这表明 EVC 可以独立于视觉和视觉意象来表示动作。在 EVC 之外,我们发现盲人群体的手部运动方向表示在对有视力者的动作处理至关重要的背侧脑区最强。这表明,人类大脑中动作表示的发展在很大程度上可能独立于视觉经验。