Department of Otorhinolaryngology, University of Pennsylvania, Philadelphia, Pennsylvania, 19104.
Department of Neuroscience, University of Pennsylvania, Philadelphia, Pennsylvania, 19104.
J Neurosci. 2023 Apr 19;43(16):2885-2906. doi: 10.1523/JNEUROSCI.2444-21.2023. Epub 2023 Mar 21.
In everyday life, we integrate visual and auditory information in routine tasks such as navigation and communication. While concurrent sound can improve visual perception, the neuronal correlates of audiovisual integration are not fully understood. Specifically, it remains unclear whether neuronal firing patters in the primary visual cortex (V1) of awake animals demonstrate similar sound-induced improvement in visual discriminability. Furthermore, presentation of sound is associated with movement in the subjects, but little is understood about whether and how sound-associated movement affects audiovisual integration in V1. Here, we investigated how sound and movement interact to modulate V1 visual responses in awake, head-fixed mice and whether this interaction improves neuronal encoding of the visual stimulus. We presented visual drifting gratings with and without simultaneous auditory white noise to awake mice while recording mouse movement and V1 neuronal activity. Sound modulated activity of 80% of light-responsive neurons, with 95% of neurons increasing activity when the auditory stimulus was present. A generalized linear model (GLM) revealed that sound and movement had distinct and complementary effects of the neuronal visual responses. Furthermore, decoding of the visual stimulus from the neuronal activity was improved with sound, an effect that persisted even when controlling for movement. These results demonstrate that sound and movement modulate visual responses in complementary ways, improving neuronal representation of the visual stimulus. This study clarifies the role of movement as a potential confound in neuronal audiovisual responses and expands our knowledge of how multimodal processing is mediated at a neuronal level in the awake brain. Sound and movement are both known to modulate visual responses in the primary visual cortex; however, sound-induced movement has largely remained unaccounted for as a potential confound in audiovisual studies in awake animals. Here, authors found that sound and movement both modulate visual responses in an important visual brain area, the primary visual cortex, in distinct, yet complementary ways. Furthermore, sound improved encoding of the visual stimulus even when accounting for movement. This study reconciles contrasting theories on the mechanism underlying audiovisual integration and asserts the primary visual cortex as a key brain region participating in tripartite sensory interactions.
在日常生活中,我们在导航和交流等常规任务中整合视觉和听觉信息。虽然同时出现的声音可以提高视觉感知,但视听整合的神经元相关性尚不完全清楚。具体来说,目前尚不清楚清醒动物初级视觉皮层 (V1) 的神经元放电模式是否表现出类似的声音引起的视觉可分辨性提高。此外,声音的呈现伴随着主体的运动,但对于声音相关的运动是否以及如何影响 V1 中的视听整合知之甚少。在这里,我们研究了声音和运动如何相互作用来调节清醒、头部固定的小鼠 V1 中的视觉反应,以及这种相互作用是否改善了视觉刺激的神经元编码。我们在清醒小鼠中同时呈现视觉漂移光栅和听觉白噪声,同时记录小鼠运动和 V1 神经元活动。声音调制了 80%的光响应神经元的活动,当听觉刺激存在时,95%的神经元增加了活动。广义线性模型 (GLM) 显示,声音和运动对神经元视觉反应有明显不同且互补的影响。此外,通过声音,从神经元活动中解码视觉刺激得到了改善,即使在控制运动的情况下,这种效果仍然存在。这些结果表明,声音和运动以互补的方式调节视觉反应,从而改善了视觉刺激的神经元表示。这项研究阐明了运动作为潜在混杂因素在清醒动物的神经元视听反应中的作用,并扩展了我们对多模态处理如何在清醒大脑中的神经元水平上进行介导的认识。声音和运动都已知会调节初级视觉皮层中的视觉反应;然而,在清醒动物的视听研究中,声音引起的运动在很大程度上仍未被视为潜在的混杂因素。在这里,作者发现声音和运动以不同但互补的方式调节重要视觉脑区——初级视觉皮层中的视觉反应。此外,即使考虑到运动,声音也能改善视觉刺激的编码。这项研究调和了关于视听整合机制的对立理论,并断言初级视觉皮层是参与三分感官相互作用的关键大脑区域。