Meijer Guido T, Montijn Jorrit S, Pennartz Cyriel M A, Lansink Carien S
Swammerdam Institute for Life Sciences, Center for Neuroscience, Faculty of Science and.
Research Priority Program Brain and Cognition, University of Amsterdam, 1098XH Amsterdam, The Netherlands.
J Neurosci. 2017 Sep 6;37(36):8783-8796. doi: 10.1523/JNEUROSCI.0468-17.2017. Epub 2017 Aug 8.
The sensory neocortex is a highly connected associative network that integrates information from multiple senses, even at the level of the primary sensory areas. Although a growing body of empirical evidence supports this view, the neural mechanisms of cross-modal integration in primary sensory areas, such as the primary visual cortex (V1), are still largely unknown. Using two-photon calcium imaging in awake mice, we show that the encoding of audiovisual stimuli in V1 neuronal populations is highly dependent on the features of the stimulus constituents. When the visual and auditory stimulus features were modulated at the same rate (i.e., temporally congruent), neurons responded with either an enhancement or suppression compared with unisensory visual stimuli, and their prevalence was balanced. Temporally incongruent tones or white-noise bursts included in audiovisual stimulus pairs resulted in predominant response suppression across the neuronal population. Visual contrast did not influence multisensory processing when the audiovisual stimulus pairs were congruent; however, when white-noise bursts were used, neurons generally showed response suppression when the visual stimulus contrast was high whereas this effect was absent when the visual contrast was low. Furthermore, a small fraction of V1 neurons, predominantly those located near the lateral border of V1, responded to sound alone. These results show that V1 is involved in the encoding of cross-modal interactions in a more versatile way than previously thought. The neural substrate of cross-modal integration is not limited to specialized cortical association areas but extends to primary sensory areas. Using two-photon imaging of large groups of neurons, we show that multisensory modulation of V1 populations is strongly determined by the individual and shared features of cross-modal stimulus constituents, such as contrast, frequency, congruency, and temporal structure. Congruent audiovisual stimulation resulted in a balanced pattern of response enhancement and suppression compared with unisensory visual stimuli, whereas incongruent or dissimilar stimuli at full contrast gave rise to a population dominated by response-suppressing neurons. Our results indicate that V1 dynamically integrates nonvisual sources of information while still attributing most of its resources to coding visual information.
感觉新皮层是一个高度连通的联合网络,它整合来自多种感官的信息,甚至在初级感觉区域层面也是如此。尽管越来越多的实证证据支持这一观点,但初级感觉区域(如初级视觉皮层V1)中跨模态整合的神经机制仍 largely unknown。在清醒小鼠中使用双光子钙成像,我们发现V1神经元群体中视听刺激的编码高度依赖于刺激成分的特征。当视觉和听觉刺激特征以相同速率调制(即时间上一致)时,与单感官视觉刺激相比,神经元的反应表现为增强或抑制,且二者的发生率是平衡的。视听刺激对中包含的时间上不一致的音调或白噪声爆发导致整个神经元群体的主要反应抑制。当视听刺激对一致时,视觉对比度不影响多感官处理;然而,当使用白噪声爆发时,当视觉刺激对比度高时,神经元通常表现出反应抑制,而当视觉对比度低时则没有这种效应。此外,一小部分V1神经元,主要是位于V1外侧边界附近的那些神经元,对单独的声音有反应。这些结果表明,V1参与跨模态相互作用编码的方式比以前认为的更加多样。跨模态整合的神经基础不仅限于专门的皮层联合区域,还延伸到初级感觉区域。通过对大量神经元进行双光子成像,我们发现V1群体的多感官调制在很大程度上由跨模态刺激成分的个体和共同特征决定,如对比度、频率、一致性和时间结构。与单感官视觉刺激相比,一致的视听刺激导致反应增强和抑制的平衡模式,而完全对比度下不一致或不同的刺激导致以反应抑制神经元为主的群体反应。我们的结果表明,V1在动态整合非视觉信息源的同时,仍将其大部分资源用于编码视觉信息。