Seillier Lenka, Lorenz Corinna, Kawaguchi Katsuhisa, Ott Torben, Nieder Andreas, Pourriahi Paria, Nienborg Hendrikje
Werner Reichardt Centre for Integrative Neuroscience and.
Department of Animal Physiology, Institute of Neurobiology, University of Tübingen, 72076 Tübingen, Germany.
J Neurosci. 2017 Nov 22;37(47):11390-11405. doi: 10.1523/JNEUROSCI.1339-17.2017. Epub 2017 Oct 17.
Serotonin, an important neuromodulator in the brain, is implicated in affective and cognitive functions. However, its role even for basic cortical processes is controversial. For example, in the mammalian primary visual cortex (V1), heterogenous serotonergic modulation has been observed in anesthetized animals. Here, we combined extracellular single-unit recordings with iontophoresis in awake animals. We examined the role of serotonin on well-defined tuning properties (orientation, spatial frequency, contrast, and size) in V1 of two male macaque monkeys. We find that in the awake macaque the modulatory effect of serotonin is surprisingly uniform: it causes a mainly multiplicative decrease of the visual responses and a slight increase in the stimulus-selective response latency. Moreover, serotonin neither systematically changes the selectivity or variability of the response, nor the interneuronal correlation unexplained by the stimulus ("noise-correlation"). The modulation by serotonin has qualitative similarities with that for a decrease in stimulus contrast, but differs quantitatively from decreasing contrast. It can be captured by a simple additive change to a threshold-linear spiking nonlinearity. Together, our results show that serotonin is well suited to control the response gain of neurons in V1 depending on the animal's behavioral or motivational context, complementing other known state-dependent gain-control mechanisms. Serotonin is an important neuromodulator in the brain and a major target for drugs used to treat psychiatric disorders. Nonetheless, surprisingly little is known about how it shapes information processing in sensory areas. Here we examined the serotonergic modulation of visual processing in the primary visual cortex of awake behaving macaque monkeys. We found that serotonin mainly decreased the gain of the visual responses, without systematically changing their selectivity, variability, or covariability. This identifies a simple computational function of serotonin for state-dependent sensory processing, depending on the animal's affective or motivational state.
血清素是大脑中一种重要的神经调质,与情感和认知功能有关。然而,其在基本皮层过程中的作用仍存在争议。例如,在哺乳动物的初级视觉皮层(V1)中,已在麻醉动物中观察到异质性血清素调节。在此,我们将细胞外单单元记录与清醒动物的离子电渗疗法相结合。我们研究了血清素对两只雄性猕猴V1中明确的调谐特性(方向、空间频率、对比度和大小)的作用。我们发现,在清醒的猕猴中,血清素的调节作用惊人地一致:它主要导致视觉反应的乘法性降低以及刺激选择性反应潜伏期的轻微增加。此外,血清素既不会系统性地改变反应的选择性或变异性,也不会改变刺激无法解释的神经元间相关性(“噪声相关性”)。血清素的调节与刺激对比度降低的调节在质量上相似,但在数量上与降低对比度不同。它可以通过对阈值线性脉冲非线性的简单加法变化来捕捉。总之,我们的结果表明,血清素非常适合根据动物的行为或动机背景来控制V1中神经元的反应增益,补充了其他已知的状态依赖性增益控制机制。血清素是大脑中一种重要的神经调质,也是用于治疗精神疾病的药物的主要靶点。尽管如此,令人惊讶的是,关于它如何塑造感觉区域的信息处理,人们知之甚少。在此,我们研究了清醒行为猕猴初级视觉皮层中血清素对视觉处理的调节作用。我们发现,血清素主要降低了视觉反应的增益,而没有系统性地改变其选择性、变异性或协变性。这确定了血清素在依赖状态的感觉处理中的一个简单计算功能,取决于动物的情感或动机状态。