An inferior-superior colliculus circuit controls auditory cue-directed visual spatial attention

Fei Hu and Yang Dan

Neuron (2021.10)

doi: 10.1016/j.neuron.2021.10.004

Neuron是一个专业的脑科学的顶级杂志，我们来看一下面向专业读者和面向大众读者的杂志（比如Nature, Science, 2021-12-30科学论文写作案例分析之三——科学论文其实是新时代的“八股文” - 简书 (jianshu.com)）行文风格有何不同。

SUMMARY

Selective attention modulates neuronal activity in multiple brain regions, but the origins of attention signals remain unclear （直接提出具体问题）. We show that, during a visual task requiring spatial attention directed by an auditory cue, an inferior-superior colliculus circuit provides the key attention signal （概述本研究的主要发现）. In mice performing a task based on a visual stimulus in the cued hemifield while ignoring a conflicting stimulus on the uncued side, the visual cortex (V1) and superior colliculus (SC) showed strong attentional modulation, with a shorter latency in the SC（发现1）. The nucleus of the brachium of the inferior colliculus (nBIC), which provides auditory inputs to the SC, was activated not only at auditory cue onset but also during the delay period before the visual stimulus（发现2）. The delay activity, but not cue onset activity, was crucial for task performance and attentional modulation in the SC and V1（发现3）. These results establish a new behavioral paradigm for studying visual attention in mice and identify a midbrain signal controlling auditory cue-directed spatial attention （结论）.

相比于昨天分析的那篇面向大众读者的论文（2021-12-30科学论文写作案例分析之三——科学论文其实是新时代的“八股文” - 简书 (jianshu.com)），这篇论文开局没有尝试去画一个大的图景，而是直入主题，直接提出Challenge。属于CAR结构。如果不是脑科学研究人员，只怕不能轻易看懂。

INTRODUCTION

Visual spatial attention allows an animal to select the input at a specific location to guide behavior while ignoring stimuli in other regions of the visual field（开局依然是直入主题）. Neurons in multiple visual cortex areas exhibit enhanced responses to the attended stimuli (Desimone and Duncan, 1995; Maunsell, 2015; Reynolds and Heeger, 2009), and the brain network directing spatial attention has been under active investigation. In addition to several prefrontal and parietal cortical areas (Bisley and Goldberg, 2010; Kastner and Ungerleider, 2000; Miller and Cohen, 2001; Moore and Zirnsak, 2017; Petersen and Posner, 2012), the superior colliculus (SC) in the midbrain also plays an important role in controlling spatial attention (Basso and May, 2017; Knudsen, 2018; Krauzlis et al., 2013)（用3句话引出SC脑区）. In primates, microstimulation (Cavanaugh and Wurtz, 2004; Gattass and Desimone, 2014; Muller et al., 2005) or pharmacological inactivation (Bollimunta et al., 2018; Ze´ non and Krauzlis, 2012) of SC neurons strongly affects visually guided behavior. Recent optogenetic experiments in mice showed that activation of SC neurons improved visual performance and enhanced visual cortex responses, whereas SC inactivation had the opposite effects (Hu et al., 2019; Wanget al., 2020).

In addition to studies based on activity manipulation, recordings from SC neurons have revealed attentional modulation of their firing rates. In primates, neurons in the SC superficial layers show stronger responses to a stimulus when it is the target for an impending saccade (Goldberg and Wurtz,1972 ). Firing rate modulation by covert attention, in which the monkey attends to a certain location without making a detectable eye movement, has also been observed in superficial and intermediate layers (Gattass and Desimone, 1996; Herman and Krauzlis, 2017; Ignashchenkova et al., 2004). A recent study in mice has shown attentional modulation in SC intermediate and deep layers as well (Wang et al., 2021) （用6句话介绍以往关于SC对于spatial attention调节的研究，从猴子到小鼠，从因果性到相关性）. Although these studies have demonstrated the prevalence of firing rate modulation in the SC, the origin of attention signals during these tasks remains poorly understood （介绍已知，提出未知/问题）. This is partly due to the difficulty of dissecting neural circuits in primates and the scarcity of behavioral paradigms for studying visual attention in mice（提出回答该问题所面临的困难）.

In this study, we developed a visual spatial attention task for head-fixed mice in which the Go or No-go behavioral response is instructed by a visual stimulus in the cued hemifield while a conflicting stimulus on the uncued side must be ignored. Single-unit recordings showed strong attentional modulation in the visual cortex (V1) and motor layers of the SC (SCm), with the effect appearing earlier in the SCm. The nucleus of the brachium of the inferior colliculus (nBIC), which provides the main source of auditory inputs to the SCm, was activated not only following onset of the auditory attention cue but also during the delay period before the visual stimulus; this nBIC activity was transmitted faithfully to the SCm. Optogenetic activation and inactivation experiments showed that the delay activity was crucial for task performance of the mice and attentional modulation of SCm and V1 neurons. These results identify a midbrain circuit as the key source of attention signal in auditory cuedirected visual spatial attention（介绍实验内容，发现，得出结论）. 

相比于昨天介绍的Science论文，这一篇面向专业读者的论文写作风格明显要更加的专业，直接，基本上使用的都是领域里的行话。不过，依然可以清晰地看出由背景介绍——发现未知，提出问题——实验，结果，结论，这一个大的写作框架。

我们再来看看丹扬老师是如何写Discussion的。

DISCUSSION

Using a new visual spatial attention task for head-fixed mice (Figure 1), we have shown strong attentional modulation of V1 and SCm neurons (Figures 2 and 3). As the main source of auditory input to the SCm, nBIC neurons were activated following auditory cue onset and during the pre-visual delay period, but only the delay-period activity showed a strong contralateral bias (Figure 4). Optogenetic activation and inactivation experiments showed that the delay-period activity, but not the cue-onset activity, was crucial for task performance and attentional modulation of SCm and V1 neurons (Figures 5, 6, and 7). （首先总结主要发现）

Although mice are a powerful animal model for dissecting neuronal circuits underlying various behaviors, their cognitive capability for selective attention was demonstrated only recently (Li et al., 2021; Schmitt et al., 2017; Speed et al., 2020; Wang and Krauzlis, 2018 ; Wimmer et al., 2015; You and Mysore, 2020). Attentional modulation of V1 responses has been characterized extensively in primates (Desimone and Duncan, 1995; Maunsell,2015; Reynolds and Heeger, 2009) and reported recently in mice (Speed et al., 2020), but how the modulatory signals are generated in the attention network remains poorly understood (Knudsen, 2018)（Opening, 指出大的认知空白）. Unlike previous studies of mouse spatial attention, in which the locus of attention remained constant across tens of trials in each block (Speed et al., 2020; Wang and Krauzlis, 2018; You and Mysore, 2020), in our study, the task-relevant hemifield varied randomly on a trial-by-trial basis. This ensured that only the auditory cue, but not recent trial history, is informative of the location of a behaviorally relevant visual stimulus, narrowing down potential sources of attention signals（突出指出本研究所用行为范式的独特之处，似乎意图强调其新意）. Previous studies of automatic capture of visual spatial attention by salient environmental stimuli (Posner and Cohen, 1984) have shown that the behavioral improvement and increased SC firing rate induced by a preceding visual cue are limited to a less than 100-ms cue-target interval, whereas an auditory cue evoked little attentional modulation (Bell et al., 2004; Fecteau et al., 2004). In our study, the auditory cue caused strong attentional modulation of V1 and SCm neurons even though it was terminated 500 ms before onset of the visual stimulus, suggesting that the task depends on endogenous rather than exogenous attention（讨论自己的研究和以往研究的不同之处，并提出可能的解释）. nBIC neuron activity during the delay period, but not following auditory cue onset, plays a critical role in task performance and neuronal response modulation in the SCm and V1 (Figures 5, 6, and 7), suggesting involvement of working memory, known to be linked closely to attention (Awh and Jonides, 2001; Desimone and Duncan, 1995; Kastner and Ungerleider, 2000; Panichello and Buschman, 2021)（解释性讨论）. As demonstrated by previous optogenetic experiments, SCm neuron activity can powerfully regulate V1 responses in the same hemisphere (Hu et al., 2019). Our observation that some SCm neurons faithfully inherit the activity from auditory neurons in the nBIC (Figures 3 and 4) points to a simple mechanism for generating attention signals from sensory neuron activity（此处作者在做从“知识——理解”的讨论，2021-12-10科学写作的成败在于能否讲好一个故事 - 简书 (jianshu.com)）. Neurons in the SCm are known to receive inputs from multiple sources (Basso and May, 2017), including V1 and SC superficial layers signaling salient visual stimuli for bottom-up attention (Knudsen, 2018), frontal cortical areas providing task-related top-down instructions (Hu et al., 2019), and subcortical neurons carrying sensory signals from other modalities (Basso and May, 2017; Bedna´ rova´ et al., 2018). Although the task used in the current study strongly engages the nBIC, natural visual behaviors are likely to involve additional inputs. SCm neurons, in turn, direct spatial attention with or without detectable eye- or body-orienting movement (Ignashchenkova et al., 2004; Kustov and Robinson,1996). Thus, the SCm provides a critical hub that integrates attention cues from multiple sensory modalities with behavioral context to control overt and covert visual spatial attention（最后3句是开放性讨论，作者尝试放大这项研究发现的意义）.

这个讨论写得还是挺中规中矩的，基本上是紧密地围绕具体的研究发现展开，没有做太多发散性的讨论。而且讨论都是紧紧地围绕以往的研究，非专业读者只怕很难从中获得阅读的快感。

意外的是，记得几年前问过attention领域的资深研究人员Desimone一个问题，即大脑通过产生top-down的attention signal调节感觉皮层的反应，那么所谓的top attentional signal是如何产生的呢？这项研究似乎部分地回答了这个问题，即attentional signal也可以通过bottom-up的方式从感觉皮层产生。