Katz Leor N, Bohlen Martin O, Yu Gongchen, Mejias-Aponte Carlos, Sommer Marc A, Krauzlis Richard J
National Eye Institute.
Duke University.
J Cogn Neurosci. 2025 Feb 1;37(2):266-285. doi: 10.1162/jocn_a_02274.
Optogenetics affords new opportunities to interrogate neuronal circuits that control behavior. In primates, the usefulness of optogenetics in studying cognitive functions remains a challenge. The technique has been successfully wielded, but behavioral effects have been demonstrated primarily for sensorimotor processes. Here, we tested whether brief optogenetic suppression of primate superior colliculus can change performance in a covert attention task, in addition to previously reported optogenetic effects on saccadic eye movements. We used an attention task that required the monkey to detect and report a stimulus change at a cued location via joystick release, while ignoring changes at an uncued location. When the cued location was positioned in the response fields of transduced neurons in the superior colliculus, transient light delivery coincident with the stimulus change disrupted the monkey's detection performance, significantly lowering hit rates. When the cued location was elsewhere, hit rates were unaltered, indicating that the effect was spatially specific and not a motor deficit. Hit rates for trials with only one stimulus were also unaltered, indicating that the effect depended on selection among distractors rather than a low-level visual impairment. Psychophysical analysis revealed that optogenetic suppression increased perceptual threshold, but only for locations matching the transduced site. These data show that optogenetic manipulations can cause brief and spatially specific deficits in covert attention, independent of sensorimotor functions. This dissociation of effect, and the temporal precision provided by the technique, demonstrates the utility of optogenetics in interrogating neuronal circuits that mediate cognitive functions in the primate.
光遗传学为研究控制行为的神经回路提供了新机会。在灵长类动物中，光遗传学在研究认知功能方面的实用性仍然是一个挑战。该技术已得到成功应用，但行为效应主要在感觉运动过程中得到了证实。在此，我们测试了除了先前报道的光遗传学对眼球扫视运动的影响外，短暂光遗传学抑制灵长类动物上丘是否会改变隐蔽注意任务中的表现。我们使用了一项注意任务，要求猴子通过释放操纵杆来检测并报告提示位置处的刺激变化，同时忽略未提示位置处的变化。当提示位置位于上丘中转导神经元的反应野内时，与刺激变化同时进行的短暂光刺激会干扰猴子的检测表现，显著降低命中率。当提示位置在其他地方时，命中率没有改变，这表明该效应具有空间特异性，而非运动缺陷。仅呈现一个刺激的试验的命中率也没有改变，这表明该效应取决于在干扰物之间进行选择，而非低级视觉损伤。心理物理学分析表明，光遗传学抑制增加了感知阈值，但仅针对与转导部位匹配的位置。这些数据表明，光遗传学操作可在隐蔽注意中导致短暂且具有空间特异性的缺陷，与感觉运动功能无关。这种效应的分离以及该技术所提供的时间精度，证明了光遗传学在研究介导灵长类动物认知功能的神经回路方面的实用性。
