Department of Integrative Biology and Physiology, Los Angeles, California 90095.
Fuster Laboratory of Cognitive Neuroscience, Department of Psychiatry and Biobehavioral Sciences, Jane and Terry Semel Institute for Neuroscience and Human Behaviour, David Geffen School of Medicine, University of California Los Angeles, Los Angeles, California 90095.
J Neurosci. 2021 Apr 7;41(14):3234-3253. doi: 10.1523/JNEUROSCI.1491-20.2021. Epub 2021 Feb 23.
Popular models of decision-making propose that noisy sensory evidence accumulates until reaching a bound. Behavioral evidence as well as trial-averaged ramping of neuronal activity in sensorimotor regions of the brain support this idea. However, averaging activity across trials can mask other processes, such as rapid shifts in decision commitment, calling into question the hypothesis that evidence accumulation is encoded by delay period activity of individual neurons. We mined two sets of data from experiments in four monkeys in which we recorded from superior colliculus neurons during two different decision-making tasks and a delayed saccade task. We applied second-order statistical measures and spike train simulations to determine whether spiking statistics were similar or different in the different tasks and monkeys, despite similar trial-averaged activity across tasks and monkeys. During a motion direction discrimination task, single-trial delay period activity behaved statistically consistent with accumulation. During an orientation detection task, the activity behaved superficially like accumulation, but statistically consistent with stepping. Simulations confirmed both findings. Importantly, during a simple saccade task, with similar trial-averaged activity, neither process explained spiking activity, ruling out interpretations based on differences in attention, reward, or motor planning. These results highlight the need for exploring single-trial spiking dynamics to understand cognitive processing and raise the interesting hypothesis that the superior colliculus participates in different aspects of decision-making depending on task differences. How are decisions based on sensory information transformed into actions? We report that single-trial neuronal activity dynamics in the superior colliculus of monkeys show differences in decision-making tasks depending on task idiosyncrasies and requirements and despite similar trial-averaged ramping activity. These results highlight the importance of exploring single-trial spiking dynamics to understand cognitive processing and raise the interesting hypothesis that the superior colliculus participates in different aspects of decision-making depending on task requirements.
流行的决策模型提出，嘈杂的感觉证据会累积，直到达到一个界限。行为证据以及大脑感觉运动区域中神经元活动的试验平均加斜率支持了这一观点。然而，跨试验平均活动可以掩盖其他过程，例如决策承诺的快速转变，这使得证据积累是由单个神经元的延迟期活动编码的假设受到质疑。我们从四只猴子的两项实验中挖掘了两组数据，在这两项实验中，我们在两个不同的决策任务和一个延迟扫视任务期间记录了上丘神经元的活动。我们应用二阶统计测量和尖峰火车模拟来确定在不同任务和猴子中，尖峰统计数据是否相似或不同，尽管跨任务和猴子的试验平均活动相似。在运动方向辨别任务中，单试延迟期活动在统计学上表现出与积累一致的行为。在方向检测任务中，活动在表面上表现为积累，但在统计学上与跨步一致。模拟证实了这两种发现。重要的是，在一个简单的扫视任务中，尽管试验平均活动相似，但这两种过程都不能解释尖峰活动，从而排除了基于注意力、奖励或运动计划差异的解释。这些结果强调了需要探索单试尖峰动力学来理解认知处理，并提出了一个有趣的假设，即上丘根据任务差异参与决策的不同方面。基于感觉信息的决策如何转化为行动？我们报告说，猴子上丘的单试神经元活动动力学在决策任务中表现出差异，这取决于任务的特殊性和要求，尽管试验平均加斜率活动相似。这些结果强调了探索单试尖峰动力学以理解认知处理的重要性，并提出了一个有趣的假设，即上丘根据任务要求参与决策的不同方面。
