Webb James, Steffan Paul, Hayden Benjamin Y, Lee Daeyeol, Kemere Caleb, McGinley Matthew
Department of Neuroscience, Baylor College of Medicine, Houston, Texas, United States of America.
Jan and Dan Duncan Neurological Research Institute, Texas Children's Hospital, Houston, Texas, United States of America.
PLoS Comput Biol. 2025 Apr 30;21(4):e1012989. doi: 10.1371/journal.pcbi.1012989. eCollection 2025 Apr.
Foraging theory predicts animal behavior in many contexts. In patch-based foraging behaviors, the marginal value theorem (MVT) gives the optimal strategy for deterministic environments whose parameters are fully known to the forager. In natural settings, environmental parameters exhibit variability and are only partially known to the animal based on its experience, creating uncertainty. Models of uncertainty in foraging are well established. However, natural environments also exhibit unpredicted changes in their statistics. As a result, animals must ascertain whether the currently observed quality of the environment is consistent with their internal models, or whether something has changed, creating meta-uncertainty. Behavioral strategies for optimizing foraging behavior under meta-uncertainty, and their neural underpinnings, are largely unknown. Here, we developed a novel behavioral task and computational framework for studying patch-leaving decisions in head-fixed and freely moving mice in conditions of meta-uncertainty. We stochastically varied between-patch travel time, as well as within-patch reward depletion rate. We find that, when uncertainty is minimal, mice adopt patch residence times in a manner consistent with the MVT and not explainable by simple ethologically motivated heuristic strategies. However, behavior in highly variable environments was best explained by modeling both first- and second-order uncertainty in environmental parameters, wherein local variability and global statistics are captured by a Bayesian estimator and dynamic prior, respectively. Thus, mice forage under meta-uncertainty by employing a hierarchical Bayesian strategy, which is essential for efficiently foraging in volatile environments. The results provide a foundation for understanding the neural basis of decision-making that exhibits naturalistic meta-uncertainty.
觅食理论在许多情况下预测动物行为。在基于斑块的觅食行为中,边际价值定理(MVT)给出了确定性环境中的最优策略,其参数对于觅食者来说是完全已知的。在自然环境中,环境参数具有变异性,动物仅根据自身经验部分了解这些参数,从而产生不确定性。觅食中的不确定性模型已得到充分确立。然而,自然环境在其统计数据方面也表现出不可预测的变化。因此,动物必须确定当前观察到的环境质量是否与它们的内部模型一致,或者是否发生了某些变化,从而产生元不确定性。在元不确定性下优化觅食行为的行为策略及其神经基础在很大程度上尚不清楚。在这里,我们开发了一种新颖的行为任务和计算框架,用于研究在元不确定性条件下头固定和自由移动的小鼠的斑块离开决策。我们随机改变斑块间的旅行时间以及斑块内奖励消耗率。我们发现,当不确定性最小时,小鼠采用的斑块停留时间与MVT一致,并且不能用简单的基于行为学动机的启发式策略来解释。然而,在高度可变环境中的行为最好通过对环境参数的一阶和二阶不确定性进行建模来解释,其中局部变异性和全局统计数据分别由贝叶斯估计器和动态先验来捕捉。因此,小鼠通过采用分层贝叶斯策略在元不确定性下觅食,这对于在多变环境中高效觅食至关重要。这些结果为理解表现出自然主义元不确定性的决策的神经基础提供了基础。