The propensity of animals to shift choices immediately after unexpectedly poor reinforcement outcomes is a pervasive strategy across species and tasks. We report here on the memory supporting such lose-shift responding in humans, assessed using a binary choice task in which random responding is the optimal strategy. Participants exhibited little lose-shift responding when fully attending to the task, but this increased by 30%–40% in participants that performed with additional cognitive load that is known to tax executive systems. Lose-shift responding in the cognitively loaded adults persisted throughout the testing session, despite being a sub-optimal strategy, but was less likely as the time increased between reinforcement and the subsequent choice. Furthermore, children (5–9 years old) without load performed similarly to the cognitively loaded adults. This effect disappeared in older children aged 11–13 years old. These data provide evidence supporting our hypothesis that lose-shift responding is a default and reflexive strategy in the mammalian brain, likely mediated by a decaying memory trace, and is normally suppressed by executive systems. Reducing the efficacy of executive control by cognitive load (adults) or underdevelopment (children) increases its prevalence. It may therefore be an important component to consider when interpreting choice data, and may serve as an objective behavioral assay of executive function in humans that is easy to measure.

Observations of neurons in a resting brain and neurons in cultures often display spontaneous scale-free (SF) collective dynamics in the form of information cascades, also called ‘neuronal avalanches’. This has motivated the so called critical brain hypothesis which posits that the brain is self-tuned to a critical point or regime, separating exponentially-growing dynamics from quiescent states, to achieve optimality. Yet, how such optimality of information transmission is related to behavior and whether it persists under behavioral transitions has remained a fundamental knowledge gap. Here, we aim to tackle this challenge by studying behavioral transitions in mice using two-photon calcium imaging of the retrosplenial cortex (RSC)—an area of the brain well positioned to integrate sensory, mnemonic, and cognitive information by virtue of its strong connectivity with the hippocampus, medial prefrontal cortex, and primary sensory cortices. Our work shows that the response of the underlying neural population to behavioral transitions can vary significantly between different sub-populations such that one needs to take the structural and functional network properties of these sub-populations into account to understand the properties at the total population level. Specifically, we show that the RSC contains at least one sub-population capable of switching between two different SF regimes, indicating an intricate relationship between behavior and the optimality of neuronal response at the subgroup level. This asks for a potential reinterpretation of the emergence of self-organized criticality in neuronal systems.

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