Requirement of Prefrontal and Midbrain Regions for Rapid Executive Control of Behavior in the Rat.

Chunyu A. Duan, Jeffrey C. Erlich, and Carlos D. Brody, Neuron 2015

Neuron also published a preview on this paper.

first-author Ann Duan

Executive control, defined by flexible and rapid sensorimotor routing in response to changing environmental demands, is a fundamental aspect of adaptive behavior. This remarkable cognitive ability is predominantly studied in primates and has been hypothesized to be mediated by the prefrontal cortex (PFC).

In this paper, we establish a novel rapid task-switching paradigm in the rat to study fast executive control via reversible inactivations of the underlying neural circuit. This new behavioral paradigm is closely parallel to comparable primate tasks in its structure, its timing, and its cued single-trial, seconds-timescale sensorimotor remapping. The resulting rat behavior demonstrates numerous parallels to that of primates, suggesting that mechanisms underlying rapid sensorimotor remapping may be comparable across species.

Using this paradigm, we find that fast executive control is not a uniquely cortical function. Based on past literature, we expect the PFC and the midbrain superior colliculus (SC), a structure traditionally associated with stimulus-driven motor functions, to play opposite roles during the cognitively demanding task. In contrast, bilateral inactivation results reveal that both the PFC and the SC are causally required for fast executive control. Our data suggest a more diffuse network underlying response inhibition and flexible task-switching, including the PFC and the SC.

We also provide the first causal evidence for the the task-set inertia theory of switch cost, in that disrupting the cognitively demanding task set eliminates the cost of switching out of this task but leaves the cost of switching into this task intact, linking switch cost to the temporal carryover of the previous task set. The source of task switch cost is the focus of a large executive control literature in humans. Our inactivation data further support the importance of a rodent executive control paradigm to complement primate models of task switch cost.