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

• Published in: Neuron (Cambridge, Mass.) Mass.), 2015-06, Vol.86 (6), p.1491-1503
• Main Authors: Duan, Chunyu A., Erlich, Jeffrey C., Brody, Carlos D.
• Format: Article
• Language: English
• Subjects: Analysis of Variance; Animal cognition; Animals; Attention - physiology; Behavior; Brain Mapping; Executive Function - drug effects; Executive Function - physiology; Functional Laterality - drug effects; Functional Laterality - physiology; GABA Agonists - pharmacology; Inhibition (Psychology); Learning - drug effects; Learning - physiology; Male; Multitasking; Muscimol - pharmacology; Orientation - drug effects; Orientation - physiology; Prefrontal Cortex - drug effects; Prefrontal Cortex - physiology; Primates; Rats; Rats, Long-Evans; Reaction Time - drug effects; Superior Colliculi - drug effects; Superior Colliculi - physiology
• ISSN: 0896-6273; 1097-4199
• DOI: 10.1016/j.neuron.2015.05.042

To study rapid sensorimotor remapping, we developed a method to train rats in a behavior in which subjects are cued, on each trial, to apply a sensorimotor association to orient either toward a visual target (“Pro”) or away from it, toward its reverse (“Anti”). Multiple behavioral asymmetries suggested that Anti behavior is cognitively demanding while Pro is easier to learn and perform. This is consistent with a prominent hypothesis in the primate literature that Anti requires prefrontal cortex (PFC), whereas Pro could be mediated by midbrain superior colliculus (SC). Pharmacological inactivation of rat medial PFC supported its expected role in Anti. Remarkably, bilateral SC inactivation substantially impaired Anti while leaving Pro essentially intact. Moreover, SC inactivation eliminated the performance cost of switching from Anti to Pro tasks. Our results establish a rodent model of single-trial sensorimotor remapping and suggest a critical role for SC in the cognitively demanding Anti task. •To study executive control in the rat, we use a novel rapid sensorimotor remapping behavior•Rats switch rapidly between tasks with opposite sensorimotor mappings•Inactivation of SC or PFC selectively disrupts a cognitively demanding task•Inactivating the circuit for one task eliminates the cost of switching out of it Flexible task switching is an executive function predominantly studied in primates and putatively mediated by prefrontal cortex. Duan et al. developed a novel rapid task-switching paradigm in the rat and revealed a more diffuse network underlying executive control, including the midbrain superior colliculus.