A Cholinergic Mechanism for Reward Timing within Primary Visual Cortex

• Published in: Neuron (Cambridge, Mass.) Mass.), 2013-02, Vol.77 (4), p.723-735
• Main Authors: Chubykin, Alexander A., Roach, Emma B., Bear, Mark F., Shuler, Marshall G. Hussain
• Format: Article
• Language: English
• Subjects: Acetylcholine - metabolism; Acetylcholine receptors (muscarinic); Acquisitions & mergers; Action Potentials - physiology; Animals; Behavior; Cholinergic Agents - metabolism; Experiments; Learning - physiology; Male; Neuronal Plasticity - physiology; Neurons; Neurons - metabolism; Population; Rats; Rats, Long-Evans; Reinforcement, Psychology; Reward; Rodents; Singers; Time Factors; Visual Cortex - metabolism
• ISSN: 0896-6273; 1097-4199
• DOI: 10.1016/j.neuron.2012.12.039

Neurons in rodent primary visual cortex (V1) relate operantly conditioned stimulus-reward intervals with modulated patterns of spiking output, but little is known about the locus or mechanism of this plasticity. Here we show that cholinergic basal forebrain projections to V1 are necessary for the neural acquisition, but not the expression, of reward timing in the visual cortex of awake, behaving animals. We then mimic reward timing in vitro by pairing white matter stimulation with muscarinic receptor activation at a fixed interval and show that this protocol results in the prolongation of electrically evoked spike train durations out to the conditioned interval. Together, these data suggest that V1 possesses the circuitry and plasticity to support reward time prediction learning and the cholinergic system serves as an important reinforcement signal which, in vivo, conveys to the cortex the outcome of behavior. ► V1 neurons report stimulus-reward intervals after operant conditioning ► Cholinergic input is required to learn, but not express, reward timing in V1 ► Response duration plasticity is induced in V1 slices by timed delivery of carbachol ► V1 contains the circuitry and mechanisms required for learning reward timing When a light flash predicts delayed reward, visual cortical responses are transformed to encode the cue-reward interval. Chubykin et al. show that the neural mechanism underlying reward timing requires acetylcholine and occurs locally within the primary visual cortex.