Gated feedforward inhibition in the frontal cortex releases goal-directed action

• Published in: Nature neuroscience Vol. 24; no. 10; pp. 1452 - 1464
• Main Authors: Kim, Jae-Hyun, Ma, Dong-Hyun, Jung, Eunji, Choi, Ilsong, Lee, Seung-Hee
• Format: Journal Article
• Language: English
• Published: New York Nature Publishing Group US 01.10.2021; Nature Publishing Group
• Subjects: 13; 13/51; 14; 14/34; 42; 42/35; 631/378/2629/1409; 631/378/3920; 64; 64/60; Analysis; Animal Genetics and Genomics; Animals; Behavioral Sciences; Biological Techniques; Biomedical and Life Sciences; Biomedicine; Circuits; Cortex (cingulate); Cortex (frontal); Cortex (motor); Cortex (somatosensory); Feedback, Psychological; Feedforward control systems; Firing pattern; Frontal Lobe - physiology; Go/no-go discrimination learning; Goals; Gyrus Cinguli - physiology; Inhibition, Psychological; Mice; Mice, Inbred C57BL; Motor neurons; Motor Neurons - physiology; Neostriatum; Neostriatum - cytology; Neostriatum - physiology; Nerve Net - physiology; Neurobiology; Neurons; Neurosciences; Optogenetics; Perceptual-motor processes; Prefrontal cortex; Psychomotor Performance - physiology; Reaction Time; Sensorimotor integration; Sensory neurons; Visual pathways; Visual Perception - physiology; Visual tasks; South Korea
• ISSN: 1097-6256; 1546-1726
• DOI: 10.1038/s41593-021-00910-9

Cortical circuits process both sensory and motor information in animals performing perceptual tasks. However, it is still unclear how sensory inputs are transformed into motor signals in the cortex to initiate goal-directed actions. In this study, we found that a visual-to-motor inhibitory circuit in the anterior cingulate cortex (ACC) triggers precise action in mice performing visual Go/No-go tasks. Three distinct features of ACC neurons—visual amplitudes of sensory neurons, suppression times of motor neurons and network activity from other neurons—predicted response times of the mice. Moreover, optogenetic activation of visual inputs in the ACC, which drives fast-spiking sensory neurons, prompted task-relevant actions in mice by suppressing ACC motor neurons and disinhibiting downstream striatal neurons. Notably, when mice terminated actions in response to stop signals, both motor neuron and network activity increased. Collectively, our data demonstrate that visual inputs to the frontal cortex trigger gated feedforward inhibition to initiate goal-directed actions. Kim et al. found that visual inputs trigger gated feedforward inhibition of ACC neurons, which disinhibits striatal motor neurons and initiates precise responses in mice performing a visual Go/No-go task.