Post-error recruitment of frontal sensory cortical projections promotes attention in mice

Kevin J Norman; Justin S Riceberg; Hiroyuki Koike; Julia Bateh; Sarah E McCraney; Keaven Caro; Daisuke Kato; Ana Liang; Kazuhiko Yamamuro; Meghan E Flanigan; Korey Kam; Elisa N Falk; Daniel M Brady; Christina Cho; Masato Sadahiro; Kohei Yoshitake; Priscilla Maccario; Michael P Demars; Leah Waltrip; Andrew W Varga; Scott J Russo; Mark G Baxter; Matthew L Shapiro; Peter H Rudebeck; Hirofumi Morishita

doi:10.1016/j.neuron.2021.02.001

Post-error recruitment of frontal sensory cortical projections promotes attention in mice

Neuron. 2021 Apr 7;109(7):1202-1213.e5. doi: 10.1016/j.neuron.2021.02.001. Epub 2021 Feb 19.

Authors

Kevin J Norman¹, Justin S Riceberg², Hiroyuki Koike¹, Julia Bateh¹, Sarah E McCraney¹, Keaven Caro¹, Daisuke Kato¹, Ana Liang¹, Kazuhiko Yamamuro¹, Meghan E Flanigan³, Korey Kam⁴, Elisa N Falk¹, Daniel M Brady¹, Christina Cho¹, Masato Sadahiro¹, Kohei Yoshitake¹, Priscilla Maccario¹, Michael P Demars¹, Leah Waltrip¹, Andrew W Varga⁴, Scott J Russo³, Mark G Baxter⁵, Matthew L Shapiro⁶, Peter H Rudebeck⁷, Hirofumi Morishita⁸

Affiliations

¹ Department of Psychiatry, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA; Department of Neuroscience, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA; Department of Ophthalmology, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA; Mindich Child Health and Development Institute, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA; Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA.
² Department of Psychiatry, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA; Department of Neuroscience, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA; Department of Ophthalmology, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA; Mindich Child Health and Development Institute, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA; Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA; Department of Neuroscience and Experimental Therapeutics, Albany Medical College, 47 New Scotland Avenue, MC-136, Albany, NY 12208, USA.
³ Department of Neuroscience, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA; Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA.
⁴ Mount Sinai Integrative Sleep Center, Division of Pulmonary, Critical Care, and Sleep Medicine, One Gustave L. Levy Place, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
⁵ Department of Neuroscience, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA; Department of Anesthesiology, Perioperative & Pain Medicine, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA; Department of Geriatrics and Palliative Medicine, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA.
⁶ Department of Neuroscience, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA; Department of Neuroscience and Experimental Therapeutics, Albany Medical College, 47 New Scotland Avenue, MC-136, Albany, NY 12208, USA; Department of Geriatrics and Palliative Medicine, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA.
⁷ Department of Psychiatry, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA; Department of Neuroscience, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA.
⁸ Department of Psychiatry, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA; Department of Neuroscience, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA; Department of Ophthalmology, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA; Mindich Child Health and Development Institute, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA; Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA. Electronic address: hirofumi.morishita@mssm.edu.

Abstract

The frontal cortex, especially the anterior cingulate cortex area (ACA), is essential for exerting cognitive control after errors, but the mechanisms that enable modulation of attention to improve performance after errors are poorly understood. Here we demonstrate that during a mouse visual attention task, ACA neurons projecting to the visual cortex (VIS; ACA_VIS neurons) are recruited selectively by recent errors. Optogenetic manipulations of this pathway collectively support the model that rhythmic modulation of ACA_VIS neurons in anticipation of visual stimuli is crucial for adjusting performance following errors. 30-Hz optogenetic stimulation of ACA_VIS neurons in anesthetized mice recapitulates the increased gamma and reduced theta VIS oscillatory changes that are associated with endogenous post-error performance during behavior and subsequently increased visually evoked spiking, a hallmark feature of visual attention. This frontal sensory neural circuit links error monitoring with implementing adjustments of attention to guide behavioral adaptation, pointing to a circuit-based mechanism for promoting cognitive control.

Keywords: attention; cognitive control; error monitoring; frontal cortex; frontal sensory cortical projection; top-down; visual cortex.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

MeSH terms

Animals
Attention / physiology*
Behavior, Animal
Electroencephalography
Electrophysiological Phenomena
Frontal Lobe / physiology*
Male
Mice
Mice, Inbred C57BL
Motor Activity / physiology
Neural Pathways / physiology
Neurons / physiology
Optogenetics
Photic Stimulation
Psychomotor Performance / physiology
Reaction Time / physiology
Recruitment, Neurophysiological / physiology*
Somatosensory Cortex / physiology
Visual Cortex / physiology

Abstract

Publication types

MeSH terms

Grants and funding