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

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. VargaScott J. Russo, Mark G. Baxter, Matthew L. Shapiro, Peter H. Rudebeck, Hirofumi Morishita

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32 Scopus citations

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.

Original language	English
Pages (from-to)	1202-1213.e5
Journal	Neuron
Volume	109
Issue number	7
DOIs	https://doi.org/10.1016/j.neuron.2021.02.001
State	Published - 7 Apr 2021

Keywords

attention
cognitive control
error monitoring
frontal cortex
frontal sensory cortical projection
top-down
visual cortex

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10.1016/j.neuron.2021.02.001

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Norman, K. J., Riceberg, J. S., Koike, H., Bateh, J., McCraney, S. E., Caro, K., Kato, D., Liang, A., Yamamuro, K., Flanigan, M. E., Kam, K., Falk, E. N., Brady, D. M., Cho, C., Sadahiro, M., Yoshitake, K., Maccario, P., Demars, M. P., Waltrip, L., ... Morishita, H. (2021). Post-error recruitment of frontal sensory cortical projections promotes attention in mice. Neuron, 109(7), 1202-1213.e5. https://doi.org/10.1016/j.neuron.2021.02.001

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title = "Post-error recruitment of frontal sensory cortical projections promotes attention in mice",

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; ACAVIS neurons) are recruited selectively by recent errors. Optogenetic manipulations of this pathway collectively support the model that rhythmic modulation of ACAVIS neurons in anticipation of visual stimuli is crucial for adjusting performance following errors. 30-Hz optogenetic stimulation of ACAVIS 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",

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

note = "Publisher Copyright: {\textcopyright} 2021 Elsevier Inc.",

year = "2021",

month = apr,

day = "7",

doi = "10.1016/j.neuron.2021.02.001",

language = "English",

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Norman, KJ, Riceberg, JS, Koike, H, Bateh, J, McCraney, SE, Caro, K, Kato, D, Liang, A, Yamamuro, K, Flanigan, ME, Kam, K, Falk, EN, Brady, DM, Cho, C, Sadahiro, M, Yoshitake, K, Maccario, P, Demars, MP, Waltrip, L, Varga, AW , Russo, SJ, Baxter, MG, Shapiro, ML , Rudebeck, PH & Morishita, H 2021, 'Post-error recruitment of frontal sensory cortical projections promotes attention in mice', Neuron, vol. 109, no. 7, pp. 1202-1213.e5. https://doi.org/10.1016/j.neuron.2021.02.001

TY - JOUR

T1 - Post-error recruitment of frontal sensory cortical projections promotes attention in mice

AU - Norman, Kevin J.

AU - Riceberg, Justin S.

AU - Koike, Hiroyuki

AU - Bateh, Julia

AU - McCraney, Sarah E.

AU - Caro, Keaven

AU - Kato, Daisuke

AU - Liang, Ana

AU - Yamamuro, Kazuhiko

AU - Flanigan, Meghan E.

AU - Kam, Korey

AU - Falk, Elisa N.

AU - Brady, Daniel M.

AU - Cho, Christina

AU - Sadahiro, Masato

AU - Yoshitake, Kohei

AU - Maccario, Priscilla

AU - Demars, Michael P.

AU - Waltrip, Leah

AU - Varga, Andrew W.

AU - Russo, Scott J.

AU - Baxter, Mark G.

AU - Shapiro, Matthew L.

AU - Rudebeck, Peter H.

AU - Morishita, Hirofumi

PY - 2021/4/7

Y1 - 2021/4/7

N2 - 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; ACAVIS neurons) are recruited selectively by recent errors. Optogenetic manipulations of this pathway collectively support the model that rhythmic modulation of ACAVIS neurons in anticipation of visual stimuli is crucial for adjusting performance following errors. 30-Hz optogenetic stimulation of ACAVIS 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.

AB - 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; ACAVIS neurons) are recruited selectively by recent errors. Optogenetic manipulations of this pathway collectively support the model that rhythmic modulation of ACAVIS neurons in anticipation of visual stimuli is crucial for adjusting performance following errors. 30-Hz optogenetic stimulation of ACAVIS 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.

KW - attention

KW - cognitive control

KW - error monitoring

KW - frontal cortex

KW - frontal sensory cortical projection

KW - top-down

KW - visual cortex

UR - http://www.scopus.com/inward/record.url?scp=85103267743&partnerID=8YFLogxK

U2 - 10.1016/j.neuron.2021.02.001

DO - 10.1016/j.neuron.2021.02.001

M3 - Article

C2 - 33609483

AN - SCOPUS:85103267743

SN - 0896-6273

VL - 109

SP - 1202-1213.e5

JO - Neuron

JF - Neuron

IS - 7

ER -

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

Abstract

Keywords

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