Sustained Attentional States Require Distinct Temporal Involvement of the Dorsal and Ventral Medial Prefrontal Cortex

Antonio Luchicchi, Ouissame Mnie-Filali, Huub Terra, Bastiaan Bruinsma, Sybren F de Kloet, Joshua Obermayer, Tim S Heistek, Roel de Haan, Christiaan P J de Kock, Karl Deisseroth, Tommy Pattij, Huibert D Mansvelder

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

Attending the sensory environment for cue detection is a cognitive operation that occurs on a time scale of seconds. The dorsal and ventral medial prefrontal cortex (mPFC) contribute to separate aspects of attentional processing. Pyramidal neurons in different parts of the mPFC are active during cognitive behavior, yet whether this activity is causally underlying attentional processing is not known. We aimed to determine the precise temporal requirements for activation of the mPFC subregions during the seconds prior to cue detection. To test this, we used optogenetic silencing of dorsal or ventral mPFC pyramidal neurons at defined time windows during a sustained attentional state. We find that the requirement of ventral mPFC pyramidal neuron activity is strictly time-locked to stimulus detection. Inhibiting the ventral mPFC 2 s before or during cue presentation reduces response accuracy and hampers behavioral inhibition. The requirement for dorsal mPFC activity on the other hand is temporally more loosely related to a preparatory attentional state, and short lapses in pyramidal neuron activity in dorsal mPFC do not affect performance. This only occurs when the dorsal mPFC is inhibited during the entire preparatory period. Together, our results reveal that a dissociable temporal recruitment of ventral and dorsal mPFC is required during attentional processing.

Original languageEnglish
Article number70
JournalFrontiers in Neural Circuits
Volume10
DOIs
Publication statusPublished - 31 Aug 2016

Cite this

Luchicchi, Antonio ; Mnie-Filali, Ouissame ; Terra, Huub ; Bruinsma, Bastiaan ; de Kloet, Sybren F ; Obermayer, Joshua ; Heistek, Tim S ; de Haan, Roel ; de Kock, Christiaan P J ; Deisseroth, Karl ; Pattij, Tommy ; Mansvelder, Huibert D. / Sustained Attentional States Require Distinct Temporal Involvement of the Dorsal and Ventral Medial Prefrontal Cortex. In: Frontiers in Neural Circuits. 2016 ; Vol. 10.
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title = "Sustained Attentional States Require Distinct Temporal Involvement of the Dorsal and Ventral Medial Prefrontal Cortex",
abstract = "Attending the sensory environment for cue detection is a cognitive operation that occurs on a time scale of seconds. The dorsal and ventral medial prefrontal cortex (mPFC) contribute to separate aspects of attentional processing. Pyramidal neurons in different parts of the mPFC are active during cognitive behavior, yet whether this activity is causally underlying attentional processing is not known. We aimed to determine the precise temporal requirements for activation of the mPFC subregions during the seconds prior to cue detection. To test this, we used optogenetic silencing of dorsal or ventral mPFC pyramidal neurons at defined time windows during a sustained attentional state. We find that the requirement of ventral mPFC pyramidal neuron activity is strictly time-locked to stimulus detection. Inhibiting the ventral mPFC 2 s before or during cue presentation reduces response accuracy and hampers behavioral inhibition. The requirement for dorsal mPFC activity on the other hand is temporally more loosely related to a preparatory attentional state, and short lapses in pyramidal neuron activity in dorsal mPFC do not affect performance. This only occurs when the dorsal mPFC is inhibited during the entire preparatory period. Together, our results reveal that a dissociable temporal recruitment of ventral and dorsal mPFC is required during attentional processing.",
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author = "Antonio Luchicchi and Ouissame Mnie-Filali and Huub Terra and Bastiaan Bruinsma and {de Kloet}, {Sybren F} and Joshua Obermayer and Heistek, {Tim S} and {de Haan}, Roel and {de Kock}, {Christiaan P J} and Karl Deisseroth and Tommy Pattij and Mansvelder, {Huibert D}",
year = "2016",
month = "8",
day = "31",
doi = "10.3389/fncir.2016.00070",
language = "English",
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journal = "Frontiers in Neural Circuits",
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Luchicchi, A, Mnie-Filali, O, Terra, H, Bruinsma, B, de Kloet, SF, Obermayer, J, Heistek, TS, de Haan, R, de Kock, CPJ, Deisseroth, K, Pattij, T & Mansvelder, HD 2016, 'Sustained Attentional States Require Distinct Temporal Involvement of the Dorsal and Ventral Medial Prefrontal Cortex' Frontiers in Neural Circuits, vol. 10, 70. https://doi.org/10.3389/fncir.2016.00070

Sustained Attentional States Require Distinct Temporal Involvement of the Dorsal and Ventral Medial Prefrontal Cortex. / Luchicchi, Antonio; Mnie-Filali, Ouissame; Terra, Huub; Bruinsma, Bastiaan; de Kloet, Sybren F; Obermayer, Joshua; Heistek, Tim S; de Haan, Roel; de Kock, Christiaan P J; Deisseroth, Karl; Pattij, Tommy; Mansvelder, Huibert D.

In: Frontiers in Neural Circuits, Vol. 10, 70, 31.08.2016.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Sustained Attentional States Require Distinct Temporal Involvement of the Dorsal and Ventral Medial Prefrontal Cortex

AU - Luchicchi, Antonio

AU - Mnie-Filali, Ouissame

AU - Terra, Huub

AU - Bruinsma, Bastiaan

AU - de Kloet, Sybren F

AU - Obermayer, Joshua

AU - Heistek, Tim S

AU - de Haan, Roel

AU - de Kock, Christiaan P J

AU - Deisseroth, Karl

AU - Pattij, Tommy

AU - Mansvelder, Huibert D

PY - 2016/8/31

Y1 - 2016/8/31

N2 - Attending the sensory environment for cue detection is a cognitive operation that occurs on a time scale of seconds. The dorsal and ventral medial prefrontal cortex (mPFC) contribute to separate aspects of attentional processing. Pyramidal neurons in different parts of the mPFC are active during cognitive behavior, yet whether this activity is causally underlying attentional processing is not known. We aimed to determine the precise temporal requirements for activation of the mPFC subregions during the seconds prior to cue detection. To test this, we used optogenetic silencing of dorsal or ventral mPFC pyramidal neurons at defined time windows during a sustained attentional state. We find that the requirement of ventral mPFC pyramidal neuron activity is strictly time-locked to stimulus detection. Inhibiting the ventral mPFC 2 s before or during cue presentation reduces response accuracy and hampers behavioral inhibition. The requirement for dorsal mPFC activity on the other hand is temporally more loosely related to a preparatory attentional state, and short lapses in pyramidal neuron activity in dorsal mPFC do not affect performance. This only occurs when the dorsal mPFC is inhibited during the entire preparatory period. Together, our results reveal that a dissociable temporal recruitment of ventral and dorsal mPFC is required during attentional processing.

AB - Attending the sensory environment for cue detection is a cognitive operation that occurs on a time scale of seconds. The dorsal and ventral medial prefrontal cortex (mPFC) contribute to separate aspects of attentional processing. Pyramidal neurons in different parts of the mPFC are active during cognitive behavior, yet whether this activity is causally underlying attentional processing is not known. We aimed to determine the precise temporal requirements for activation of the mPFC subregions during the seconds prior to cue detection. To test this, we used optogenetic silencing of dorsal or ventral mPFC pyramidal neurons at defined time windows during a sustained attentional state. We find that the requirement of ventral mPFC pyramidal neuron activity is strictly time-locked to stimulus detection. Inhibiting the ventral mPFC 2 s before or during cue presentation reduces response accuracy and hampers behavioral inhibition. The requirement for dorsal mPFC activity on the other hand is temporally more loosely related to a preparatory attentional state, and short lapses in pyramidal neuron activity in dorsal mPFC do not affect performance. This only occurs when the dorsal mPFC is inhibited during the entire preparatory period. Together, our results reveal that a dissociable temporal recruitment of ventral and dorsal mPFC is required during attentional processing.

KW - Animals

KW - Attention

KW - Behavior, Animal

KW - Male

KW - Optogenetics

KW - Prefrontal Cortex

KW - Pyramidal Cells

KW - Rats

KW - Rats, Long-Evans

KW - Journal Article

KW - Research Support, Non-U.S. Gov't

U2 - 10.3389/fncir.2016.00070

DO - 10.3389/fncir.2016.00070

M3 - Article

VL - 10

JO - Frontiers in Neural Circuits

JF - Frontiers in Neural Circuits

SN - 1662-5110

M1 - 70

ER -