Prefrontal cortical ChAT-VIP interneurons provide local excitation by cholinergic synaptic transmission and control attention

Joshua Obermayer; Antonio Luchicchi; Tim S Heistek; Sybren F de Kloet; Huub Terra; Bastiaan Bruinsma; Ouissame Mnie-Filali; Christian Kortleven; Anna A Galakhova; Ayoub J Khalil; Tim Kroon; Allert J Jonker; Roel de Haan; Wilma D J van den Berg; Natalia A Goriounova; Christiaan P J de Kock; Tommy Pattij; Huibert D Mansvelder

doi:10.1038/s41467-019-13244-9

Prefrontal cortical ChAT-VIP interneurons provide local excitation by cholinergic synaptic transmission and control attention

Joshua Obermayer
, Antonio Luchicchi
, Tim S Heistek
, Sybren F de Kloet
, Huub Terra
, Bastiaan Bruinsma
, Ouissame Mnie-Filali
, Christian Kortleven
, Anna A Galakhova
, Ayoub J Khalil
, Tim Kroon
, Allert J Jonker
, Roel de Haan
, Wilma D J van den Berg
, Natalia A Goriounova
, Christiaan P J de Kock
, Tommy Pattij
, Huibert D Mansvelder

Department of Integrative Neurophysiology, Center for Neurogenomics and Cognitive Research (CNCR), Vrije Universiteit, Amsterdam Neuroscience, The Netherlands.
MRC Centre-Developmental Neurobiology, King's College London, London, UK.
Department of Anatomy and Neurosciences, Amsterdam Neuroscience, Amsterdam UMC, Vrije Universiteit Amsterdam, Amsterdam, the Netherlands.
Department of Integrative Neurophysiology, Center for Neurogenomics and Cognitive Research (CNCR), Vrije Universiteit, Amsterdam Neuroscience, The Netherlands. [email protected].

Research output: Contribution to journal › Article › Academic › peer-review

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Abstract

Neocortical choline acetyltransferase (ChAT)-expressing interneurons are a subclass of vasoactive intestinal peptide (ChAT-VIP) neurons of which circuit and behavioural function are unknown. Here, we show that ChAT-VIP neurons directly excite neighbouring neurons in several layers through fast synaptic transmission of acetylcholine (ACh) in rodent medial prefrontal cortex (mPFC). Both interneurons in layers (L)1-3 as well as pyramidal neurons in L2/3 and L6 receive direct inputs from ChAT-VIP neurons mediated by fast cholinergic transmission. A fraction (10-20%) of postsynaptic neurons that received cholinergic input from ChAT-VIP interneurons also received GABAergic input from these neurons. In contrast to regular VIP interneurons, ChAT-VIP neurons did not disinhibit pyramidal neurons. Finally, we show that activity of these neurons is relevant for behaviour and they control attention behaviour distinctly from basal forebrain ACh inputs. Thus, ChAT-VIP neurons are a local source of cortical ACh that directly excite neurons throughout cortical layers and contribute to attention.

Original language	English
Pages (from-to)	5280
Journal	Nature communications
Volume	10
Issue number	1
DOIs	https://doi.org/10.1038/s41467-019-13244-9
Publication status	Published - 21 Nov 2019

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Obermayer, J., Luchicchi, A., Heistek, T. S., de Kloet, S. F., Terra, H., Bruinsma, B., Mnie-Filali, O., Kortleven, C., Galakhova, A. A., Khalil, A. J., Kroon, T., Jonker, A. J., de Haan, R., van den Berg, W. D. J., Goriounova, N. A., de Kock, C. P. J., Pattij, T., & Mansvelder, H. D. (2019). Prefrontal cortical ChAT-VIP interneurons provide local excitation by cholinergic synaptic transmission and control attention. Nature communications, 10(1), 5280. https://doi.org/10.1038/s41467-019-13244-9

@article{00d1c78216714826b789d0bd27985ff9,

title = "Prefrontal cortical ChAT-VIP interneurons provide local excitation by cholinergic synaptic transmission and control attention",

abstract = "Neocortical choline acetyltransferase (ChAT)-expressing interneurons are a subclass of vasoactive intestinal peptide (ChAT-VIP) neurons of which circuit and behavioural function are unknown. Here, we show that ChAT-VIP neurons directly excite neighbouring neurons in several layers through fast synaptic transmission of acetylcholine (ACh) in rodent medial prefrontal cortex (mPFC). Both interneurons in layers (L)1-3 as well as pyramidal neurons in L2/3 and L6 receive direct inputs from ChAT-VIP neurons mediated by fast cholinergic transmission. A fraction (10-20\%) of postsynaptic neurons that received cholinergic input from ChAT-VIP interneurons also received GABAergic input from these neurons. In contrast to regular VIP interneurons, ChAT-VIP neurons did not disinhibit pyramidal neurons. Finally, we show that activity of these neurons is relevant for behaviour and they control attention behaviour distinctly from basal forebrain ACh inputs. Thus, ChAT-VIP neurons are a local source of cortical ACh that directly excite neurons throughout cortical layers and contribute to attention.",

author = "Joshua Obermayer and Antonio Luchicchi and Heistek, \{Tim S\} and \{de Kloet\}, \{Sybren F\} and Huub Terra and Bastiaan Bruinsma and Ouissame Mnie-Filali and Christian Kortleven and Galakhova, \{Anna A\} and Khalil, \{Ayoub J\} and Tim Kroon and Jonker, \{Allert J\} and \{de Haan\}, Roel and \{van den Berg\}, \{Wilma D J\} and Goriounova, \{Natalia A\} and \{de Kock\}, \{Christiaan P J\} and Tommy Pattij and Mansvelder, \{Huibert D\}",

year = "2019",

month = nov,

day = "21",

doi = "10.1038/s41467-019-13244-9",

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Obermayer, J, Luchicchi, A, Heistek, TS, de Kloet, SF, Terra, H, Bruinsma, B, Mnie-Filali, O, Kortleven, C, Galakhova, AA, Khalil, AJ, Kroon, T, Jonker, AJ, de Haan, R, van den Berg, WDJ, Goriounova, NA, de Kock, CPJ, Pattij, T & Mansvelder, HD 2019, 'Prefrontal cortical ChAT-VIP interneurons provide local excitation by cholinergic synaptic transmission and control attention', Nature communications, vol. 10, no. 1, pp. 5280. https://doi.org/10.1038/s41467-019-13244-9

TY - JOUR

T1 - Prefrontal cortical ChAT-VIP interneurons provide local excitation by cholinergic synaptic transmission and control attention

AU - Obermayer, Joshua

AU - Luchicchi, Antonio

AU - Heistek, Tim S

AU - de Kloet, Sybren F

AU - Terra, Huub

AU - Bruinsma, Bastiaan

AU - Mnie-Filali, Ouissame

AU - Kortleven, Christian

AU - Galakhova, Anna A

AU - Khalil, Ayoub J

AU - Kroon, Tim

AU - Jonker, Allert J

AU - de Haan, Roel

AU - van den Berg, Wilma D J

AU - Goriounova, Natalia A

AU - de Kock, Christiaan P J

AU - Pattij, Tommy

AU - Mansvelder, Huibert D

PY - 2019/11/21

Y1 - 2019/11/21

N2 - Neocortical choline acetyltransferase (ChAT)-expressing interneurons are a subclass of vasoactive intestinal peptide (ChAT-VIP) neurons of which circuit and behavioural function are unknown. Here, we show that ChAT-VIP neurons directly excite neighbouring neurons in several layers through fast synaptic transmission of acetylcholine (ACh) in rodent medial prefrontal cortex (mPFC). Both interneurons in layers (L)1-3 as well as pyramidal neurons in L2/3 and L6 receive direct inputs from ChAT-VIP neurons mediated by fast cholinergic transmission. A fraction (10-20%) of postsynaptic neurons that received cholinergic input from ChAT-VIP interneurons also received GABAergic input from these neurons. In contrast to regular VIP interneurons, ChAT-VIP neurons did not disinhibit pyramidal neurons. Finally, we show that activity of these neurons is relevant for behaviour and they control attention behaviour distinctly from basal forebrain ACh inputs. Thus, ChAT-VIP neurons are a local source of cortical ACh that directly excite neurons throughout cortical layers and contribute to attention.

AB - Neocortical choline acetyltransferase (ChAT)-expressing interneurons are a subclass of vasoactive intestinal peptide (ChAT-VIP) neurons of which circuit and behavioural function are unknown. Here, we show that ChAT-VIP neurons directly excite neighbouring neurons in several layers through fast synaptic transmission of acetylcholine (ACh) in rodent medial prefrontal cortex (mPFC). Both interneurons in layers (L)1-3 as well as pyramidal neurons in L2/3 and L6 receive direct inputs from ChAT-VIP neurons mediated by fast cholinergic transmission. A fraction (10-20%) of postsynaptic neurons that received cholinergic input from ChAT-VIP interneurons also received GABAergic input from these neurons. In contrast to regular VIP interneurons, ChAT-VIP neurons did not disinhibit pyramidal neurons. Finally, we show that activity of these neurons is relevant for behaviour and they control attention behaviour distinctly from basal forebrain ACh inputs. Thus, ChAT-VIP neurons are a local source of cortical ACh that directly excite neurons throughout cortical layers and contribute to attention.

U2 - 10.1038/s41467-019-13244-9

DO - 10.1038/s41467-019-13244-9

M3 - Article

SN - 2041-1723

VL - 10

SP - 5280

JO - Nature communications

JF - Nature communications

IS - 1

ER -

Prefrontal cortical ChAT-VIP interneurons provide local excitation by cholinergic synaptic transmission and control attention

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