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Article ; Online: Experience shapes chandelier cell function and structure in the visual cortex.

Seignette, Koen / Jamann, Nora / Papale, Paolo / Terra, Huub / Porneso, Ralph O / de Kraker, Leander / van der Togt, Chris / van der Aa, Maaike / Neering, Paul / Ruimschotel, Emma / Roelfsema, Pieter R / Montijn, Jorrit S / Self, Matthew W / Kole, Maarten H P / Levelt, Christiaan N

eLife

2024 Volume 12

Abstract: Detailed characterization of interneuron types in primary visual cortex (V1) has greatly contributed to understanding visual perception, yet the role of chandelier cells (ChCs) in visual processing remains poorly characterized. Using viral tracing we ... ...

Abstract	Detailed characterization of interneuron types in primary visual cortex (V1) has greatly contributed to understanding visual perception, yet the role of chandelier cells (ChCs) in visual processing remains poorly characterized. Using viral tracing we found that V1 ChCs predominantly receive monosynaptic input from local layer 5 pyramidal cells and higher-order cortical regions. Two-photon calcium imaging and convolutional neural network modeling revealed that ChCs are visually responsive but weakly selective for stimulus content. In mice running in a virtual tunnel, ChCs respond strongly to events known to elicit arousal, including locomotion and visuomotor mismatch. Repeated exposure of the mice to the virtual tunnel was accompanied by reduced visual responses of ChCs and structural plasticity of ChC boutons and axon initial segment length. Finally, ChCs only weakly inhibited pyramidal cells. These findings suggest that ChCs provide an arousal-related signal to layer 2/3 pyramidal cells that may modulate their activity and/or gate plasticity of their axon initial segments during behaviorally relevant events.
MeSH term(s)	Animals ; Mice ; Neurons ; Pyramidal Cells ; Visual Cortex ; Interneurons ; Arousal
Language	English
Publishing date	2024-01-09
Publishing country	England
Document type	Journal Article
ZDB-ID	2687154-3
ISSN	2050-084X ; 2050-084X
ISSN (online)	2050-084X
ISSN	2050-084X
DOI	10.7554/eLife.91153
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Article ; Online: Prefrontal Cortical Projection Neurons Targeting Dorsomedial Striatum Control Behavioral Inhibition.

Terra, Huub / Bruinsma, Bastiaan / de Kloet, Sybren F / van der Roest, Marcel / Pattij, Tommy / Mansvelder, Huibert D

Current biology : CB

2020 Volume 30, Issue 21, Page(s) 4188–4200.e5

Abstract: A neural pathway from prefrontal cortex (PFC) to dorsal striatum (DS) has been suggested to mediate cognitive control of behavior, including proactive inhibitory control and attention. However, a direct causal demonstration thereof is lacking. Here, we ... ...

Abstract	A neural pathway from prefrontal cortex (PFC) to dorsal striatum (DS) has been suggested to mediate cognitive control of behavior, including proactive inhibitory control and attention. However, a direct causal demonstration thereof is lacking. Here, we show that selective chemogenetic silencing of corticostriatal PFC neurons in rats increases premature responses. Wireless single-unit electrophysiological recordings of optogenetically identified corticostriatal PFC neurons revealed that the majority of these neurons encode behavioral trial outcome with persistent changes in firing rate. Attentional parameters were not affected by silencing corticostriatal PFC neurons, suggesting that these projection neurons encode a specific subset of cognitive behaviors. Compared to the general non-identified neuronal population in the PFC, frontostriatal neurons showed selective engagement during periods of inhibitory control. Our results demonstrate a role for corticostriatal neurons in inhibitory control and possibly suggest that distinct domains of cognitive control over behavior are encoded by specific projection neuron populations.
MeSH term(s)	Action Potentials/physiology ; Animals ; Behavior, Animal ; Cognition/physiology ; Corpus Striatum/cytology ; Corpus Striatum/physiology ; Inhibition, Psychological ; Male ; Models, Animal ; Neural Pathways/physiology ; Neurons/physiology ; Optogenetics ; Prefrontal Cortex/cytology ; Prefrontal Cortex/physiology ; Rats ; Stereotaxic Techniques ; Synaptic Transmission/physiology
Language	English
Publishing date	2020-09-03
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1071731-6
ISSN	1879-0445 ; 0960-9822
ISSN (online)	1879-0445
ISSN	0960-9822
DOI	10.1016/j.cub.2020.08.031
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Article ; Online: Bi-directional regulation of cognitive control by distinct prefrontal cortical output neurons to thalamus and striatum.

de Kloet, Sybren F / Bruinsma, Bastiaan / Terra, Huub / Heistek, Tim S / Passchier, Emma M J / van den Berg, Alexandra R / Luchicchi, Antonio / Min, Rogier / Pattij, Tommy / Mansvelder, Huibert D

Nature communications

2021 Volume 12, Issue 1, Page(s) 1994

Abstract: The medial prefrontal cortex (mPFC) steers goal-directed actions and withholds inappropriate behavior. Dorsal and ventral mPFC (dmPFC/vmPFC) circuits have distinct roles in cognitive control, but underlying mechanisms are poorly understood. Here we use ... ...

Abstract	The medial prefrontal cortex (mPFC) steers goal-directed actions and withholds inappropriate behavior. Dorsal and ventral mPFC (dmPFC/vmPFC) circuits have distinct roles in cognitive control, but underlying mechanisms are poorly understood. Here we use neuroanatomical tracing techniques, in vitro electrophysiology, chemogenetics and fiber photometry in rats engaged in a 5-choice serial reaction time task to characterize dmPFC and vmPFC outputs to distinct thalamic and striatal subdomains. We identify four spatially segregated projection neuron populations in the mPFC. Using fiber photometry we show that these projections distinctly encode behavior. Postsynaptic striatal and thalamic neurons differentially process synaptic inputs from dmPFC and vmPFC, highlighting mechanisms that potentially amplify distinct pathways underlying cognitive control of behavior. Chemogenetic silencing of dmPFC and vmPFC projections to lateral and medial mediodorsal thalamus subregions oppositely regulate cognitive control. In addition, dmPFC neurons projecting to striatum and thalamus divergently regulate cognitive control. Collectively, we show that mPFC output pathways targeting anatomically and functionally distinct striatal and thalamic subregions encode bi-directional command of cognitive control.
MeSH term(s)	Animals ; Cognition/physiology ; Corpus Striatum/cytology ; Corpus Striatum/physiology ; Electrophysiological Phenomena ; Male ; Models, Neurological ; Neural Pathways/physiology ; Neurons/physiology ; Prefrontal Cortex/cytology ; Prefrontal Cortex/physiology ; Rats, Long-Evans ; Thalamus/cytology ; Thalamus/physiology ; Rats
Language	English
Publishing date	2021-03-31
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-021-22260-7
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Article ; Online: Cognitive effects of endocrine therapy for breast cancer: keep calm and carry on?

Zwart, Wilbert / Terra, Huub / Linn, Sabine C / Schagen, Sanne B

Nature reviews. Clinical oncology

2015 Volume 12, Issue 10, Page(s) 597–606

Abstract: The number of breast cancer survivors is gradually increasing and a subset of these patients experience long-term adverse effects of adjuvant systemic therapy, including cognitive decline. Surprisingly, relatively little is known about the long-term ... ...

Abstract	The number of breast cancer survivors is gradually increasing and a subset of these patients experience long-term adverse effects of adjuvant systemic therapy, including cognitive decline. Surprisingly, relatively little is known about the long-term adverse effects of endocrine treatment on cognition. As 75% of all patients with breast cancer are eligible to receive hormonal treatment, understanding the potential neurocognitive adverse effects of such therapy is of utmost importance. Concerns about adverse cognitive effects of adjuvant endocrine therapy are timely, as recently updated guidelines recommend increasing the length of such therapy from 5 years to 10 years for a subset of patients. The decline of cognitive functions can have a detrimental impact on quality of life and might interfere with independent living. This Review discusses the tissue-selective side effects of endocrine therapies and specifically their impact on cognitive function, on the basis of clinical data; the neurobiological effects of endocrine therapies as observed in preclinical models are also discussed. We highlight the critical issues that need to be addressed in future preclinical and clinical studies in order to best assess the cognitive effects of endocrine treatment in patients with breast cancer.
MeSH term(s)	Antineoplastic Agents, Hormonal/adverse effects ; Breast Neoplasms/drug therapy ; Cognition Disorders/chemically induced ; Decision Making ; Female ; Humans
Chemical Substances	Antineoplastic Agents, Hormonal
Language	English
Publishing date	2015-10
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	2491410-1
ISSN	1759-4782 ; 1759-4774
ISSN (online)	1759-4782
ISSN	1759-4774
DOI	10.1038/nrclinonc.2015.124
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Article ; Online: Dorsomedial prefrontal cortex neurons encode nicotine-cue associations.

Struik, Roeland F / Marchant, Nathan J / de Haan, Roel / Terra, Huub / van Mourik, Yvar / Schetters, Dustin / Carr, Madison R / van der Roest, Marcel / Heistek, Tim S / De Vries, Taco J

Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology

2019 Volume 44, Issue 12, Page(s) 2011–2021

Abstract: The role of medial prefrontal cortex (mPFC) in regulating nicotine taking and seeking remains largely unexplored. In this study we took advantage of the high time-resolution of optogenetic intervention by decreasing (Arch3.0) or increasing (ChR2) the ... ...

Abstract	The role of medial prefrontal cortex (mPFC) in regulating nicotine taking and seeking remains largely unexplored. In this study we took advantage of the high time-resolution of optogenetic intervention by decreasing (Arch3.0) or increasing (ChR2) the activity of neurons in the dorsal and ventral mPFC during 5-s nicotine cue presentations in order to evaluate their contribution to cued nicotine seeking and taking. Wistar rats were trained to self-administer intravenous nicotine in 1 h self-administration sessions twice a day for a minimum of 10 days. Subsequently, dmPFC or vmPFC neuronal activity was modulated during or following presentation of the 5-s nicotine cue, both under extinction and self-administration conditions. We also used in vivo electrophysiology to record the activity of dmPFC neurons during nicotine self-administration and extinction tests. We show that optogenetic inhibition of dmPFC neurons during, but not following, response-contingent presentations of the nicotine cue increased nicotine seeking. We found no effect on nicotine self-administration or on food seeking in an extinction test. We also show that this effect is specific to dmPFC, because optogenetic inhibition of vmPFC had no effect on nicotine seeking and taking. In vivo recordings revealed that dmPFC network neuronal activity was modulated more strongly following nicotine cue presentation in extinction, compared to following nicotine self-administration. Our results strongly suggest that a population of neurons within the dmPFC is involved in encoding the incentive value of nicotine-associated cues.
MeSH term(s)	Animals ; Conditioning, Operant/drug effects ; Conditioning, Operant/physiology ; Cues ; Drug-Seeking Behavior/physiology ; Extinction, Psychological/drug effects ; Extinction, Psychological/physiology ; Male ; Neurons/drug effects ; Neurons/physiology ; Nicotine/administration & dosage ; Optogenetics ; Prefrontal Cortex/drug effects ; Prefrontal Cortex/physiology ; Rats, Wistar
Chemical Substances	Nicotine (6M3C89ZY6R)
Language	English
Publishing date	2019-06-26
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	639471-1
ISSN	1740-634X ; 0893-133X
ISSN (online)	1740-634X
ISSN	0893-133X
DOI	10.1038/s41386-019-0449-x
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Article ; Online: Author Correction: Prefrontal cortical ChAT-VIP interneurons provide local excitation by cholinergic synaptic transmission and control attention.

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

Nature communications

2020 Volume 11, Issue 1, Page(s) 794

Abstract: An amendment to this paper has been published and can be accessed via a link at the top of the paper. ...

Abstract	An amendment to this paper has been published and can be accessed via a link at the top of the paper.
Language	English
Publishing date	2020-02-04
Publishing country	England
Document type	Published Erratum
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-020-14315-y
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Article ; Online: 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

Frontiers in neural circuits

2016 Volume 10, Page(s) 70

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 ... ...

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.
MeSH term(s)	Animals ; Attention/physiology ; Behavior, Animal ; Male ; Optogenetics ; Prefrontal Cortex/physiology ; Pyramidal Cells/physiology ; Rats ; Rats, Long-Evans
Language	English
Publishing date	2016-08-31
Publishing country	Switzerland
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2452968-0
ISSN	1662-5110 ; 1662-5110
ISSN (online)	1662-5110
ISSN	1662-5110
DOI	10.3389/fncir.2016.00070
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Article ; Online: Prefrontal cortical ChAT-VIP interneurons provide local excitation by cholinergic synaptic transmission and control attention.

Nature communications

2019 Volume 10, Issue 1, Page(s) 5280

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 ... ...

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.
MeSH term(s)	Acetylcholine/pharmacology ; Animals ; Attention/drug effects ; Attention/physiology ; Cerebral Cortex/cytology ; Cerebral Cortex/metabolism ; Choline O-Acetyltransferase/metabolism ; Cholinergic Agents/pharmacology ; Female ; Interneurons/drug effects ; Interneurons/metabolism ; Interneurons/physiology ; Male ; Mice, 129 Strain ; Neurons/drug effects ; Neurons/metabolism ; Neurons/physiology ; Prefrontal Cortex/cytology ; Prefrontal Cortex/metabolism ; Rats ; Synaptic Transmission/drug effects ; Synaptic Transmission/physiology ; Vasoactive Intestinal Peptide/metabolism
Chemical Substances	Cholinergic Agents ; Vasoactive Intestinal Peptide (37221-79-7) ; Choline O-Acetyltransferase (EC 2.3.1.6) ; Acetylcholine (N9YNS0M02X)
Language	English
Publishing date	2019-11-21
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-019-13244-9
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Article ; Online: Role of vasoactive intestinal peptide in the light input to the circadian system.

Vosko, Andrew / van Diepen, Hester C / Kuljis, Dika / Chiu, Andrew M / Heyer, Djai / Terra, Huub / Carpenter, Ellen / Michel, Stephan / Meijer, Johanna H / Colwell, Christopher S

The European journal of neuroscience

2015 Volume 42, Issue 2, Page(s) 1839–1848

Abstract: The neuropeptide vasoactive intestinal peptide (VIP) is expressed at high levels in a subset of neurons in the ventral region of the suprachiasmatic nucleus (SCN). While VIP is known to be important for the synchronization of the SCN network, the role of ...

Abstract	The neuropeptide vasoactive intestinal peptide (VIP) is expressed at high levels in a subset of neurons in the ventral region of the suprachiasmatic nucleus (SCN). While VIP is known to be important for the synchronization of the SCN network, the role of VIP in photic regulation of the circadian system has received less attention. In the present study, we found that the light-evoked increase in electrical activity in vivo was unaltered by the loss of VIP. In the absence of VIP, the ventral SCN still exhibited N-methyl-d-aspartate-evoked responses in a brain slice preparation, although the absolute levels of neural activity before and after treatment were significantly reduced. Next, we used calcium imaging techniques to determine if the loss of VIP altered the calcium influx due to retinohypothalamic tract stimulation. The magnitude of the evoked calcium influx was not reduced in the ventral SCN, but did decline in the dorsal SCN regions. We examined the time course of the photic induction of Period1 in the SCN using in situ hybridization in VIP-mutant mice. We found that the initial induction of Period1 was not reduced by the loss of this signaling peptide. However, the sustained increase in Period1 expression (after 30 min) was significantly reduced. Similar results were found by measuring the light induction of cFOS in the SCN. These findings suggest that VIP is critical for longer-term changes within the SCN circuit, but does not play a role in the acute light response.
MeSH term(s)	Action Potentials/drug effects ; Action Potentials/physiology ; Animals ; Calcium/metabolism ; Darkness ; Excitatory Amino Acid Agonists/pharmacology ; Gene Expression Regulation/drug effects ; Gene Expression Regulation/genetics ; Light ; Male ; Mice ; Mice, Inbred C57BL ; Mice, Transgenic ; Molecular Sequence Data ; N-Methylaspartate/pharmacology ; Nerve Net/drug effects ; Nerve Net/physiology ; Neurons/drug effects ; Neurons/physiology ; Oncogene Proteins v-fos/metabolism ; Patch-Clamp Techniques ; Period Circadian Proteins/genetics ; Period Circadian Proteins/metabolism ; Suprachiasmatic Nucleus/cytology ; Suprachiasmatic Nucleus/drug effects ; Suprachiasmatic Nucleus/physiology ; Vasoactive Intestinal Peptide/genetics ; Vasoactive Intestinal Peptide/metabolism
Chemical Substances	Excitatory Amino Acid Agonists ; Oncogene Proteins v-fos ; Per1 protein, mouse ; Period Circadian Proteins ; Vasoactive Intestinal Peptide (37221-79-7) ; N-Methylaspartate (6384-92-5) ; Calcium (SY7Q814VUP)
Language	English
Publishing date	2015-07
Publishing country	France
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	645180-9
ISSN	1460-9568 ; 0953-816X
ISSN (online)	1460-9568
ISSN	0953-816X
DOI	10.1111/ejn.12919
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