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Article ; Online: Serotonin modulates excitatory synapse maturation in the developing prefrontal cortex.

Ogelman, Roberto / Gomez Wulschner, Luis E / Hoelscher, Victoria M / Hwang, In-Wook / Chang, Victoria N / Oh, Won Chan

2024 Volume 15, Issue 1, Page(s) 1368

Abstract: Serotonin (5-HT) imbalances in the developing prefrontal cortex (PFC) are linked to long-term behavioral deficits. However, the synaptic mechanisms underlying 5-HT-mediated PFC development are unknown. We found that chemogenetic suppression and ... ...

Abstract	Serotonin (5-HT) imbalances in the developing prefrontal cortex (PFC) are linked to long-term behavioral deficits. However, the synaptic mechanisms underlying 5-HT-mediated PFC development are unknown. We found that chemogenetic suppression and enhancement of 5-HT release in the PFC during the first two postnatal weeks decreased and increased the density and strength of excitatory spine synapses, respectively, on prefrontal layer 2/3 pyramidal neurons in mice. 5-HT release on single spines induced structural and functional long-term potentiation (LTP), requiring both 5-HT2A and 5-HT7 receptor signals, in a glutamatergic activity-independent manner. Notably, LTP-inducing 5-HT stimuli increased the long-term survival of newly formed spines ( ≥ 6 h) via 5-HT7 Gα
MeSH term(s)	Mice ; Animals ; Serotonin/pharmacology ; Fluoxetine/pharmacology ; Pyramidal Cells/physiology ; Prefrontal Cortex/physiology ; Synapses/physiology
Chemical Substances	Serotonin (333DO1RDJY) ; Fluoxetine (01K63SUP8D)
Language	English
Publishing date	2024-02-16
Publishing country	England
Document type	Journal Article
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-024-45734-w
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Article ; Online: Trans-synaptic mechanisms orchestrated by mammalian synaptic cell adhesion molecules.

Kim, Jinhu / Wulschner, Luis E Gomez / Oh, Won Chan / Ko, Jaewon

BioEssays : news and reviews in molecular, cellular and developmental biology

2022 Volume 44, Issue 11, Page(s) e2200134

Abstract: Bidirectional trans-synaptic signaling is essential for the formation, maturation, and plasticity of synaptic connections. Synaptic cell adhesion molecules (CAMs) are prime drivers in shaping the identities of trans-synaptic signaling pathways. A series ... ...

Abstract	Bidirectional trans-synaptic signaling is essential for the formation, maturation, and plasticity of synaptic connections. Synaptic cell adhesion molecules (CAMs) are prime drivers in shaping the identities of trans-synaptic signaling pathways. A series of recent studies provide evidence that diverse presynaptic cell adhesion proteins dictate the regulation of specific synaptic properties in postsynaptic neurons. Focusing on mammalian synaptic CAMs, this article outlines several exemplary cases supporting this notion and highlights how these trans-synaptic signaling pathways collectively contribute to the specificity and diversity of neural circuit architecture.
MeSH term(s)	Animals ; Synapses/metabolism ; Neurons/metabolism ; Cell Adhesion Molecules/metabolism ; Cell Communication ; Mammals/metabolism
Chemical Substances	Cell Adhesion Molecules
Language	English
Publishing date	2022-09-11
Publishing country	United States
Document type	Journal Article
ZDB-ID	50140-2
ISSN	1521-1878 ; 0265-9247
ISSN (online)	1521-1878
ISSN	0265-9247
DOI	10.1002/bies.202200134
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Article ; Online: Trans‐synaptic mechanisms orchestrated by mammalian synaptic cell adhesion molecules

Kim, Jinhu / Wulschner, Luis E. Gomez / Oh, Won Chan / Ko, Jaewon

BioEssays. 2022 Nov., v. 44, no. 11 p.e2200134-

2022

Abstract: Bidirectional trans‐synaptic signaling is essential for the formation, maturation, and plasticity of synaptic connections. Synaptic cell adhesion molecules (CAMs) are prime drivers in shaping the identities of trans‐synaptic signaling pathways. A series ... ...

Abstract	Bidirectional trans‐synaptic signaling is essential for the formation, maturation, and plasticity of synaptic connections. Synaptic cell adhesion molecules (CAMs) are prime drivers in shaping the identities of trans‐synaptic signaling pathways. A series of recent studies provide evidence that diverse presynaptic cell adhesion proteins dictate the regulation of specific synaptic properties in postsynaptic neurons. Focusing on mammalian synaptic CAMs, this article outlines several exemplary cases supporting this notion and highlights how these trans‐synaptic signaling pathways collectively contribute to the specificity and diversity of neural circuit architecture.
Keywords	cell adhesion ; mammals ; neural networks ; plasticity
Language	English
Dates of publication	2022-11
Publishing place	John Wiley & Sons, Ltd
Document type	Article ; Online
Note	JOURNAL ARTICLE
ZDB-ID	50140-2
ISSN	1521-1878 ; 0265-9247
ISSN (online)	1521-1878
ISSN	0265-9247
DOI	10.1002/bies.202200134
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Article ; Online: Activity-dependent development of GABAergic synapses.

Oh, Won Chan / Smith, Katharine R

Brain research

2018 Volume 1707, Page(s) 18–26

Abstract: In the brain, dendrites of pyramidal neurons contain intermingled excitatory and inhibitory synapses. Synaptic connections dynamically change during development and throughout our lifetime, yet the brain can properly maintain an optimal ratio of synaptic ...

Abstract	In the brain, dendrites of pyramidal neurons contain intermingled excitatory and inhibitory synapses. Synaptic connections dynamically change during development and throughout our lifetime, yet the brain can properly maintain an optimal ratio of synaptic excitation to inhibition. Despite recent advances in our understanding of the formation and refinement of excitatory glutamatergic synapses, little is known about signals that regulate inhibitory GABAergic synapse development. In this review, we discuss previous and recent insights in the cellular and molecular mechanisms that underlie GABAergic synapse formation and plasticity, with a specific focus on the key roles of synaptic activity and postsynaptic membrane molecules.
MeSH term(s)	Animals ; Brain/metabolism ; GABAergic Neurons/metabolism ; GABAergic Neurons/physiology ; Humans ; Nerve Tissue Proteins/metabolism ; Neuronal Plasticity/physiology ; Pyramidal Cells/metabolism ; Pyramidal Cells/physiology ; Synapses/metabolism ; Synapses/physiology ; Synaptic Transmission/physiology
Chemical Substances	Nerve Tissue Proteins
Language	English
Publishing date	2018-11-12
Publishing country	Netherlands
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	1200-2
ISSN	1872-6240 ; 0006-8993
ISSN (online)	1872-6240
ISSN	0006-8993
DOI	10.1016/j.brainres.2018.11.014
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Article ; Online: Cloaked caged glutamate eliminates off-target GABA-A receptor antagonism and opens a new door in neuroscience.

Ogelman, Roberto / Hwang, In-Wook / Oh, Won Chan

Lab animal

2020 Volume 49, Issue 6, Page(s) 177–179

MeSH term(s)	Animals ; GABA-A Receptor Antagonists ; Glutamic Acid ; Learning ; Receptors, GABA-A ; Rodentia
Chemical Substances	GABA-A Receptor Antagonists ; Receptors, GABA-A ; Glutamic Acid (3KX376GY7L)
Language	English
Publishing date	2020-05-27
Publishing country	United States
Document type	Journal Article ; Comment
ISSN	1548-4475
ISSN (online)	1548-4475
DOI	10.1038/s41684-020-0555-8
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Article ; Online: Induction of input-specific spine shrinkage on dendrites of rodent hippocampal CA1 neurons using two-photon glutamate uncaging.

Jang, Jinyoung / Anisimova, Margarita / Oh, Won Chan / Zito, Karen

STAR protocols

2021 Volume 2, Issue 4, Page(s) 100996

Abstract: Shrinkage and loss of dendritic spines are vital components of the neuronal plasticity that supports learning. To investigate the mechanisms of spine shrinkage and loss, Oh and colleagues established a two-photon glutamate uncaging protocol that reliably ...

Abstract	Shrinkage and loss of dendritic spines are vital components of the neuronal plasticity that supports learning. To investigate the mechanisms of spine shrinkage and loss, Oh and colleagues established a two-photon glutamate uncaging protocol that reliably induces input-specific spine shrinkage on dendrites of rodent hippocampal CA1 pyramidal neurons. Here, we provide a detailed description of that protocol and also an optimized version that can be used to induce input- and synapse-specific shrinkage of dendritic spines at physiological Ca
MeSH term(s)	Animals ; CA1 Region, Hippocampal/cytology ; CA1 Region, Hippocampal/metabolism ; Dendritic Spines/metabolism ; Female ; Glutamic Acid/metabolism ; Male ; Mice ; Mice, Inbred C57BL ; Photons ; Pyramidal Cells/metabolism ; Rats ; Rats, Sprague-Dawley
Chemical Substances	Glutamic Acid (3KX376GY7L)
Language	English
Publishing date	2021-12-11
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ISSN	2666-1667
ISSN (online)	2666-1667
DOI	10.1016/j.xpro.2021.100996
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Article ; Online: Fetal cannabidiol (CBD) exposure alters thermal pain sensitivity, problem-solving, and prefrontal cortex excitability.

Swenson, Karli S / Gomez Wulschner, Luis E / Hoelscher, Victoria M / Folts, Lillian / Korth, Kamryn M / Oh, Won Chan / Bates, Emily Anne

Molecular psychiatry

2023 Volume 28, Issue 8, Page(s) 3397–3413

Abstract: Thousands of people suffer from nausea with pregnancy each year. Nausea can be alleviated with cannabidiol (CBD), a primary component of cannabis that is widely available. However, it is unknown how fetal CBD exposure affects embryonic development and ... ...

Abstract	Thousands of people suffer from nausea with pregnancy each year. Nausea can be alleviated with cannabidiol (CBD), a primary component of cannabis that is widely available. However, it is unknown how fetal CBD exposure affects embryonic development and postnatal outcomes. CBD binds and activates receptors that are expressed in the fetal brain and are important for brain development, including serotonin receptors (5HT
MeSH term(s)	Humans ; Pregnancy ; Male ; Female ; Mice ; Animals ; Cannabidiol/pharmacology ; Cannabidiol/metabolism ; Sunflower Oil/metabolism ; Prefrontal Cortex/metabolism ; Pain/metabolism ; Nausea/metabolism
Chemical Substances	Cannabidiol (19GBJ60SN5) ; Sunflower Oil
Language	English
Publishing date	2023-07-11
Publishing country	England
Document type	Journal Article
ZDB-ID	1330655-8
ISSN	1476-5578 ; 1359-4184
ISSN (online)	1476-5578
ISSN	1359-4184
DOI	10.1038/s41380-023-02130-y
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Zs.A 4812: Show issues

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ab Jg. 2022: Lesesaal (EG)

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Article ; Online: Dysregulation of the mesoprefrontal dopamine circuit mediates an early-life stress-induced synaptic imbalance in the prefrontal cortex.

Oh, Won Chan / Rodríguez, Gabriela / Asede, Douglas / Jung, Kanghoon / Hwang, In-Wook / Ogelman, Roberto / Bolton, McLean M / Kwon, Hyung-Bae

Cell reports

2021 Volume 35, Issue 5, Page(s) 109074

Abstract: Stress adversely affects an array of cognitive functions. Although stress-related disorders are often addressed in adulthood, far less is known about how early-life stress (ELS) affects the developing brain in early postnatal periods. Here we show that ... ...

Abstract	Stress adversely affects an array of cognitive functions. Although stress-related disorders are often addressed in adulthood, far less is known about how early-life stress (ELS) affects the developing brain in early postnatal periods. Here we show that ELS, induced by maternal separation, leads to synaptic alteration of layer 2/3 pyramidal neurons in the prefrontal cortex (PFC) of mice. We find that layer 2/3 neurons show increased excitatory synapse numbers following ELS and that this is accompanied by hyperexcitability of PFC-projecting dopamine (DA) neurons in the ventral tegmental area. Notably, excitatory synaptic change requires local signaling through DA D2 receptors. In vivo pharmacological treatment with a D2 receptor agonist in the PFC of control mice mimics the effects of ELS on synaptic alterations. Our findings reveal a neuromodulatory mechanism underlying ELS-induced PFC dysfunction, and this mechanism may facilitate a more comprehensive understanding of how ELS leads to mental disorders.
MeSH term(s)	Animals ; Dopamine/metabolism ; Male ; Mice ; Prefrontal Cortex/physiology
Chemical Substances	Dopamine (VTD58H1Z2X)
Language	English
Publishing date	2021-05-05
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2649101-1
ISSN	2211-1247 ; 2211-1247
ISSN (online)	2211-1247
ISSN	2211-1247
DOI	10.1016/j.celrep.2021.109074
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Article ; Online: Heterosynaptic structural plasticity on local dendritic segments of hippocampal CA1 neurons.

Oh, Won Chan / Parajuli, Laxmi Kumar / Zito, Karen

Cell reports

2015 Volume 10, Issue 2, Page(s) 162–169

Abstract: Competition between synapses contributes to activity-dependent refinement of the nervous system during development. Does local competition between neighboring synapses drive circuit remodeling during experience-dependent plasticity in the cerebral cortex? ...

Abstract	Competition between synapses contributes to activity-dependent refinement of the nervous system during development. Does local competition between neighboring synapses drive circuit remodeling during experience-dependent plasticity in the cerebral cortex? Here, we examined the role of activity-mediated competitive interactions in regulating dendritic spine structure and function on hippocampal CA1 neurons. We found that high-frequency glutamatergic stimulation at individual spines, which leads to input-specific synaptic potentiation, induces shrinkage and weakening of nearby unstimulated synapses. This heterosynaptic plasticity requires potentiation of multiple neighboring spines, suggesting that a local threshold of neural activity exists beyond which inactive synapses are punished. Notably, inhibition of calcineurin, IP3Rs, or group I metabotropic glutamate receptors (mGluRs) blocked heterosynaptic shrinkage without blocking structural potentiation, and inhibition of Ca(2+)/calmodulin-dependent protein kinase II (CaMKII) blocked structural potentiation without blocking heterosynaptic shrinkage. Our results support a model in which activity-induced shrinkage signal, and not competition for limited structural resources, drives heterosynaptic structural and functional depression during neural circuit refinement.
MeSH term(s)	Animals ; CA1 Region, Hippocampal/physiology ; Calcineurin/chemistry ; Calcineurin/metabolism ; Calcium-Calmodulin-Dependent Protein Kinase Type 2/antagonists & inhibitors ; Calcium-Calmodulin-Dependent Protein Kinase Type 2/metabolism ; Dendrites/physiology ; Inositol 1,4,5-Trisphosphate Receptors/antagonists & inhibitors ; Inositol 1,4,5-Trisphosphate Receptors/metabolism ; Neuronal Plasticity ; Rats ; Rats, Sprague-Dawley ; Receptors, Metabotropic Glutamate/antagonists & inhibitors ; Receptors, Metabotropic Glutamate/metabolism ; Synapses/physiology
Chemical Substances	Inositol 1,4,5-Trisphosphate Receptors ; Receptors, Metabotropic Glutamate ; Calcium-Calmodulin-Dependent Protein Kinase Type 2 (EC 2.7.11.17) ; Calcineurin (EC 3.1.3.16)
Language	English
Publishing date	2015-01-13
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2649101-1
ISSN	2211-1247 ; 2211-1247
ISSN (online)	2211-1247
ISSN	2211-1247
DOI	10.1016/j.celrep.2014.12.016
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Article ; Online: MDGA1 negatively regulates amyloid precursor protein-mediated synapse inhibition in the hippocampus.

Kim, Jinhu / Kim, Seungjoon / Kim, Hyeonho / Hwang, In-Wook / Bae, Sungwon / Karki, Sudeep / Kim, Dongwook / Ogelman, Roberto / Bang, Geul / Kim, Jin Young / Kajander, Tommi / Um, Ji Won / Oh, Won Chan / Ko, Jaewon

Proceedings of the National Academy of Sciences of the United States of America

2022 Volume 119, Issue 4

Abstract: Balanced synaptic inhibition, controlled by multiple synaptic adhesion proteins, is critical for proper brain function. MDGA1 (meprin, A-5 protein, and receptor protein-tyrosine phosphatase mu [MAM] domain-containing glycosylphosphatidylinositol anchor ... ...

Abstract	Balanced synaptic inhibition, controlled by multiple synaptic adhesion proteins, is critical for proper brain function. MDGA1 (meprin, A-5 protein, and receptor protein-tyrosine phosphatase mu [MAM] domain-containing glycosylphosphatidylinositol anchor protein 1) suppresses synaptic inhibition in mammalian neurons, yet the molecular mechanisms underlying MDGA1-mediated negative regulation of GABAergic synapses remain unresolved. Here, we show that the MDGA1 MAM domain directly interacts with the extension domain of amyloid precursor protein (APP). Strikingly, MDGA1-mediated synaptic disinhibition requires the MDGA1 MAM domain and is prominent at distal dendrites of hippocampal CA1 pyramidal neurons. Down-regulation of APP in presynaptic GABAergic interneurons specifically suppressed GABAergic, but not glutamatergic, synaptic transmission strength and inputs onto both the somatic and dendritic compartments of hippocampal CA1 pyramidal neurons. Moreover, APP deletion manifested differential effects in somatostatin- and parvalbumin-positive interneurons in the hippocampal CA1, resulting in distinct alterations in inhibitory synapse numbers, transmission, and excitability. The infusion of MDGA1 MAM protein mimicked postsynaptic MDGA1 gain-of-function phenotypes that involve the presence of presynaptic APP. The overexpression of MDGA1 wild type or MAM, but not MAM-deleted MDGA1, in the hippocampal CA1 impaired novel object-recognition memory in mice. Thus, our results establish unique roles of APP-MDGA1 complexes in hippocampal neural circuits, providing unprecedented insight into
MeSH term(s)	Amyloid beta-Protein Precursor/genetics ; Amyloid beta-Protein Precursor/metabolism ; CA1 Region, Hippocampal ; Carrier Proteins ; Dendrites/metabolism ; GABAergic Neurons/metabolism ; Hippocampus/metabolism ; Hippocampus/physiopathology ; Interneurons ; Models, Biological ; Neural Cell Adhesion Molecules/chemistry ; Neural Cell Adhesion Molecules/genetics ; Neural Cell Adhesion Molecules/metabolism ; Neural Inhibition/genetics ; Protein Binding ; Protein Interaction Domains and Motifs ; Pyramidal Cells/metabolism ; Receptors, GABA-B/metabolism ; Synapses/metabolism ; Synaptic Transmission
Chemical Substances	Amyloid beta-Protein Precursor ; Carrier Proteins ; Mdga1 protein, mouse ; Neural Cell Adhesion Molecules ; Receptors, GABA-B
Language	English
Publishing date	2022-01-24
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	209104-5
ISSN	1091-6490 ; 0027-8424
ISSN (online)	1091-6490
ISSN	0027-8424
DOI	10.1073/pnas.2115326119
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