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Article ; Online: From aversive associations to defensive programs: experience-dependent synaptic modifications in the central amygdala.

Penzo, Mario A / Moscarello, Justin M

2023 Volume 46, Issue 9, Page(s) 701–711

Abstract: Plasticity elicited by fear conditioning (FC) is thought to support the storage of aversive associative memories. Although work over the past decade has revealed FC-induced plasticity beyond canonical sites in the basolateral complex of the amygdala (BLA) ...

Abstract	Plasticity elicited by fear conditioning (FC) is thought to support the storage of aversive associative memories. Although work over the past decade has revealed FC-induced plasticity beyond canonical sites in the basolateral complex of the amygdala (BLA), it is not known whether modifications across distributed circuits make equivalent or distinct contributions to aversive memory. Here, we review evidence demonstrating that experience-dependent synaptic plasticity in the central nucleus of the amygdala (CeA) has a circumscribed role in memory expression per se, guiding the selection of defensive programs in response to acquired threats. We argue that the CeA may be a key example of a broader phenomenon by which synaptic plasticity at specific nodes of a distributed network makes a complementary contribution to distinct memory processes.
MeSH term(s)	Humans ; Central Amygdaloid Nucleus ; Fear/physiology ; Neuronal Plasticity/physiology ; Memory/physiology ; Affect
Language	English
Publishing date	2023-07-24
Publishing country	England
Document type	Journal Article ; Review ; Research Support, N.I.H., Intramural
ZDB-ID	282488-7
ISSN	1878-108X ; 0378-5912 ; 0166-2236
ISSN (online)	1878-108X
ISSN	0378-5912 ; 0166-2236
DOI	10.1016/j.tins.2023.06.006
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Article ; Online: The central nucleus of the amygdala and the construction of defensive modes across the threat-imminence continuum.

Moscarello, Justin M / Penzo, Mario A

Nature neuroscience

2022 Volume 25, Issue 8, Page(s) 999–1008

Abstract: In nature, animals display defensive behaviors that reflect the spatiotemporal distance of threats. Laboratory-based paradigms that elicit specific defensive responses in rodents have provided valuable insight into the brain mechanisms that mediate the ... ...

Abstract	In nature, animals display defensive behaviors that reflect the spatiotemporal distance of threats. Laboratory-based paradigms that elicit specific defensive responses in rodents have provided valuable insight into the brain mechanisms that mediate the construction of defensive modes with varying degrees of threat imminence. In this Review, we discuss accumulating evidence that the central nucleus of the amygdala (CeA) plays a key role in this process. Specifically, we propose that the mutually inhibitory circuits of the CeA use a winner-takes-all strategy that supports transitioning across defensive modes and the execution of specific defensive behaviors to previously formed threat associations. Our proposal provides a conceptual framework in which seemingly divergent observations regarding CeA function can be interpreted and identifies various areas of priority for future research.
MeSH term(s)	Animals ; Central Amygdaloid Nucleus/physiology
Language	English
Publishing date	2022-08-01
Publishing country	United States
Document type	Journal Article ; Review ; Research Support, N.I.H., Intramural
ZDB-ID	1420596-8
ISSN	1546-1726 ; 1097-6256
ISSN (online)	1546-1726
ISSN	1097-6256
DOI	10.1038/s41593-022-01130-5
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Article ; Online: The paraventricular nucleus of the thalamus: an integrative node underlying homeostatic behavior.

Penzo, Mario A / Gao, Claire

Trends in neurosciences

2021 Volume 44, Issue 7, Page(s) 538–549

Abstract: Early anatomical evidence suggested that the paraventricular nucleus of the thalamus (PVT) regulates arousal, as well as emotional and motivated behaviors. We discuss recent studies using modern techniques which now confirm and expand the involvement of ... ...

Abstract	Early anatomical evidence suggested that the paraventricular nucleus of the thalamus (PVT) regulates arousal, as well as emotional and motivated behaviors. We discuss recent studies using modern techniques which now confirm and expand the involvement of the rodent PVT in these functions. Despite the emerging notion that the PVT is implicated in various behavioral processes, a recurrent theme is that activity in this brain region depends on internal state information arriving from the hypothalamus and brainstem, and is influenced by prior experience. We propose that the primary function of the PVT is to detect homeostatic challenges by integrating information about prior experiences, competing needs, and internal state to guide adaptive behavioral responses aimed at restoring homeostasis.
MeSH term(s)	Homeostasis ; Humans ; Midline Thalamic Nuclei ; Neurons ; Paraventricular Hypothalamic Nucleus ; Thalamus
Language	English
Publishing date	2021-03-25
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Intramural ; Review
ZDB-ID	282488-7
ISSN	1878-108X ; 0378-5912 ; 0166-2236
ISSN (online)	1878-108X
ISSN	0378-5912 ; 0166-2236
DOI	10.1016/j.tins.2021.03.001
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Article: Dissociable encoding of motivated behavior by parallel thalamo-striatal projections.

Beas, Sofia / Khan, Isbah / Gao, Claire / Loewinger, Gabriel / Macdonald, Emma / Bashford, Alison / Rodriguez-Gonzalez, Shakira / Pereira, Francisco / Penzo, Mario A

bioRxiv : the preprint server for biology

2024

Abstract: The successful pursuit of goals requires the coordinated execution and termination of actions that lead to positive outcomes. This process is thought to rely on motivational states that are guided by internal drivers, such as hunger or fear. However, the ...

Abstract	The successful pursuit of goals requires the coordinated execution and termination of actions that lead to positive outcomes. This process is thought to rely on motivational states that are guided by internal drivers, such as hunger or fear. However, the mechanisms by which the brain tracks motivational states to shape instrumental actions are not fully understood. The paraventricular nucleus of the thalamus (PVT) is a midline thalamic nucleus that shapes motivated behaviors via its projections to the nucleus accumbens (NAc)
Language	English
Publishing date	2024-01-21
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.07.07.548113
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Article ; Online: Dissociable encoding of motivated behavior by parallel thalamo-striatal projections.

Beas, Sofia / Khan, Isbah / Gao, Claire / Loewinger, Gabriel / Macdonald, Emma / Bashford, Alison / Rodriguez-Gonzalez, Shakira / Pereira, Francisco / Penzo, Mario A

Current biology : CB

2024 Volume 34, Issue 7, Page(s) 1549–1560.e3

Abstract: The successful pursuit of goals requires the coordinated execution and termination of actions that lead to positive outcomes. This process relies on motivational states that are guided by internal drivers, such as hunger or fear. However, the mechanisms ... ...

Abstract	The successful pursuit of goals requires the coordinated execution and termination of actions that lead to positive outcomes. This process relies on motivational states that are guided by internal drivers, such as hunger or fear. However, the mechanisms by which the brain tracks motivational states to shape instrumental actions are not fully understood. The paraventricular nucleus of the thalamus (PVT) is a midline thalamic nucleus that shapes motivated behaviors via its projections to the nucleus accumbens (NAc)
MeSH term(s)	Mice ; Animals ; Motivation ; Nucleus Accumbens/physiology ; Thalamus ; Midline Thalamic Nuclei/physiology ; Hypothalamus
Language	English
Publishing date	2024-03-07
Publishing country	England
Document type	Journal Article
ZDB-ID	1071731-6
ISSN	1879-0445 ; 0960-9822
ISSN (online)	1879-0445
ISSN	0960-9822
DOI	10.1016/j.cub.2024.02.037
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Article ; Online: Molecular and spatial profiling of the paraventricular nucleus of the thalamus.

Gao, Claire / Gohel, Chiraag A / Leng, Yan / Ma, Jun / Goldman, David / Levine, Ariel J / Penzo, Mario A

eLife

2023 Volume 12

Abstract: The paraventricular nucleus of the thalamus (PVT) is known to regulate various cognitive and behavioral processes. However, while functional diversity among PVT circuits has often been linked to cellular differences, the molecular identity and spatial ... ...

Abstract	The paraventricular nucleus of the thalamus (PVT) is known to regulate various cognitive and behavioral processes. However, while functional diversity among PVT circuits has often been linked to cellular differences, the molecular identity and spatial distribution of PVT cell types remain unclear. To address this gap, here we used single nucleus RNA sequencing (snRNA-seq) and identified five molecularly distinct PVT neuronal subtypes in the mouse brain. Additionally, multiplex fluorescent in situ hybridization of top marker genes revealed that PVT subtypes are organized by a combination of previously unidentified molecular gradients. Lastly, comparing our dataset with a recently published single-cell sequencing atlas of the thalamus yielded novel insight into the PVT's connectivity with the cortex, including unexpected innervation of auditory and visual areas. This comparison also revealed that our data contains a largely non-overlapping transcriptomic map of multiple midline thalamic nuclei. Collectively, our findings uncover previously unknown features of the molecular diversity and anatomical organization of the PVT and provide a valuable resource for future investigations.
MeSH term(s)	Rats ; Mice ; Animals ; Paraventricular Hypothalamic Nucleus ; In Situ Hybridization, Fluorescence ; Rats, Sprague-Dawley ; Neural Pathways/physiology ; Thalamus ; Midline Thalamic Nuclei/metabolism
Language	English
Publishing date	2023-03-03
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Intramural
ZDB-ID	2687154-3
ISSN	2050-084X ; 2050-084X
ISSN (online)	2050-084X
ISSN	2050-084X
DOI	10.7554/eLife.81818
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Article ; Online: Divergent projections of the paraventricular nucleus of the thalamus mediate the selection of passive and active defensive behaviors.

Ma, Jun / du Hoffmann, Johann / Kindel, Morgan / Beas, B Sofia / Chudasama, Yogita / Penzo, Mario A

Nature neuroscience

2021 Volume 24, Issue 10, Page(s) 1429–1440

Abstract: The appropriate selection of passive and active defensive behaviors in threatening situations is essential for survival. Previous studies have shown that passive defensive responses depend on activity of the central nucleus of the amygdala (CeA), whereas ...

Abstract	The appropriate selection of passive and active defensive behaviors in threatening situations is essential for survival. Previous studies have shown that passive defensive responses depend on activity of the central nucleus of the amygdala (CeA), whereas active ones primarily rely on the nucleus accumbens (NAc). However, the mechanisms underlying flexible switching between these two types of responses remain unknown. Here we show in mice that the paraventricular thalamus (PVT) mediates the selection of defensive behaviors through its interaction with the CeA and the NAc. We show that the PVT-CeA pathway drives conditioned freezing responses, whereas the PVT-NAc pathway is inhibited during freezing and, instead, signals active avoidance events. Optogenetic manipulations revealed that activity in the PVT-CeA or PVT-NAc pathway biases behavior toward the selection of passive or active defensive responses, respectively. These findings provide evidence that the PVT mediates flexible switching between opposing defensive behaviors.
MeSH term(s)	Animals ; Avoidance Learning ; Behavior, Animal/physiology ; Mice ; Mice, Inbred C57BL ; Neural Pathways/physiology ; Optogenetics ; Paraventricular Hypothalamic Nucleus/physiology
Language	English
Publishing date	2021-08-19
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Intramural
ZDB-ID	1420596-8
ISSN	1546-1726 ; 1097-6256
ISSN (online)	1546-1726
ISSN	1097-6256
DOI	10.1038/s41593-021-00912-7
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Article ; Online: A distinct cortical code for socially learned threat.

Silverstein, Shana E / O'Sullivan, Ruairi / Bukalo, Olena / Pati, Dipanwita / Schaffer, Julia A / Limoges, Aaron / Zsembik, Leo / Yoshida, Takayuki / O'Malley, John J / Paletzki, Ronald F / Lieberman, Abby G / Nonaka, Mio / Deisseroth, Karl / Gerfen, Charles R / Penzo, Mario A / Kash, Thomas L / Holmes, Andrew

Nature

2024 Volume 626, Issue 8001, Page(s) 1066–1072

Abstract: Animals can learn about sources of danger while minimizing their own risk by observing how others respond to threats. However, the distinct neural mechanisms by which threats are learned through social observation (known as observational fear ... ...

Abstract	Animals can learn about sources of danger while minimizing their own risk by observing how others respond to threats. However, the distinct neural mechanisms by which threats are learned through social observation (known as observational fear learning
MeSH term(s)	Animals ; Mice ; Amygdala/physiology ; Calcium/metabolism ; Cues ; Electrophysiology ; Fear/physiology ; Hippocampus/physiology ; Neural Pathways/physiology ; Neurons/physiology ; Optogenetics ; Periaqueductal Gray/cytology ; Periaqueductal Gray/physiology ; Photic Stimulation ; Prefrontal Cortex/cytology ; Prefrontal Cortex/physiology ; Social Learning/physiology ; Freezing Reaction, Cataleptic/physiology
Chemical Substances	Calcium (SY7Q814VUP)
Language	English
Publishing date	2024-02-07
Publishing country	England
Document type	Journal Article
ZDB-ID	120714-3
ISSN	1476-4687 ; 0028-0836
ISSN (online)	1476-4687
ISSN	0028-0836
DOI	10.1038/s41586-023-07008-1
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Article ; Online: An inhibitory circuit from central amygdala to zona incerta drives pain-related behaviors in mice.

Singh, Sudhuman / Wilson, Torri D / Valdivia, Spring / Benowitz, Barbara / Chaudhry, Sarah / Ma, Jun / Adke, Anisha P / Soler-Cedeño, Omar / Velasquez, Daniela / Penzo, Mario A / Carrasquillo, Yarimar

eLife

2022 Volume 11

Abstract: Central amygdala neurons expressing protein kinase C-delta (CeA-PKCδ) are sensitized following nerve injury and promote pain-related responses in mice. The neural circuits underlying modulation of pain-related behaviors by CeA-PKCδ neurons, however, ... ...

Abstract	Central amygdala neurons expressing protein kinase C-delta (CeA-PKCδ) are sensitized following nerve injury and promote pain-related responses in mice. The neural circuits underlying modulation of pain-related behaviors by CeA-PKCδ neurons, however, remain unknown. In this study, we identified a neural circuit that originates in CeA-PKCδ neurons and terminates in the ventral region of the zona incerta (ZI), a subthalamic structure previously linked to pain processing. Behavioral experiments show that chemogenetic inhibition of GABAergic ZI neurons induced bilateral hypersensitivity in uninjured mice and contralateral hypersensitivity after nerve injury. In contrast, chemogenetic activation of GABAergic ZI neurons reversed nerve injury-induced hypersensitivity. Optogenetic manipulations of CeA-PKCδ axonal terminals in the ZI further showed that inhibition of this pathway reduces nerve injury-induced hypersensitivity whereas activation of the pathway produces hypersensitivity in the uninjured paws. Altogether, our results identify a novel nociceptive inhibitory efferent pathway from CeA-PKCδ neurons to the ZI that bidirectionally modulates pain-related behaviors in mice.
MeSH term(s)	Animals ; Mice ; Zona Incerta/physiology ; Central Amygdaloid Nucleus ; Pain ; GABAergic Neurons/physiology ; Optogenetics
Language	English
Publishing date	2022-10-21
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Intramural
ZDB-ID	2687154-3
ISSN	2050-084X ; 2050-084X
ISSN (online)	2050-084X
ISSN	2050-084X
DOI	10.7554/eLife.68760
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Article ; Online: Retinal innervation tunes circuits that drive nonphotic entrainment to food.

Fernandez, Diego Carlos / Komal, Ruchi / Langel, Jennifer / Ma, Jun / Duy, Phan Q / Penzo, Mario A / Zhao, Haiqing / Hattar, Samer

Nature

2020 Volume 581, Issue 7807, Page(s) 194–198

Abstract: Daily changes in light and food availability are major time cues that influence circadian ... ...

Abstract	Daily changes in light and food availability are major time cues that influence circadian timing
MeSH term(s)	Animals ; Axons/physiology ; Axons/radiation effects ; Circadian Rhythm/physiology ; Circadian Rhythm/radiation effects ; Cues ; Eating/physiology ; Eating/radiation effects ; Feeding Behavior/physiology ; Feeding Behavior/radiation effects ; Female ; Geniculate Bodies/cytology ; Geniculate Bodies/physiology ; Geniculate Bodies/radiation effects ; Light ; Male ; Mice ; Neural Pathways/radiation effects ; Neuropeptide Y/metabolism ; Retina/cytology ; Retina/physiology ; Retina/radiation effects ; Retinal Ganglion Cells/physiology ; Retinal Ganglion Cells/radiation effects ; Signal Transduction/radiation effects ; Suprachiasmatic Nucleus/cytology ; Suprachiasmatic Nucleus/physiology ; Suprachiasmatic Nucleus/radiation effects ; Time Factors
Chemical Substances	Neuropeptide Y
Language	English
Publishing date	2020-04-22
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, N.I.H., Intramural
ZDB-ID	120714-3
ISSN	1476-4687 ; 0028-0836
ISSN (online)	1476-4687
ISSN	0028-0836
DOI	10.1038/s41586-020-2204-1
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