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Article: Hippocampal neurogenesis facilitates cognitive flexibility in a fear discrimination task.

Martínez-Canabal, Alonso / López-Oropeza, Grecia / Sotres-Bayón, Francisco

2024 Volume 17, Page(s) 1331928

Abstract: Hippocampal neurogenesis, the continuous creation of new neurons in the adult brain, influences memory, regulates the expression of defensive responses to threat (fear), and cognitive processes like pattern separation and behavioral flexibility. One ... ...

Abstract	Hippocampal neurogenesis, the continuous creation of new neurons in the adult brain, influences memory, regulates the expression of defensive responses to threat (fear), and cognitive processes like pattern separation and behavioral flexibility. One hypothesis proposes that neurogenesis promotes cognitive flexibility by degrading established memories and promoting relearning. Yet, empirical evidence on its role in fear discrimination tasks is scarce. In this study, male rats were initially trained to differentiate between two similar environments, one associated with a threat. Subsequently, we enhanced neurogenesis through environmental enrichment and memantine treatments. We then reversed the emotional valence of these contexts. In both cases, neurogenesis improved the rats' ability to relearn the aversive context. Interestingly, we observed increased hippocampal activity, and decreased activity in the prelimbic cortex and lateral habenula, while the infralimbic cortex remained unchanged, suggesting neurogenesis-induced plasticity changes in this brain network. Moreover, when we pharmacologically inhibited the increased neurogenesis with Methotrexate, rats struggled to relearn context discrimination, confirming the crucial role of neurogenesis in this cognitive process. Overall, our findings highlight neurogenesis's capacity to facilitate changes in fear discrimination and emphasize the involvement of a prefrontal-hippocampal-habenula mechanism in this process. This study emphasizes the intricate relationship between hippocampal neurogenesis, cognitive flexibility, and the modulation of fear-related memories.
Language	English
Publishing date	2024-01-11
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2452960-6
ISSN	1662-5153
ISSN	1662-5153
DOI	10.3389/fnbeh.2023.1331928
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Article ; Online: Ventral pallidum and amygdala cooperate to restrain reward approach under threat.

Hernández-Jaramillo, Alejandra / Illescas-Huerta, Elizabeth / Sotres-Bayon, Francisco

The Journal of neuroscience : the official journal of the Society for Neuroscience

2024

Abstract: Foraging decisions involve assessing potential risks and prioritizing food sources, which can be difficult when confronted with changing and conflicting circumstances. A crucial aspect of this decision-making process is the ability to actively overcome ... ...

Abstract	Foraging decisions involve assessing potential risks and prioritizing food sources, which can be difficult when confronted with changing and conflicting circumstances. A crucial aspect of this decision-making process is the ability to actively overcome defensive reactions to threats and focus on achieving specific goals. The ventral pallidum (VP) and basolateral amygdala (BLA) are two brain regions that play key roles in regulating behavior motivated by either rewards or threats. However, it is unclear whether these regions are necessary in decision-making processes involving competing motivational drives during conflict. Our aim was to investigate the requirements of the VP and BLA for foraging choices in conflicts involving overcoming fear. Here, we used a novel foraging task and pharmacological techniques to inactivate either the VP or BLA, or to disconnect these brain regions before conducting a conflict test in male rats. Our findings showed that BLA is necessary for making risky choices during conflicts, whereas VP is necessary for invigorating the drive to obtain food, regardless of the presence of conflict. Importantly, our research revealed that the connection between VP and BLA is critical in limiting risk behaviors when searching for food requires effort in conflict situations. This study provides a new perspective on the collaborative function of VP and BLA in driving behavior, aimed at achieving goals in the face of dangers.
Language	English
Publishing date	2024-04-17
Publishing country	United States
Document type	Journal Article
ZDB-ID	604637-x
ISSN	1529-2401 ; 0270-6474
ISSN (online)	1529-2401
ISSN	0270-6474
DOI	10.1523/JNEUROSCI.2327-23.2024
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Article ; Online: Lateral Habenula Mediates Defensive Responses Only When Threat and Safety Memories Are in Conflict.

Velazquez-Hernandez, Geronimo / Sotres-Bayon, Francisco

eNeuro

2021 Volume 8, Issue 2

Abstract: Survival depends on the ability to adaptively react or execute actions based on previous aversive salient experiences. Although lateral habenula (LHb) activity has been broadly implicated in the regulation of aversively motivated responses, it is not ... ...

Abstract	Survival depends on the ability to adaptively react or execute actions based on previous aversive salient experiences. Although lateral habenula (LHb) activity has been broadly implicated in the regulation of aversively motivated responses, it is not clear under which conditions this brain structure is necessary to regulate defensive responses to a threat. To address this issue, we combined pharmacological inactivations with behavioral tasks that involve aversive and appetitive events and evaluated defensive responses in rats. We found that LHb pharmacological inactivation did not affect cued threat conditioning (fear) and extinction (safety) learning and memory, anxiety-like or reward-seeking behaviors. Surprisingly, we found that LHb inactivation abolished reactive defensive responses (tone-elicited freezing) only when threat (conditioning) and safety memories (extinction and latent inhibition) compete during retrieval. Consistently, we found that LHb inactivation impaired active defensive responses [platform-mediated avoidance (PMA)], thereby biasing choice behavior (between avoiding a threat or approaching food) toward reward-seeking responses. Together, our findings suggest that LHb activity mediates defensive responses only when guided by competing threat and safety memories, consequently revealing a previously uncharacterized role for LHb in experience-dependent emotional conflict.
MeSH term(s)	Animals ; Anxiety ; Fear ; Habenula ; Memory ; Rats ; Reward
Language	English
Publishing date	2021-04-19
Publishing country	United States
Document type	Journal Article
ZDB-ID	2800598-3
ISSN	2373-2822 ; 2373-2822
ISSN (online)	2373-2822
ISSN	2373-2822
DOI	10.1523/ENEURO.0482-20.2021
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Article: From Isolated Emotional Memories to Their Competition During Conflict.

Bravo-Rivera, Christian / Sotres-Bayon, Francisco

Frontiers in behavioral neuroscience

2020 Volume 14, Page(s) 36

Abstract: Aversive or rewarding experiences are remembered better than those of lesser survival significance. These emotional memories, whether negative or positive, leave traces in the brain which can later be retrieved and strongly influence how we perceive, how ...

Abstract	Aversive or rewarding experiences are remembered better than those of lesser survival significance. These emotional memories, whether negative or positive, leave traces in the brain which can later be retrieved and strongly influence how we perceive, how we form associations with environmental stimuli and, ultimately, guide our decision-making. In this review aticle, we outline what constitutes an emotional memory by focusing on threat- and reward-related memories and describe how they are formed in the brain during learning and reformed during retrieval. Finally, we discuss how the field is moving from understanding emotional memory brain circuits separately, towards studying how these two opposing brain systems interact to guide choices during conflict. Here, we outline two novel tasks in rodents that model opposing binary choices (approach or avoid) guided by competing emotional memories. The prefrontal cortex (PFC) is a major integration hub of emotional information which is also known to be critical for decision-making. Consequently, brain circuits that involve this brain region may be key for understanding how the retrieval of emotional memories flexibly orchestrates adaptive choice behavior. Because several mental disorders (e.g., drug addiction and depression) are characterized by deficits in decision-making in the face of conflicting emotional memories (maladaptively giving more weight to one memory over the other), the development of choice-based animal models for emotional regulation could give rise to new approaches for the treatment of these disorders in humans.
Language	English
Publishing date	2020-03-12
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2452960-6
ISSN	1662-5153
ISSN	1662-5153
DOI	10.3389/fnbeh.2020.00036
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Article: Conflict Test Battery for Studying the Act of Facing Threats in Pursuit of Rewards.

Illescas-Huerta, Elizabeth / Ramirez-Lugo, Leticia / Sierra, Rodrigo O / Quillfeldt, Jorge A / Sotres-Bayon, Francisco

Frontiers in neuroscience

2021 Volume 15, Page(s) 645769

Abstract: Survival depends on the ability of animals to avoid threats and approach rewards. Traditionally, these two opposing motivational systems have been studied separately. In nature, however, they regularly compete for the control of behavior. When threat- ... ...

Abstract	Survival depends on the ability of animals to avoid threats and approach rewards. Traditionally, these two opposing motivational systems have been studied separately. In nature, however, they regularly compete for the control of behavior. When threat- and reward-eliciting stimuli (learned or unlearned) occur simultaneously, a motivational conflict emerges that challenges individuals to weigh available options and execute a single behavioral response (avoid or approach). Most previous animal models using approach/avoidance conflicts have often focused on the ability to avoid threats by forgoing or delaying the opportunity to obtain rewards. In contrast, behavioral tasks designed to capitalize on the ability to actively choose to execute approach behaviors despite threats are scarce. Thus, we developed a behavioral test battery composed of three conflict tasks to directly study rats confronting threats to obtain rewards guided by innate and conditioned cues. One conflict task involves crossing a potentially electrified grid to obtain food on the opposite end of a straight alley, the second task is based on the step-down threat avoidance paradigm, and the third one is a modified version of the open field test. We used diazepam to pharmacologically validate conflict behaviors in our tasks. We found that, regardless of whether competing stimuli were conditioned or innate, a low diazepam dose decreased risk assessment and facilitated taking action to obtain rewards in the face of threats during conflict, without affecting choice behavior when there was no conflict involved. Using this pharmacologically validated test battery of ethologically designed innate/learned conflict tasks could help understand the fundamental brain mechanisms underlying the ability to confront threats to achieve goals.
Language	English
Publishing date	2021-05-04
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2411902-7
ISSN	1662-453X ; 1662-4548
ISSN (online)	1662-453X
ISSN	1662-4548
DOI	10.3389/fnins.2021.645769
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Article ; Online: Recurrent moderate hypoglycemia exacerbates oxidative damage and neuronal death leading to cognitive dysfunction after the hypoglycemic coma.

Languren, Gabriela / Montiel, Teresa / Ramírez-Lugo, Leticia / Balderas, Israela / Sánchez-Chávez, Gustavo / Sotres-Bayón, Francisco / Bermúdez-Rattoni, Federico / Massieu, Lourdes

Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism

2017 Volume 39, Issue 5, Page(s) 808–821

Abstract: Moderate recurrent hypoglycemia (RH) is frequent in Type 1 diabetes mellitus (TIDM) patients who are under intensive insulin therapy increasing the risk for severe hypoglycemia (SH). The consequences of RH are not well understood and its repercussions on ...

Abstract	Moderate recurrent hypoglycemia (RH) is frequent in Type 1 diabetes mellitus (TIDM) patients who are under intensive insulin therapy increasing the risk for severe hypoglycemia (SH). The consequences of RH are not well understood and its repercussions on neuronal damage and cognitive function after a subsequent episode of SH have been poorly investigated. In the current study, we have addressed this question and observed that previous RH during seven consecutive days exacerbated oxidative damage and neuronal death induced by a subsequent episode of SH accompanied by a short period of coma, in the parietal cortex, the striatum and mainly in the hippocampus. These changes correlated with a severe decrease in reduced glutathione content (GSH), and a significant spatial and contextual memory deficit. Administration of the antioxidant, N-acetyl-L-cysteine, (NAC) reduced neuronal death and prevented cognitive impairment. These results demonstrate that previous RH enhances brain vulnerability to acute hypoglycemia and suggests that this effect is mediated by the decline in the antioxidant defense and oxidative damage. The present results highlight the importance of an adequate control of moderate hypoglycemic episodes in TIDM.
MeSH term(s)	Animals ; Blood Glucose/metabolism ; Cell Death ; Cognitive Dysfunction/etiology ; Cognitive Dysfunction/metabolism ; Cognitive Dysfunction/pathology ; Coma/complications ; Coma/metabolism ; Coma/pathology ; Glutathione/metabolism ; Humans ; Hypoglycemia/complications ; Hypoglycemia/metabolism ; Hypoglycemia/pathology ; Male ; Neurons/metabolism ; Neurons/pathology ; Oxidative Stress ; Rats, Wistar
Chemical Substances	Blood Glucose ; Glutathione (GAN16C9B8O)
Language	English
Publishing date	2017-10-19
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	604628-9
ISSN	1559-7016 ; 0271-678X
ISSN (online)	1559-7016
ISSN	0271-678X
DOI	10.1177/0271678X17733640
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Article ; Online: Choice Behavior Guided by Learned, But Not Innate, Taste Aversion Recruits the Orbitofrontal Cortex.

Ramírez-Lugo, Leticia / Peñas-Rincón, Ana / Ángeles-Durán, Sandybel / Sotres-Bayon, Francisco

The Journal of neuroscience : the official journal of the Society for Neuroscience

2015 Volume 36, Issue 41, Page(s) 10574–10583

Abstract: The ability to select an appropriate behavioral response guided by previous emotional experiences is critical for survival. Although much is known about brain mechanisms underlying emotional associations, little is known about how these associations ... ...

Abstract	The ability to select an appropriate behavioral response guided by previous emotional experiences is critical for survival. Although much is known about brain mechanisms underlying emotional associations, little is known about how these associations guide behavior when several choices are available. To address this, we performed local pharmacological inactivations of several cortical regions before retrieval of an aversive memory in choice-based versus no-choice-based conditioned taste aversion (CTA) tasks in rats. Interestingly, we found that inactivation of the orbitofrontal cortex (OFC), but not the dorsal or ventral medial prefrontal cortices, blocked retrieval of choice CTA. However, OFC inactivation left retrieval of no-choice CTA intact, suggesting its role in guiding choice, but not in retrieval of CTA memory. Consistently, OFC activity increased in the choice condition compared with no-choice, as measured with c-Fos immunolabeling. Notably, OFC inactivation did not affect choice behavior when it was guided by innate taste aversion. Consistent with an anterior insular cortex (AIC) involvement in storing taste memories, we found that AIC inactivation impaired retrieval of both choice and no-choice CTA. Therefore, this study provides evidence for OFC's role in guiding choice behavior and shows that this is dissociable from AIC-dependent taste aversion memory. Together, our results suggest that OFC is required and recruited to guide choice selection between options of taste associations relayed from AIC. Significance statement: Survival and mental health depend on being able to choose stimuli not associated with danger. This is particularly important when danger is associated with stimuli that we ingest. Although much is known about the brain mechanisms that underlie associations with dangerous taste stimuli, very little is known about how these stored emotional associations guide behavior when it involves choice. By combining pharmacological and immunohistochemistry tools with taste-guided tasks, our study provides evidence for the key role of orbitofrontal cortex activity in choice behavior and shows that this is dissociable from the adjacent insular cortex-dependent taste aversion memory. Understanding the brain mechanisms that underlie the impact that emotional associations have on survival choice behaviors may lead to better treatments for mental disorders characterized by emotional decision-making deficits.
MeSH term(s)	Animals ; Avoidance Learning/drug effects ; Avoidance Learning/physiology ; Choice Behavior/drug effects ; Choice Behavior/physiology ; GABA Agonists/pharmacology ; Learning/drug effects ; Learning/physiology ; Male ; Memory/drug effects ; Muscimol/pharmacology ; Prefrontal Cortex/drug effects ; Prefrontal Cortex/physiology ; Proto-Oncogene Proteins c-fos/metabolism ; Rats ; Rats, Wistar ; Receptors, GABA-A/drug effects ; Receptors, GABA-B/drug effects ; Taste/drug effects ; Taste/physiology ; Taste Perception
Chemical Substances	GABA Agonists ; Proto-Oncogene Proteins c-fos ; Receptors, GABA-A ; Receptors, GABA-B ; Muscimol (2763-96-4)
Language	English
Publishing date	2015-12-18
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	604637-x
ISSN	1529-2401 ; 0270-6474
ISSN (online)	1529-2401
ISSN	0270-6474
DOI	10.1523/JNEUROSCI.0796-16.2016
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Article ; Online: Prefrontal control of fear: more than just extinction.

Sotres-Bayon, Francisco / Quirk, Gregory J

Current opinion in neurobiology

2010 Volume 20, Issue 2, Page(s) 231–235

Abstract: Although fear research has largely focused on the amygdala, recent findings highlight cortical control of the amygdala in the service of fear regulation. In rodent models, it is becoming well established that the infralimbic (IL) prefrontal cortex plays ... ...

Abstract	Although fear research has largely focused on the amygdala, recent findings highlight cortical control of the amygdala in the service of fear regulation. In rodent models, it is becoming well established that the infralimbic (IL) prefrontal cortex plays a key role in extinction learning, and recent findings are uncovering molecular mechanisms involved in extinction-related plasticity. Furthermore, mounting evidence implicates the prelimbic (PL) prefrontal cortex in the production of fear responses. Both IL and PL integrate inputs from the amygdala, as well as other structures to gate the expression of fear via projections to inhibitory or excitatory circuits within the amygdala. We suggest that dual control of the amygdala by separate prefrontal modules increases the flexibility of an organism's response to danger cues.
MeSH term(s)	Affect/physiology ; Amygdala/anatomy & histology ; Amygdala/physiology ; Animals ; Association Learning/physiology ; Behavior/physiology ; Extinction, Psychological/physiology ; Fear/physiology ; Humans ; Neural Pathways/anatomy & histology ; Neural Pathways/physiology ; Neuronal Plasticity/physiology ; Prefrontal Cortex/anatomy & histology ; Prefrontal Cortex/physiology
Language	English
Publishing date	2010-03-18
Publishing country	England
Document type	Journal Article ; Review
ZDB-ID	1078046-4
ISSN	1873-6882 ; 0959-4388
ISSN (online)	1873-6882
ISSN	0959-4388
DOI	10.1016/j.conb.2010.02.005
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Zs.A 3260: Show issues

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Article ; Online: Hippocampal neurogenesis regulates recovery of defensive responses by recruiting threat- and extinction-signalling brain networks.

Martínez-Canabal, Alonso / López-Oropeza, Grecia / Gaona-Gamboa, Abril / Ballesteros-Zebadua, Paola / de la Cruz, Olinca Galvan / Moreno-Jimenez, Sergio / Sotres-Bayon, Francisco

Scientific reports

2019 Volume 9, Issue 1, Page(s) 2939

Abstract: Safe exposure to a context that was previously associated with threat leads to extinction of defensive responses. Such contextual fear extinction involves the formation of a new memory that inhibits a previously acquired contextual fear memory. However, ... ...

Abstract	Safe exposure to a context that was previously associated with threat leads to extinction of defensive responses. Such contextual fear extinction involves the formation of a new memory that inhibits a previously acquired contextual fear memory. However, fear-related responses often return with the simple passage of time (spontaneous fear recovery). Given that contextual fear and extinction memories are hippocampus-dependent and hippocampal neurogenesis has been reported to modify preexisting memories, we hypothesized that neurogenesis-mediated modification of preexisting extinction memory would modify spontaneous fear recovery. To test this, rats underwent contextual fear conditioning followed by extinction. Subsequently, we exposed rats to an enriched environment or focal X-irradiation to enhance or ablate hippocampal neurogenesis, respectively. Over a month later, rats were tested to evaluate spontaneous fear recovery. We found that enhancing neurogenesis after, but not before, extinction prevented fear recovery. In contrast, neurogenesis ablation after, but not before, extinction promoted fear recovery. Using the neuronal activity marker c-Fos, we identified brain regions recruited in these opposing neurogenesis-mediated changes during fear recovery. Together, our findings indicate that neurogenesis manipulation after extinction learning modifies fear recovery by recruiting brain network activity that mediates the expression of preexisting contextual fear and extinction memories.
MeSH term(s)	Animals ; Behavior, Animal/physiology ; Conditioning, Psychological/physiology ; Extinction, Psychological/physiology ; Fear/physiology ; Hippocampus/growth & development ; Male ; Memory/physiology ; Neurogenesis/physiology ; Neurons/physiology ; Proto-Oncogene Proteins c-fos/metabolism ; Rats ; Rats, Wistar
Chemical Substances	Proto-Oncogene Proteins c-fos
Language	English
Publishing date	2019-02-27
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2615211-3
ISSN	2045-2322 ; 2045-2322
ISSN (online)	2045-2322
ISSN	2045-2322
DOI	10.1038/s41598-019-39136-y
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Article: Reimplantable Microdrive for Long-Term Chronic Extracellular Recordings in Freely Moving Rats.

Polo-Castillo, Leopoldo Emmanuel / Villavicencio, Miguel / Ramírez-Lugo, Leticia / Illescas-Huerta, Elizabeth / Moreno, Mario Gil / Ruiz-Huerta, Leopoldo / Gutierrez, Ranier / Sotres-Bayon, Francisco / Caballero-Ruiz, Alberto

Frontiers in neuroscience

2019 Volume 13, Page(s) 128

Abstract: Extracellular recordings of electrical activity in freely moving rats are fundamental to understand brain function in health and disease. Such recordings require a small-size, lightweight device that includes movable electrodes (microdrive) to record ... ...

Abstract	Extracellular recordings of electrical activity in freely moving rats are fundamental to understand brain function in health and disease. Such recordings require a small-size, lightweight device that includes movable electrodes (microdrive) to record either a new set of neurons every day or the same set of neurons over time. Ideally, microdrives should be easy to implant, allowing precise and smooth displacement of electrodes. The main caveat of most commercially available microdrives is their relatively short half-life span, in average ranging from weeks to a month. For most experiments, recording days-weeks is sufficient, but when the experiment depends on training animals for several months, it is crucial to develop new approaches. Here, we present a low-cost, reusable, and reimplantable device design as a solution to extend chronic recordings to long-term. This device is composed of a baseplate that is permanently fixed to the rodent's skull, as well as a reusable and replaceable microdrive that can be attached and detached from the baseplate, allowing its implantation and reimplantation. Reimplanting this microdrive is particularly convenient when no clear neuronal signal is present, or when the signal gradually decays across days. Our microdrive incorporates a mechanism for moving a 16 tungsten-wire bundle within a small (∼15 mm
Language	English
Publishing date	2019-02-21
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2411902-7
ISSN	1662-453X ; 1662-4548
ISSN (online)	1662-453X
ISSN	1662-4548
DOI	10.3389/fnins.2019.00128
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