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Article ; Online: Context fear learning and renewal of extinguished fear are dissociated in juvenile female rats.

Park, Chun Hui J / Ganella, Despina E / Kim, Jee Hyun

2019 Volume 62, Issue 1, Page(s) 123–129

Abstract: Extinction is the decrease in emotion to a cue that was previously associated with an emotionally significant event. It involves repeated presentation of the cue without any consequences. In adult animals, extinguished fear to a cue can return if the cue ...

Abstract	Extinction is the decrease in emotion to a cue that was previously associated with an emotionally significant event. It involves repeated presentation of the cue without any consequences. In adult animals, extinguished fear to a cue can return if the cue is presented in a different environment/context to where extinction occurred, referred to as renewal. We have previously reported that developing female, but not male, rats show renewal. This study investigates whether the ability of developing female rats to show renewal is related to their ability in fear conditioning to the context. Additionally, facilitation of context conditioning by weaning previously shown in male rats was tested in developing female rats. In experiment 1, postnatal day 25 (P25) and P18 female rats showed renewal. P25 rats show more fear overall, suggesting a weaker extinction recall in this age. Experiment 2 tested context- and cue-elicited fear either immediately or 24 hr following conditioning. At the immediate test, P18 rats showed less context-fear compared with P25 rats. All rats showed low levels of context-fear at the 24 hr test. There were no age differences in cued fear. Weaning at P21 did not affect context or cue memory in P25 female rats. These findings suggest that the ability to form contextual fear memory is unrelated to the expression of renewal in juvenile female rats.
MeSH term(s)	Age Factors ; Animals ; Behavior, Animal/physiology ; Conditioning, Psychological/physiology ; Cues ; Extinction, Psychological/physiology ; Fear/physiology ; Female ; Rats ; Rats, Sprague-Dawley
Language	English
Publishing date	2019-07-02
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	4107-5
ISSN	1098-2302 ; 0012-1630
ISSN (online)	1098-2302
ISSN	0012-1630
DOI	10.1002/dev.21888
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Article ; Online: Dissociated roles of dorsal and ventral hippocampus in recall and extinction of conditioned fear in male and female juvenile rats.

Park, Chun Hui J / Ganella, Despina E / Perry, Christina J / Kim, Jee Hyun

Experimental neurology

2020 Volume 329, Page(s) 113306

Abstract: Reduction of conditioned fear expression by extinction underlies cue exposure therapies that treat anxiety disorders. Extinction is context-specific. Renewal, for example, is the relapse of extinguished fear when subjects are tested in a different ... ...

Abstract	Reduction of conditioned fear expression by extinction underlies cue exposure therapies that treat anxiety disorders. Extinction is context-specific. Renewal, for example, is the relapse of extinguished fear when subjects are tested in a different context to extinction. This context-specificity is developmentally regulated and sex-dependent, with renewal being observed in postnatal day (P) 18 female, but not in male, rats. Given the hippocampus (HPC) is critical for context-specific extinction in adult rodents, we investigated dorsal or ventral hippocampus (dHPC or vHPC) involvement in context-specific extinction in P18 male and female rats. We microinfused muscimol (GABA
MeSH term(s)	Animals ; Conditioning, Classical/drug effects ; Conditioning, Classical/physiology ; Extinction, Psychological/drug effects ; Extinction, Psychological/physiology ; Fear/drug effects ; Fear/physiology ; Fear/psychology ; Female ; GABA-A Receptor Agonists/administration & dosage ; Hippocampus/drug effects ; Hippocampus/physiology ; Infusions, Intraventricular ; Male ; Mental Recall/drug effects ; Mental Recall/physiology ; Muscimol/administration & dosage ; Rats ; Rats, Sprague-Dawley
Chemical Substances	GABA-A Receptor Agonists ; Muscimol (2763-96-4)
Language	English
Publishing date	2020-04-10
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	207148-4
ISSN	1090-2430 ; 0014-4886
ISSN (online)	1090-2430
ISSN	0014-4886
DOI	10.1016/j.expneurol.2020.113306
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Article ; Online: A dissociation between renewal and contextual fear conditioning in juvenile rats.

Park, Chun Hui J / Ganella, Despina E / Kim, Jee Hyun

Developmental psychobiology

2017 Volume 59, Issue 4, Page(s) 515–522

Abstract: We investigated whether juvenile rats do not express renewal following extinction of conditioned fear due to their inability to form a long-term contextual fear memory. In experiment 1, postnatal day (P) 18 and 25 rats received 3 white-noise and ... ...

Abstract	We investigated whether juvenile rats do not express renewal following extinction of conditioned fear due to their inability to form a long-term contextual fear memory. In experiment 1, postnatal day (P) 18 and 25 rats received 3 white-noise and footshock pairings, followed by 60 white-noise alone presentations the next day. When tested in a different context to extinction, P25 rats displayed renewal whereas P18 rats did not. Experiments 2A and 2B surprisingly showed that P18 and P25 rats do not show differences in contextual and cued fear, regardless of the conditioning-test intervals and the number of white-noise-footshock pairings received. Finally, we observed age differences in contextual fear when P25 rats were weaned at P21 in experiment 3. These results indicate that the developmental dissociation observed in renewal of extinguished fear is not related to the widely believed late emergence of contextual fear learning.
Language	English
Publishing date	2017-05
Publishing country	United States
Document type	Journal Article
ZDB-ID	4107-5
ISSN	1098-2302 ; 0012-1630
ISSN (online)	1098-2302
ISSN	0012-1630
DOI	10.1002/dev.21516
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Article: Extinction of Conditioned Fear in Adolescents and Adults: A Human fMRI Study.

Ganella, Despina E / Drummond, Katherine D / Ganella, Eleni P / Whittle, Sarah / Kim, Jee Hyun

Frontiers in human neuroscience

2018 Volume 11, Page(s) 647

Abstract: Little is known about the neural correlates of fear learning in adolescents, a population at increased risk for anxiety disorders. Healthy adolescents (mean age 16.26) and adults (mean age 29.85) completed a fear learning paradigm across two stages ... ...

Abstract	Little is known about the neural correlates of fear learning in adolescents, a population at increased risk for anxiety disorders. Healthy adolescents (mean age 16.26) and adults (mean age 29.85) completed a fear learning paradigm across two stages during functional magnetic resonance imaging (fMRI). Stage 1 involved conditioning and extinction, and stage 2 involved extinction recall, re-conditioning, followed by re-extinction. During extinction recall, we observed a higher skin conductance response to the CS+ relative to CS- in adolescents compared to adults, which was accompanied by a reduction in dorsolateral prefrontal cortex (dlPFC) activity. Relative to adults, adolescents also had significantly reduced activation in the ventromedial PFC, dlPFC, posterior cingulate cortex (PCC), and temporoparietal junction (TPJ) during extinction recall compared to late extinction. Age differences in PCC activation between late extinction and late conditioning were also observed. These results show for the first time that healthy adolescent humans show different behavioral responses, and dampened PFC activity during short-term extinction recall compared to healthy adults. We also identify the PCC and TPJ as novel regions that may be associated with impaired extinction in adolescents. Also, while adults showed significant correlations between differential SCR and BOLD activity in some brain regions during late extinction and recall, adolescents did not show any significant correlations. This study highlights adolescent-specific neural correlates of extinction, which may explain the peak in prevalence of anxiety disorders during adolescence.
Language	English
Publishing date	2018-01-08
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2425477-0
ISSN	1662-5161
ISSN	1662-5161
DOI	10.3389/fnhum.2017.00647
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Article ; Online: Juvenile female rats, but not male rats, show renewal, reinstatement, and spontaneous recovery following extinction of conditioned fear.

Park, Chun Hui J / Ganella, Despina E / Kim, Jee Hyun

Learning & memory (Cold Spring Harbor, N.Y.)

2017 Volume 24, Issue 12, Page(s) 630–636

Abstract: Anxiety disorders emerge early, and girls are significantly more likely to develop anxiety compared to boys. However, sex differences in fear during development are poorly understood. Therefore, we investigated juvenile male and female rats in the ... ...

Abstract	Anxiety disorders emerge early, and girls are significantly more likely to develop anxiety compared to boys. However, sex differences in fear during development are poorly understood. Therefore, we investigated juvenile male and female rats in the relapse behaviors following extinction of conditioned fear. In all experiments, 18-d-old rats first received three white-noise-footshock pairings on day 1. On day 2, extinction involved 60 white-noise alone trials. In experiment 1, we examined renewal by testing the rats in either the same or different context as extinction on day 3. Male rats did not show renewal, however, female rats showed renewal. Experiment 2 investigated reinstatement by giving rats either a mild reminder footshock or context exposure on day 3. When tested the next day, male rats did not show reinstatement, whereas female rats showed reinstatement. Experiment 3 investigated spontaneous recovery by testing the rats either 1 or 5 d following extinction. Male rats did not show any spontaneous recovery whereas female rats did. Taken together, fear regulation appear to be different in males versus females from early in development, which may explain why girls are more prone to suffer from anxiety disorders compared to boys.
MeSH term(s)	Analysis of Variance ; Animals ; Animals, Newborn ; Conditioning, Classical/physiology ; Extinction, Psychological/physiology ; Fear ; Female ; Freezing Reaction, Cataleptic/physiology ; Male ; Rats ; Rats, Sprague-Dawley ; Recovery of Function/physiology ; Sex Characteristics
Language	English
Publishing date	2017-12
Publishing country	United States
Document type	Journal Article
ZDB-ID	1204777-6
ISSN	1549-5485 ; 1072-0502
ISSN (online)	1549-5485
ISSN	1072-0502
DOI	10.1101/lm.045831.117
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Zs.A 4107: Show issues

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Article ; Online: Developmental rodent models of fear and anxiety: from neurobiology to pharmacology.

Ganella, Despina E / Kim, Jee Hyun

British journal of pharmacology

2014 Volume 171, Issue 20, Page(s) 4556–4574

Abstract: Anxiety disorders pose one of the biggest threats to mental health in the world, and they predominantly emerge early in life. However, research of anxiety disorders and fear-related memories during development has been largely neglected, and existing ... ...

Abstract	Anxiety disorders pose one of the biggest threats to mental health in the world, and they predominantly emerge early in life. However, research of anxiety disorders and fear-related memories during development has been largely neglected, and existing treatments have been developed based on adult models of anxiety. The present review describes animal models of anxiety disorders across development and what is currently known of their pharmacology. To summarize, the underlying mechanisms of intrinsic 'unlearned' fear are poorly understood, especially beyond the period of infancy. Models using 'learned' fear reveal that through development, rats exhibit a stress hyporesponsive period before postnatal day 10, where they paradoxically form odour-shock preferences, and then switch to more adult-like conditioned fear responses. Juvenile rats appear to forget these aversive associations more easily, as is observed with the phenomenon of infantile amnesia. Juvenile rats also undergo more robust extinction, until adolescence where they display increased resistance to extinction. Maturation of brain structures, such as the amygdala, prefrontal cortex and hippocampus, along with the different temporal recruitment and involvement of various neurotransmitter systems (including NMDA, GABA, corticosterone and opioids) are responsible for these developmental changes. Taken together, the studies described in this review highlight that there is a period early in development where rats appear to be more robust in overcoming adverse early life experience. We need to understand the fundamental pharmacological processes underlying anxiety early in life in order to take advantage of this period for the treatment of anxiety disorders.
MeSH term(s)	Animals ; Anxiety/drug therapy ; Anxiety/physiopathology ; Anxiety/psychology ; Avoidance Learning ; Brain/physiology ; Disease Models, Animal ; Fear/physiology ; Fear/psychology ; Humans ; Reflex, Startle ; Synaptic Transmission/physiology ; Vocalization, Animal
Language	English
Publishing date	2014-07-01
Publishing country	England
Document type	Journal Article ; Review
ZDB-ID	80081-8
ISSN	1476-5381 ; 0007-1188
ISSN (online)	1476-5381
ISSN	0007-1188
DOI	10.1111/bph.12643
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Article ; Online: Chronic activation of the relaxin-3 receptor on GABA neurons in rat ventral hippocampus promotes anxiety and social avoidance.

Rytova, Valeria / Ganella, Despina E / Hawkes, David / Bathgate, Ross A D / Ma, Sherie / Gundlach, Andrew L

Hippocampus

2019 Volume 29, Issue 10, Page(s) 905–920

Abstract: Anxiety disorders are highly prevalent in modern society and better treatments are required. Key brain areas and signaling systems underlying anxiety include prefrontal cortex, hippocampus, and amygdala, and monoaminergic and peptidergic systems, ... ...

Abstract	Anxiety disorders are highly prevalent in modern society and better treatments are required. Key brain areas and signaling systems underlying anxiety include prefrontal cortex, hippocampus, and amygdala, and monoaminergic and peptidergic systems, respectively. Hindbrain GABAergic projection neurons that express the peptide, relaxin-3, broadly innervate the forebrain, particularly the septum and hippocampus, and relaxin-3 acts via a G
MeSH term(s)	Animals ; Anxiety/metabolism ; Behavior, Animal/drug effects ; Behavior, Animal/physiology ; GABAergic Neurons/drug effects ; GABAergic Neurons/metabolism ; Hippocampus/drug effects ; Hippocampus/metabolism ; Male ; Rats ; Rats, Sprague-Dawley ; Receptors, G-Protein-Coupled/agonists ; Receptors, G-Protein-Coupled/metabolism ; Receptors, Peptide/agonists ; Receptors, Peptide/metabolism ; Social Behavior
Chemical Substances	RXFP3 protein, rat ; Receptors, G-Protein-Coupled ; Receptors, Peptide
Language	English
Publishing date	2019-03-19
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1074352-2
ISSN	1098-1063 ; 1050-9631
ISSN (online)	1098-1063
ISSN	1050-9631
DOI	10.1002/hipo.23089
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Article: Prefrontal-Amygdala Connectivity and State Anxiety during Fear Extinction Recall in Adolescents.

Ganella, Despina E / Barendse, Marjolein E A / Kim, Jee H / Whittle, Sarah

Frontiers in human neuroscience

2017 Volume 11, Page(s) 587

Abstract: While deficits in fear extinction recall have been suggested to underlie vulnerability to anxiety disorders in adolescents, the neurobiology of these deficits remain underexplored. Here we investigate the functional connectivity (FC) of the ventromedial ... ...

Abstract	While deficits in fear extinction recall have been suggested to underlie vulnerability to anxiety disorders in adolescents, the neurobiology of these deficits remain underexplored. Here we investigate the functional connectivity (FC) of the ventromedial prefrontal cortex (vmPFC) and dorsolateral PFC (dlPFC) underlying extinction recall in healthy adolescents, and assess associations between FC and state/trait anxiety. Adolescents (17) and adults (14, for comparison) completed a fear-learning paradigm involving extinction and extinction recall during a functional magnetic resonance imaging session, in which skin conductance response (SCR) was recorded. Psychophysiological interaction analyses revealed that during extinction recall there was significant negative connectivity between the vmPFC and amygdala in adults, but not adolescents. vmPFC-amygdala connectivity was positively correlated with SCR. Adolescents showed significant negative FC between the dlPFC and the left and right hippocampus, and the amygdala, which was positively correlated with state anxiety. Recall was also associated with negative connectivity between the dlPFC and thalamus, posterior cingulate cortex, fusiform gyrus, and pallidum in adolescents. These results demonstrate that fear extinction recall in healthy adolescents is associated with FC between prefrontal and limbic brain regions, and suggest that alterations in connectivity may be associated with vulnerability to anxiety in adolescence.
Language	English
Publishing date	2017-12-04
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2425477-0
ISSN	1662-5161
ISSN	1662-5161
DOI	10.3389/fnhum.2017.00587
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Article ; Online: Postnatal development of neurotransmitter systems and their relevance to extinction of conditioned fear.

Kim, Jee Hyun / Perry, Christina J / Ganella, Despina E / Madsen, Heather B

Neurobiology of learning and memory

2017 Volume 138, Page(s) 252–270

Abstract: Remembering and forgetting are fundamental features of an organism. Extinction is a type of forgetting where there is a decrease in the significance and/or the meaning of an associative memory when elements of that memory no longer predict one another. ... ...

Abstract	Remembering and forgetting are fundamental features of an organism. Extinction is a type of forgetting where there is a decrease in the significance and/or the meaning of an associative memory when elements of that memory no longer predict one another. The neural mechanisms underlying extinction of fear memories have been extensively studied in the laboratory because extinction processes are clinically relevant to exposure therapies that treat anxiety disorders. However, only in the last decade have we begun to unveil the similarities and differences in plasticity underlying extinction across development. So far it is clear that extinction is a developmentally dissociated process in behavior and in pharmacology, however there are many large gaps in the literature in understanding how the developmental trajectory of different neurotransmitters contribute to changes in the nature of extinction across development. We attempt to address these gaps in the present review. Major neurotransmitter systems including the glutamatergic and GABAergic systems, the monoamines, the endogenous opioid and cannabinoid systems, acetylcholines, and neuropeptides such as oxytocin have all been identified to play some role in extinction of fear memories and have been covered in this review. We hope to facilitate more research into mechanisms of extinction at different stages of life, especially noting that mental disorders are increasingly classified as neurodevelopmental disorders.
Language	English
Publishing date	2017-02
Publishing country	United States
Document type	Journal Article ; Review
ZDB-ID	1223366-3
ISSN	1095-9564 ; 1074-7427
ISSN (online)	1095-9564
ISSN	1074-7427
DOI	10.1016/j.nlm.2016.10.018
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Article ; Online: Associations between early life stress and anterior pituitary gland volume development - A novel index of long-term hypothalamic-pituitary-adrenal axis functioning.

Díaz-Arteche, Carmela / Simmons, Julian G / Ganella, Despina E / Schwartz, Orli / Kim, Jee Hyun / Farrow, Paige / Whittle, Sarah

Developmental psychobiology

2020 Volume 63, Issue 4, Page(s) 808–816

Abstract: Previous research has established associations between early life stress (ELS) and altered pituitary gland volume (PGV) growth during adolescence. The pituitary gland, however, is composed of an anterior and a posterior lobe with distinct histological ... ...

Abstract	Previous research has established associations between early life stress (ELS) and altered pituitary gland volume (PGV) growth during adolescence. The pituitary gland, however, is composed of an anterior and a posterior lobe with distinct histological and neuroendocrinological properties. While the anterior (but not posterior) pituitary gland is directly involved in the hypothalamic-pituitary-adrenal axis (HPAA) stress response, no studies have examined the effects of ELS on anterior PGV (aPGV). The present study investigated whether previously reported associations between ELS and PGV development during adolescence were driven by aPGV versus posterior PGV (pPGV). Ninety-one adolescents (49 males) were included from a longitudinal, community-based adolescent development study investigating risk for psychopathology. ELS (maternal affective behavior, childhood maltreatment, stressful life events) was assessed during early adolescence. Participants underwent two waves of structural magnetic resonance imaging during mid- and late-adolescence, and aPGV and pPGV were manually traced. Regression analyses showed that childhood maltreatment predicted greater aPGV growth in females. This finding was stronger than that previously reported for PGV. No associations were found between ELS and pPGV development. Neither aPGV nor pPGV changes mediated associations between ELS and psychopathology. Results suggest that ELS may accelerate aPGV (but not pPGV) growth throughout adolescence. Investigating the development of aPGV, rather than PGV, represents a novel approach to studying the effects of stress on HPAA functioning.
MeSH term(s)	Adolescent ; Adverse Childhood Experiences ; Female ; Humans ; Hypothalamo-Hypophyseal System/physiology ; Male ; Pituitary Gland ; Pituitary Gland, Anterior ; Pituitary-Adrenal System/physiology ; Stress, Psychological
Language	English
Publishing date	2020-10-19
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	4107-5
ISSN	1098-2302 ; 0012-1630
ISSN (online)	1098-2302
ISSN	0012-1630
DOI	10.1002/dev.22047
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