Heat exposure in female rats elicits abnormal fear expression and cellular changes in prefrontal cortex and hippocampus

Gruene, Tina; Lipps, Jennifer; Rey, Colin D.; Bouck, Anna; Shansky, Rebecca M.

doi:10.1016/j.nlm.2014.05.004

Cited by 13 publications

(10 citation statements)

References 30 publications

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“…In physiological studies, PL activity has been linked to elevated freezing during extinction in females but not males (31), suggesting that the PL may play a distinctly important role in females. We recently found that impaired extinction retrieval in female rats was associated with a switch in the balance of IL and PL c-fos expression, such that PL neurons were more active than those in the IL, while the reverse was the case in animals exhibiting good extinction retrieval (12). Therefore, freezing behavior in females may rely more closely on IL-PL and/or PL-BLA circuits, while IL-BLA projections are less involved.…”

Section: Discussionmentioning

confidence: 99%

“…Rats underwent habituation, fear conditioning and fear extinction as in (12) in one of four identical chambers constructed of aluminum and Plexiglas walls (Rat Test Cage, Coulbourn Instruments, Allentown, PA), with metal stainless steel rod flooring that was attached to a shock generator (Model H13–15; Coulbourn Instruments). The chambers were lit with a single house light, and each chamber was enclosed within a sound-isolation cubicle (Model H10–24A; Coulbourn Instruments).…”

Section: Methodsmentioning

confidence: 99%

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Sex-Specific Neuroanatomical Correlates of Fear Expression in Prefrontal-Amygdala Circuits

Gruene

Roberts

Thomas

et al. 2015

Biological Psychiatry

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131

109

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Background The neural projections from the infralimbic region of the prefrontal cortex (IL) to the amygdala are important for the maintenance of conditioned fear extinction. Neurons in this pathway exhibit a unique pattern of structural plasticity that is sex-dependent, but the relationship between the morphological characteristics of these neurons and successful extinction in males and females is unknown. Methods Using classic cued fear conditioning and extinction paradigm in large cohorts of male and female rats, we identified subpopulations of both sexes that exhibited high (HF) or low (LF) levels of freezing on an extinction retrieval test, representing failed or successful extinction maintenance, respectively. We then combined retrograde tracing with fluorescent intracellular microinjections to perform 3D reconstructions of IL neurons that project to the basolateral amygdala (BLA) in these groups. Results HF/LF males exhibited neuroanatomical distinctions that were not observed in HF vs. LF females. A retrospective analysis of behavior during fear conditioning and extinction revealed that despite no overall sex differences in freezing behavior, HF/LF phenotypes emerged in males during extinction, but in females during fear conditioning, which does not involve IL-BLA neurons. Conclusion Our results suggest that the neural processes underlying successful or failed extinction maintenance may be sex-specific. These findings are not only relevant to future basic research on sex differences in fear conditioning and extinction, but also to exposure-based clinical therapies, which are similar in premise to fear extinction, and which are primarily used to treat disorders that are more common in women than in men.

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Sex-Specific Neuroanatomical Correlates of Fear Expression in Prefrontal-Amygdala Circuits

Gruene

Roberts

Thomas

et al. 2015

Biological Psychiatry

Self Cite

131

109

View full text Add to dashboard Cite

show abstract

“…But Chang et al used the contextual fear paradigm in mice and observed that males showed more freezing both in acquisition and extinction [48]. Gruene et al [49] conducted a large-sample analysis of fear conditioning and extinction in large cohorts of gonadally intact male and female rats. They found that there were no gender differences in freezing over the course of fear conditioning, fear extinction and extinction recall.…”

Section: Gender Differences In Fear and Their Neural Basismentioning

confidence: 99%

Gender Differences in PTSD: Susceptibility and Resilience

Hu¹,

Biao²,

Zhu³

et al. 2017

Gender Differences in Different Contexts

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“…Additionally, future research should analyze morphology of specific subtypes of neurons that have a closer link to behavioral outcome measures. This can be achieved by combining retrograde tracer labelling (Gruene et al, 2014; Radley et al, 2013; Shansky et al, 2010, 2009) with iontophoretic microinjection, or by targeting neurons that express a marker of neuronal activity indicating their involvement during a certain behavioral paradigm. Finally, a more direct way to uncover a causal link between dendritic structure and function is to pharmacologically manipulate dendritic length or spine density and then determine a behavioral outcome.…”

Section: Discussionmentioning

confidence: 99%

“…However, another group looking at chronic stress and estradiol administration to OVX rats found a significant negative correlation between CA1 spine density and spatial memory on an object placement task (Conrad et al, 2012). Finally, we have recently reported that heat stress-exposed female rats had increased head diameter of mushroom spines within CA3 that was associated with enhanced freezing during extinction and extinction retrieval (Gruene et al, 2014). …”

Section: Relationships Between Experience-dependent Alterations In Himentioning

confidence: 99%

The influence of stress and gonadal hormones on neuronal structure and function

Farrell

Gruene

Shansky

2015

Hormones and Behavior

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The brain is highly plastic, allowing us to adapt and respond to environmental and physiological challenges and experiences. In this review, we discuss the relationships among alterations in dendritic arborization, spine morphology, and behavior due to stress exposure, endogenous hormone fluctuation, or exogenous hormonal manipulation. Very few studies investigate structure-function associations directly in the same cohort of animals, and there are notable inconsistencies in evidence of structure-function relationships in the prefrontal cortex and hippocampus. Moreover, little work has been done to probe the causal relationship between dendritic morphology and neuronal excitability, leaving only speculation about the adaptive versus maladaptive nature of experience-dependent dendritic remodeling. We propose that future studies combine electrophysiology with a circuit-level approach to better understand how dendritic structure contributes to neuronal functional properties and behavioral outcomes.

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Heat exposure in female rats elicits abnormal fear expression and cellular changes in prefrontal cortex and hippocampus

Cited by 13 publications

References 30 publications

Sex-Specific Neuroanatomical Correlates of Fear Expression in Prefrontal-Amygdala Circuits

Sex-Specific Neuroanatomical Correlates of Fear Expression in Prefrontal-Amygdala Circuits

Gender Differences in PTSD: Susceptibility and Resilience

The influence of stress and gonadal hormones on neuronal structure and function

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