Distinct Effects of Repeated Restraint Stress on Basolateral Amygdala Neuronal Membrane Properties in Resilient Adolescent and Adult Rats

Hetzel, Andrea; Rosenkranz, J Amiel

doi:10.1038/npp.2014.60

Cited by 62Stress Responses and CortisolNeuroscience and Neuropharmacology ResearchMemory and Neural Mechanisms

Distinct Effects of Repeated Restraint Stress on Basolateral Amygdala Neuronal Membrane Properties in Resilient Adolescent and Adult Rats

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Hetzel, Andrea, Rosenkranz, J Amiel·2014·Neuropsychopharmacology

DOI 10.1038/npp.2014.60PMC PMC4104329

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Abstract

Severe and repeated stress has damaging effects on health, including initiation of depression and anxiety. Stress that occurs during development has long-lasting and particularly damaging effects on emotion. The basolateral amygdala (BLA) plays a key role in many affective behaviors, and repeated stress causes different forms of BLA hyperactivity in adolescent and adult rats. However, the mechanism is not known. Furthermore, not every individual is susceptible to the negative consequences of stress. Differences in the effects of stress on the BLA might contribute to determine whether an individual will be vulnerable or resilient to the effects of stress on emotion. The purpose of this study is to test the cellular underpinnings for age dependency of BLA hyperactivity after stress, and whether protective changes occur in resilient individuals. To test this, the effects of repeated stress on membrane excitability and other membrane properties of BLA principal neurons were compared between adult and adolescent rats, and between vulnerable and resilient rats, using in vitro whole-cell recordings. Vulnerability was defined by adrenal gland weight, and verified by body weight gain after repeated restraint stress, and fecal pellet production during repeated restraint sessions. We found that repeated stress increased the excitability of BLA neurons, but in a manner that depended on age and BLA subnucleus. Furthermore, stress resilience was associated with an opposite pattern of change, with increased slow afterhyperpolarization (AHP) potential, whereas vulnerability was associated with decreased medium AHP. The opposite outcomes in these two populations were further distinguished by differences of anxiety-like behavior in the elevated plus maze that were correlated with BLA neuronal excitability and AHP. These results demonstrate a substrate for BLA hyperactivity after repeated stress, with distinct membrane properties to target, as well as age-dependent factors that contribute to resilience to the effects of stress.

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The BLA is generally hyperactive following chronic stress.
“The stress-induced attenuation of BLA→DMS activity was surprising because the BLA is, generally, hyperactive following chronic stress54–61 (c.f.62).”
From A dual-pathway architecture for stress to disrupt agency and promote habit (2025) · cites this paper as [57]

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Repeated exposure to stress across the childhood-adolescent period alters rats' anxiety-and depression-like behaviors in adulthood: The importance of stressor type and gender
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Small Conductance Ca2+-activated K+ Channels and Calmodulin
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Modulation of SK Channel Trafficking by Beta Adrenoceptors Enhances Excitatory Synaptic Transmission and Plasticity in the Amygdala
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Social stress during adolescence in Wistar rats induces social anxiety in adulthood without affecting brain monoaminergic content and activity
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Countervailing Modulation of I h by Neuropeptide Y and Corticotrophin-Releasing Factor in Basolateral Amygdala As a Possible Mechanism for Their Effects on Stress-Related Behaviors
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Differential actions of corticotropin releasing factor on basolateral and central amygdaloid neurones, in vitro.
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Pubertal maturation and time of day differentially affect behavioral and neuroendocrine responses following an acute stressor
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Stress before Puberty Exerts a Sex- and Age-Related Impact on Auditory and Contextual Fear Conditioning in the Rat
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Regulation of Surface Localization of the Small Conductance Ca2+-activated Potassium Channel, Sk2, through Direct Phosphorylation by cAMP-dependent Protein Kinase
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Genetic Strain Differences in Learned Fear Inhibition Associated with Variation in Neuroendocrine, Autonomic, and Amygdala Dendritic Phenotypes
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Greater Behavioral Effects of Stress in Immature as Compared to Mature Male Mice
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A different recruitment of the lateral and basolateral amygdala promotes contextual or elemental conditioned association in Pavlovian fear conditioning
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Personality traits in rats predict vulnerability and resilience to developing stress-induced depression-like behaviors, HPA axis hyper-reactivity and brain changes in pERK1/2 activity
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Individual Stress Vulnerability Is Predicted by Short-Term Memory and AMPA Receptor Subunit Ratio in the Hippocampus
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Postnatal development of electrophysiological properties of principal neurons in the rat basolateral amygdala
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Effects of early-life stress on behavior and neurosteroid levels in the rat hypothalamus and entorhinal cortex
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Chronic stress‐induced alterations in amygdala responsiveness and behavior – modulation by trait anxiety and corticotropin‐releasing factor systems
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Association of childhood trauma exposure and GABRA2 polymorphisms with risk of posttraumatic stress disorder in adults
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Postnatal maturation of GABAergic transmission in the rat basolateral amygdala.
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Resilience against predator stress and dendritic morphology of amygdala neurons
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Competition between Calcium-Activated K+Channels Determines Cholinergic Action on Firing Properties of Basolateral Amygdala Projection Neurons
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Repeated restraint stress increases basolateral amygdala neuronal activity in an age-dependent manner
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Effects of repeated stress on excitatory drive of basal amygdala neurons in vivo
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Dendritic Morphology of Hippocampal and Amygdalar Neurons in Adolescent Mice Is Resilient to Genetic Differences in Stress Reactivity
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Dendritic morphology of amygdala and hippocampal neurons in more and less predator stress responsive rats and more and less spontaneously anxious handled controls
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The effects of repeated social interaction stress on behavioural and physiological parameters in a stress-sensitive mouse strain
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Neurotransmitter Modulation of Small-Conductance Ca2+-Activated K+ Channels by Regulation of Ca2+ Gating
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Modulation of the Ca2+-Activated K+Current sIAHPby aPhosphatase-Kinase Balance Under Basal Conditions inRat CA1 Pyramidal Neurons
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Repeated restraint stress exerts different impact on structure of neurons in the lateral and basal nuclei of the amygdala
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Reduced Serotonin Transporter Availability Decreases Prefrontal Control of the Amygdala
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Interaction of the Serotonin Transporter-Linked Polymorphic Region and Environmental Adversity: Increased Amygdala-Hypothalamus Connectivity as a Potential Mechanism Linking Neural and Endocrine Hyperreactivity
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Age‐Related Differences in Elevated Plus Maze Behavior between Adolescent and Adult Rats
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Postnatal development of the amygdala: A stereological study in rats
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Contextual, but not auditory, fear conditioning is disrupted by neurotoxic selective lesion of the basal nucleus of amygdala in rats
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Functional Gene Polymorphisms in the Serotonin System and Traumatic Life Events Modulate the Neural Basis of Fear Acquisition and Extinction
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Acute stress induces down‐regulation of large‐conductance Ca 2+ ‐activated potassium channels in the lateral amygdala
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Repeated restraint stress enhances cue-elicited conditioned freezing and impairs acquisition of extinction in an age-dependent manner
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Synaptic and Synaptically Activated Intrinsic Conductances Underlie Inhibitory Potentials in Cat Lateral Amygdaloid Projection Neurons In Vivo
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Differential Effects of Corticosterone on the Slow Afterhyperpolarization in the Basolateral Amygdala and CA1 Region: Possible Role of Calcium Channel Subunits
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L-Type Voltage-Gated Calcium Channels in the Basolateral Amygdala Are Necessary for Fear Extinction
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Influence of Age on Behavioural Response in the Light/Dark Paradigm
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Stress Resilience: A Low-Anxiety Genotype Protects Male Mice From the Consequences of Chronic Psychosocial Stress
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Coupled Activity-Dependent Trafficking of Synaptic SK2 Channels and AMPA Receptors
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Plasma Corticosteroid Response to Stress in Four Species of Wild Mice1
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Basolateral amygdala and stress-induced hyperexcitability affect motivated behaviors and addiction
Sharp, B. M. (2017) · Translational Psychiatry · doi:10.1038/tp.2017.161 · Cited by 244 · see citing works
Increased Basolateral Amygdala Pyramidal Cell Excitability May Contribute to the Anxiogenic Phenotype Induced by Chronic Early-Life Stress
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MicroRNAs as biomarkers of resilience or vulnerability to stress
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Physiological effects of a habituation procedure for functional MRI in awake mice using a cryogenic radiofrequency probe
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It Is All in the Right Amygdala: Increased Synaptic Plasticity and Perineuronal Nets in Male, But Not Female, Juvenile Rat Pups after Exposure to Early-Life Stress
Guadagno, A., Verlezza, S., Long, H., Wong, T. P., & Walker, C.-D. (2020) · The Journal of Neuroscience · doi:10.1523/jneurosci.1029-20.2020 · Cited by 78 · see citing works
Insulin-like growth factor 2 mitigates depressive behavior in a rat model of chronic stress
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Disruptive effects of repeated stress on basolateral amygdala neurons and fear behavior across the estrous cycle in rats
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CO2 exposure as translational cross-species experimental model for panic
Leibold, N. K., van den Hove, D., Viechtbauer, W., Buchanan, G. F., Goossens, L., Lange, I., Knuts, I., Lesch, K., Steinbusch, H. W. M., & Schruers, K. R. J. (2016) · Translational Psychiatry · doi:10.1038/tp.2016.162 · Cited by 66 · see citing works
Translational relevance of rodent models of hypothalamic-pituitary-adrenal function and stressors in adolescence
McCormick, C. M., Green, M. R., & Simone, J. J. (2016) · Neurobiology of Stress · doi:10.1016/j.ynstr.2016.08.003 · Cited by 66 · see citing works
Whole body vibration training improves depression-like behaviors in a rat chronic restraint stress model
Peng, G., Yang, L., Wu, C., Zhang, L. L., Wu, C. Y., Fan, L., Shi, H. W., Hou, J., Zhang, L. M., Ma, X., et al. (2020) · Neurochemistry International · doi:10.1016/j.neuint.2020.104926 · Cited by 50 · see citing works
Prenatal Stress Alters the Development of Socioemotional Behavior and Amygdala Neuron Excitability in Rats
Ehrlich, D., & Rainnie, D. G. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.55 · Cited by 48 · see citing works
Amygdala Allostasis and Early Life Adversity: Considering Excitotoxicity and Inescapability in the Sequelae of Stress
Hanson, J. L., & Nacewicz, B. M. (2021) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2021.624705 · Cited by 48 · see citing works
Effects of Repeated Stress on Age-Dependent GABAergic Regulation of the Lateral Nucleus of the Amygdala
Zhang, W., & Rosenkranz, J. A. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2016.33 · Cited by 41 · see citing works
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Endocrine‐Autonomic Linkages
Sladek, C. D., Michelini, L. C., Stachenfeld, N. S., Stern, J. E., & Urban, J. H. (2015) · Comprehensive physiology · doi:10.1002/cphy.c140028 · Cited by 49 · see citing works
TRH and TRH receptor system in the basolateral amygdala mediate stress-induced depression-like behaviors
Choi, J., Kim, J., Kim, T.-K., Park, J. Y., Lee, J. E., Kim, H., Lee, E. H., & Han, P. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2015.03.030 · Cited by 38 · see citing works
The BigLEN-GPR171 Peptide Receptor System Within the Basolateral Amygdala Regulates Anxiety-Like Behavior and Contextual Fear Conditioning
Bobeck, E. N., Gomes, I., Pena, D. A., Cummings, K. A., Clem, R. L., Mezei, M., & Devi, L. A. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2017.79 · Cited by 34 · see citing works
Axin1 up-regulated 1 accelerates stress-induced cardiomyocytes apoptosis through activating Wnt/β-catenin signaling
Ye, X., Lin, J., Lin, Z., Xue, A., Li, L., Zhao, Z., Liu, L., Shen, Y., & Cong, B. (2017) · Experimental Cell Research · doi:10.1016/j.yexcr.2017.08.027 · Cited by 34 · see citing works
Anxiolytic-like effects of α-asarone in a mouse model of chronic pain
Tian, J., Tian, Z., Qin, S.-L., Zhao, P.-Y., Jiang, X., & Tian, Z. (2017) · Metabolic Brain Disease · doi:10.1007/s11011-017-0108-z · Cited by 33 · see citing works
Brain‐wide cellular mapping of acute stress‐induced activation in male and female mice
Kim, W., & Chung, C. (2021) · The FASEB Journal · doi:10.1096/fj.202101287r · Cited by 33 · see citing works
Maturation of amygdala inputs regulate shifts in social and fear behaviors: A substrate for developmental effects of stress
Ferrara, N. C., Trask, S., & Rosenkranz, J. A. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.01.021 · Cited by 32 · see citing works
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Association of Increased Amygdala Activity with Stress-Induced Anxiety but not Social Avoidance Behavior in Mice
Huang, S.-H., Liu, W.-Z., Qin, X., Guo, C.-Y., Xiong, Q.-C., Wang, Y., Hu, P., Pan, B., & Zhang, W.-H. (2021) · Neuroscience Bulletin · doi:10.1007/s12264-021-00762-0 · Cited by 32 · see citing works
Sex- and exposure age-dependent effects of adolescent stress on ventral tegmental area dopamine system and its afferent regulators
Zhu, X., & Grace, A. A. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01820-3 · Cited by 32 · see citing works
A dual-pathway architecture for stress to disrupt agency and promote habit
Giovanniello, J. R., Paredes, N., Wiener, A., Ramírez-Armenta, K., Oragwam, C., Uwadia, H. O., Yu, A. L., Lim, K., Pimenta, J. S., Vilchez, G. E., et al. (2025) · Nature · doi:10.1038/s41586-024-08580-w · Cited by 30 · see citing works
Qualitatively different effect of repeated stress during adolescence on principal neuron morphology across lateral and basal nuclei of the rat amygdala
Padival, M., Blume, S. R., Vantrease, J., & Rosenkranz, J. A. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.02.012 · Cited by 29 · see citing works
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Stress impacts corticoamygdalar connectivity in an age-dependent manner
Uliana, D. L., Gomes, F. V., & Grace, A. A. (2020) · Neuropsychopharmacology · doi:10.1038/s41386-020-00886-3 · Cited by 26 · see citing works
Postsynaptic Adenosine A2A Receptors Modulate Intrinsic Excitability of Pyramidal Cells in the Rat Basolateral Amygdala
Rau, A. R., Ariwodola, O. J., & Weiner, J. L. (2015) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyv017 · Cited by 24 · see citing works
Functional coupling of Tmem74 and HCN1 channels regulates anxiety-like behavior in BLA neurons
Shao, L.-X., Jiang, Q., Liu, X., Gong, D.-M., Yin, Y., Wu, G., Sun, N.-H., Wang, C.-K., Chen, Q., Yu, C., et al. (2019) · Molecular Psychiatry · doi:10.1038/s41380-019-0402-8 · Cited by 23 · see citing works
Harmine enhances GABAergic transmission onto basoamygdala projection neurons in mice
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Authors: Hetzel, A., & Rosenkranz, J. A.
Affiliations: Rosalind Franklin University of Medicine and Science (US)
Corresponding author: Rosenkranz, J Amiel
ORCID: Hetzel, Andrea
Rosenkranz, J Amiel
Venue: Neuropsychopharmacology
Publisher: Springer Science and Business Media LLC
Published: 2014-03-12
Volume: 39
Issue: 9
Pages: 2114-2130
ISSN: 0893-133X (ISSN-L)
1740-634X
DOI: 10.1038/npp.2014.60
PMC: PMC4104329
OpenAlex: W2013095929
Cited by: 62
References: 137
Citations by year: 2026: 3 · 2025: 5 · 2024: 2 · 2023: 7 · 2022: 4 · 2021: 8 · 2020: 5 · 2019: 6 · 2018: 3 · 2017: 5 · 2016: 5 · 2015: 8 · 2014: 1
FWCI: 3.11
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.springer.com/tdm (tdm)
Locations: Neuropsychopharmacology (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Rosalind Franklin University of Medicine and Science
National Institute of Mental Health (MH84970, R01MH084970)
Topics: Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords: repeated restraint stress, basolateral amygdala, neuronal membrane properties, neuronal excitability, slow afterhyperpolarization, stress resilience, developmental stress, age-dependent effects, amygdala subnuclei, anxiety-like behavior, elevated plus maze, adrenal weight
MeSH terms: Adrenal Glands, Aging, Animals, Anxiety, Cell Membrane, Defecation, Male, Neurons, Organ Size, Random Allocation, Restraint, Physical, Stress, Psychological, Weight Gain, Rats, Sprague-Dawley, Patch-Clamp Techniques, Maze Learning, Resilience, Psychological, Basolateral Nuclear Complex

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Distinct Effects of Repeated Restraint Stress on Basolateral Amygdala Neuronal Membrane Properties in Resilient Adolescent and Adult Rats

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