Basolateral amygdala and stress-induced hyperexcitability affect motivated behaviors and addiction

Sharp, B M

doi:10.1038/tp.2017.161

Cited by 244Neurotransmitter Receptor Influence on BehaviorMemory and Neural MechanismsNeuroscience and Neuropharmacology Research

Basolateral amygdala and stress-induced hyperexcitability affect motivated behaviors and addiction

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Sharp, B M·2017·Translational Psychiatry

DOI 10.1038/tp.2017.161PMC PMC5611728

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Abstract

The amygdala integrates and processes incoming information pertinent to reward and to emotions such as fear and anxiety that promote survival by warning of potential danger. Basolateral amygdala (BLA) communicates bi-directionally with brain regions affecting cognition, motivation and stress responses including prefrontal cortex, hippocampus, nucleus accumbens and hindbrain regions that trigger norepinephrine-mediated stress responses. Disruption of intrinsic amygdala and BLA regulatory neurocircuits is often caused by dysfunctional neuroplasticity frequently due to molecular alterations in local GABAergic circuits and principal glutamatergic output neurons. Changes in local regulation of BLA excitability underlie behavioral disturbances characteristic of disorders including post-traumatic stress syndrome (PTSD), autism, attention-deficit hyperactivity disorder (ADHD) and stress-induced relapse to drug use. In this Review, we discuss molecular mechanisms and neural circuits that regulate physiological and stress-induced dysfunction of BLA/amygdala and its principal output neurons. We consider effects of stress on motivated behaviors that depend on BLA; these include drug taking and drug seeking, with emphasis on nicotine-dependent behaviors. Throughout, we take a translational approach by integrating decades of addiction research on animal models and human trials. We show that changes in BLA function identified in animal addiction models illuminate human brain imaging and behavioral studies by more precisely delineating BLA mechanisms. In summary, BLA is required to promote responding for natural reward and respond to second-order drug-conditioned cues; reinstate cue-dependent drug seeking; express stress-enhanced reacquisition of nicotine intake; and drive anxiety and fear. Converging evidence indicates that chronic stress causes BLA principal output neurons to become hyperexcitable.

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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 [59]

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Martin BS, Corbin JG, Huntsman MM. Deficient tonic GABAergic conductance and synaptic balance in the fragile X syndrome amygdala. J Neurophysiol 2014; 112: 891–902. PMC4122738 24848467
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“The LTP in GABA interneurons contributes to a feed-forward inhibition of principal neurons in BLA (Sharp, 2017).”
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Connectivity characterization of the mouse basolateral amygdalar complex
Hintiryan, H., Bowman, I., Johnson, D. L., Korobkova, L., Zhu, M., Khanjani, N., Gou, L., Gao, L., Yamashita, S., Bienkowski, M. S., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-22915-5 · Cited by 121 · see citing works
“correspondence to match each section to its corresponding ARA atlas template, (2) to warp data sections to atlas templates, (3) to threshold labeling, (4)”
Background
The role of social isolation in opioid addiction
Christie, N. C. (2021) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsab029 · Cited by 108 · see citing works
“Second, the amygdala is associated with stress-induced drug-seeking behavior and is critical for responding to natural rewards, including social connection (Sharp, 2017).”
Background
Die COVID-19-Pandemie als Herausforderung für die psychische Gesundheit
Brakemeier, E., Wirkner, J., Knaevelsrud, C., Wurm, S., Christiansen, H., Lueken, U., & Schneider, S. (2020) · Zeitschrift für Klinische Psychologie und Psychotherapie · doi:10.1026/1616-3443/a000574 · Cited by 96 · see citing works
Functional Contribution of the Medial Prefrontal Circuitry in Major Depressive Disorder and Stress-Induced Depressive-Like Behaviors
Bittar, T. P., & Labonté, B. (2021) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.699592 · Cited by 87 · see citing works
“…the number of parvalbumin (PV) positive cells and PV mRNA in the PLC and ILC was reported in female mice after chronic unpredictable mild stress while in males, the number of PV positive cells was significantly increased only in the PLC with no change in PV mRNA expression (Shepard et al., 2016).”
Background
Dopaminergic Mechanisms Underlying Normal Variation in Trait Anxiety
Berry, A. S., White, R. L., Furman, D. J., Naskolnakorn, J., Shah, V. D., D'Esposito, M., & Jagust, W. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.2382-18.2019 · Cited by 50 · see citing works
“These findings should be interpreted with caution as they were not consistent for other striatal subregions, particularly for VST, which includes nucleus accumbens and whose association with limbic processes has been most clearly established (Sharp, 2017).”
Background
Neuroplastic and cognitive impairment in substance use disorders: a therapeutic potential of cognitive stimulation
Sampedro‐Piquero, P., de Guevara‐Miranda, D. L., Pavón, F. J., Serrano, A., Suárez, J., de Fonseca, F. R., Santín, L. J., & Castilla‐Ortega, E. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.11.015 · Cited by 77 · see citing works
Brain-Based Biotypes of Psychiatric Vulnerability in the Acute Aftermath of Trauma
Stevens, J. S., Harnett, N. G., Lebois, L. A. M., van Rooij, S. J. H., Ely, T. D., Roeckner, A. R., Vincent, N., Beaudoin, F. L., An, X., Zeng, D., et al. (2021) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2021.20101526 · Cited by 70 · see citing works
Neurobiology of Depression: Chronic Stress Alters the Glutamatergic System in the Brain—Focusing on AMPA Receptor
Lee, M. T., Peng, W., Kan, H., Wu, C., Wang, D., & Ho, Y. (2022) · Biomedicines · doi:10.3390/biomedicines10051005 · Cited by 67 · see citing works
“The amygdala is a brain region important for the integration of emotional processes and emotion-related memories, which receives input from divergent brain regions involved in emotion, such as the PFC, thalamus, hippocampus, raphe, and VTA [47].”
Background
Stress-induced plasticity of a CRH/GABA projection disrupts reward behaviors in mice
Birnie, M. T., Short, A. K., de Carvalho, G., Taniguchi, L., Gunn, B. G., Pham, A. L., Itoga, C. A., Xu, X., Chen, L. Y., Mahler, S. V., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-36780-x · Cited by 64 · see citing works
Brain Site-Specific Inhibitory Effects of the GLP-1 Analogue Exendin-4 on Alcohol Intake and Operant Responding for Palatable Food
Colvin, K. J., Killen, H. S., Kanter, M. J., Halperin, M. C., Engel, L., & Currie, P. J. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21249710 · Cited by 62 · see citing works
“Furthermore, long-term ethanol consumption alters several mRNAs in the BLA of rats [58], and previous research suggests that the BLA is necessary for stress-induced drug-seeking and drug-taking behavior [59].”
Background
Total Number and Ratio of GABAergic Neuron Types in the Mouse Lateral and Basal Amygdala
Vereczki, V., Müller, K., Krizsán, É., Máté, Z., Fekete, Z., Rovira-Esteban, L., Veres, J. M., Erdélyi, F., & Hájos, N. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.2700-20.2021 · Cited by 60 · see citing works
Expression map of 78 brain-expressed mouse orphan GPCRs provides a translational resource for neuropsychiatric research
Ehrlich, A. T., Maroteaux, G., Robé, A., Ventéo, L., Nasseef, M. T., van Kempen, L. C. L. T., Mechawar, N., Turecki, G., Darcq, E., & Kieffer, B. L. (2018) · Communications Biology · doi:10.1038/s42003-018-0106-7 · Cited by 60 · see citing works
Anxiolytic effects of Formononetin in an inflammatory pain mouse model
Wang, X., Guan, S., Liu, A., Yue, J., Hu, L., Zhang, K., Yang, L.-K., Lu, L., Tian, Z., Zhao, M., et al. (2019) · Molecular Brain · doi:10.1186/s13041-019-0453-4 · Cited by 61 · see citing works
Association of high-fat diet with neuroinflammation, anxiety-like defensive behavioral responses, and altered thermoregulatory responses in male rats
Noronha, S. I. S. R., Lima, P. M. A., Campos, G. S. V., Chírico, M. T. T., de Abreu, A. R. R., Figueiredo, A. B., Silva, F. C. S., Chianca, D. A., Lowry, C. A., & de Menezes, R. C. A. (2019) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2019.04.030 · Cited by 60 · see citing works
Reduced resting-state functional connectivity of the basolateral amygdala to the medial prefrontal cortex in preweaning rats exposed to chronic early-life stress
Guadagno, A., Kang, M. S., Devenyi, G. A., Mathieu, A. P., Rosa‐Neto, P., Chakravarty, M. M., & Walker, C. (2018) · Brain Structure and Function · doi:10.1007/s00429-018-1720-3 · Cited by 59 · see citing works
“Connectivity to the NAcc was significantly reduced from the left pBLA seed in LB pups (Fig.”
Influential
Cardiovascular impact of electronic-cigarette use
Middlekauff, H. R. (2019) · Trends in Cardiovascular Medicine · doi:10.1016/j.tcm.2019.04.006 · Cited by 59 · see citing works
“Nicotinic receptors are present throughout the autonomic nervous system, including the amygdala, a brain area that integrates responses to emotion and stress (25-27).”
Background
Stress induces insertion of calcium-permeable AMPA receptors in the OFC–BLA synapse and modulates emotional behaviours in mice
Kuniishi, H., Yamada, D., Wada, K., Yamada, M., & Sekiguchi, M. (2020) · Translational Psychiatry · doi:10.1038/s41398-020-0837-3 · Cited by 47 · see citing works
The Influence of Trait Compulsivity and Impulsivity on Addictive and Compulsive Behaviors During COVID-19
Albertella, L., Rotaru, K., Christensen, E., Lowe, A., Brierley, M., Richardson, K. E., Chamberlain, S. R., Lee, R. S. C., Kayayan, E., Grant, J. E., et al. (2021) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2021.634583 · Cited by 50 · see citing works
GABAA(δ) receptor hypofunction in the amygdala-hippocampal circuit underlies stress-induced anxiety
Qin, X., Pan, H., Huang, S.-H., Zou, J., Zheng, Z.-H., Liu, X., You, W.-J., Liu, Z.-P., Cao, J., Zhang, W.-H., et al. (2021) · 中国科学通报：英文版 · doi:10.1016/j.scib.2021.09.007 · Cited by 47 · see citing works
Ceramides affect alcohol consumption and depressive‐like and anxiety‐like behavior in a brain region‐ and ceramide species‐specific way in male mice
Zoicas, I., Huber, S. E., Kalinichenko, L. S., Gulbins, E., Müller, C. P., & Kornhuber, J. (2019) · Addiction Biology · doi:10.1111/adb.12847 · Cited by 48 · see citing works
Recent advances in anxiety disorders: Focus on animal models and pathological mechanisms
Zhao, H., Zhou, M., Liu, Y., Jiang, J., & Wang, Y. (2023) · Animal Models and Experimental Medicine · doi:10.1002/ame2.12360 · Cited by 46 · see citing works
Organizational principles of amygdalar input-output neuronal circuits
Huang, L., Chen, Y., Jin, S., Lin, L., Duan, S., Si, K., Gong, W., & Zhu, J. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01262-3 · Cited by 44 · see citing works
Mini-review: The neurobiology of treating substance use disorders with classical psychedelics
Urban, M. M., Stingl, M., & Meinhardt, M. W. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1156319 · Cited by 44 · see citing works
“This seems to arise from excessive excitatory input from the extended amygdala, which in turn is attributable to a disruption of inhibitory control mechanisms within this structure (Kallupi et al., 2013; Stamatakis et al., 2014; Sharp, 2017).”
Background
The mouse brain after foot shock in four dimensions: Temporal dynamics at a single-cell resolution
Bonapersona, V., Schuler, H., Damsteegt, R., Adolfs, Y., Pasterkamp, R. J., van den Heuvel, M. P., Joëls, M., & Sarabdjitsingh, R. A. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2114002119 · Cited by 43 · see citing works
“…we here illustrate the ﬁndings for the BLA, an area key for the cognitive processing of a foot shock (27) and stressful conditions in general (28); for the remaining areas, we refer to an open-source dynamic database (https://osf.io/8muvw/) (29), with which one can browse through all other…”
Early life stress induces anxiety-like behavior during adulthood through dysregulation of neuronal plasticity in the basolateral amygdala
Qin, X., Liu, X.-X., Wang, Y., Wang, D., Song, Y., Zou, J., Pan, H., Zhai, X.-Z., Zhang, Y.-M., Zhang, Y.-B., et al. (2021) · Life Sciences · doi:10.1016/j.lfs.2021.119959 · Cited by 42 · see citing works
Dopamine Dysregulation in Reward and Autism Spectrum Disorder
Blum, K., Bowirrat, A., Sunder, K. R., Thanos, P. K., Hanna, C., Gold, M. S., Dennen, C. A., Elman, I., Murphy, K. T., & Makale, M. T. (2024) · Brain Sciences · doi:10.3390/brainsci14070733 · Cited by 44 · see citing works
“The basolateral amygdala (BLA) is widely thought to play a role in ASD; it communicates bi-directionally with the nucleus accumbens (NAc), a key reward locus, and principal BLA neurons receive glu-taminergic, DAergic, and GABAergic inputs [138,139].”
Background
Reciprocal interactions across and within multiple levels of monoamine and cortico-limbic systems in stress-induced depression: A systematic review
Lee, E. H., & Han, P. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.03.014 · Cited by 40 · see citing works
Oxytocin neurons mediate stress-induced social memory impairment
Zhan, S., Qi, Z., Cai, F., Gao, Z., Xie, J., & Hu, J. (2023) · Current Biology · doi:10.1016/j.cub.2023.11.037 · Cited by 44 · see citing works
Maternal antioxidant treatment prevents the adverse effects of prenatal stress on the offspring's brain and behavior
Scott, H., Phillips, T. J., Sze, Y., Alfieri, A., Rogers, M. F., Volpato, V., Case, C. P., & Brunton, P. J. (2020) · Neurobiology of Stress · doi:10.1016/j.ynstr.2020.100281 · Cited by 41 · see citing works
“The hippocampus and amygdala are well established to be involved in regulating anxiety behavior and stress responses (McEwen, 2016; Sharp, 2017; Zhang et al., 2018) and structural and neurochemical changes within these structures have been reported following prenatal stress (Hayashi et al., 1998;…”
Background
Downregulation of kainate receptors regulating GABAergic transmission in amygdala after early life stress is associated with anxiety-like behavior in rodents
Englund, J., Haikonen, J., Shteinikov, V., Amarilla, S. P., Atanasova, T., Shintyapina, A. B., Ryazantseva, M., Partanen, J. M., Võikar, V., & Lauri, S. E. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01654-7 · Cited by 39 · see citing works
The Basolateral Amygdala to Ventral Hippocampus Circuit Controls Anxiety-Like Behaviors Induced by Morphine Withdrawal
Deji, C., Yan, P., Ji, Y., Yan, X., Feng, Y., Liu, J., Liu, Y., Wei, S., Zhu, Y., & Lai, J. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.894886 · Cited by 37 · see citing works
“The BLA is necessary to promote responses to natural rewards, respond to second-order drug-conditioned cues, express stress-enhanced reacquisition of drug intake, and reinstate cue-dependent drug seeking (Sharp, 2017).”
BackgroundInfluential
Parsing inter- and intra-individual variability in key nervous system mechanisms of stress responsivity and across functional domains
Rab, S. L., & Admon, R. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.09.007 · Cited by 34 · see citing works
ACh signaling modulates activity of the GABAergic signaling network in the basolateral amygdala and behavior in stress-relevant paradigms
Mineur, Y. S., Mose, T. N., Maibom, K. L., Pittenger, S. T., Soares, A. R., Wu, H., Taylor, S. R., Huang, Y., & Picciotto, M. R. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01749-7 · Cited by 36 · see citing works
“While this was at first somewhat surprising, since excitability of BLA principal neurons is generally thought to be critical for stress sensitivity [46], it is also consistent with the finding that principal neurons show relatively modest nAChR responses and are predominantly regulated by muscarinic receptors [45].”
Result
The amygdala in adolescents with attention-deficit/hyperactivity disorder: Structural and functional correlates of delay aversion
Dessel, J. V., Sonuga-Barke, E. J. S., Moerkerke, M., der Oord, S. V., Lemiere, J., Morsink, S., & Danckaerts, M. (2019) · The World Journal of Biological Psychiatry · doi:10.1080/15622975.2019.1585946 · Cited by 34 · see citing works
NLRP3 deficiency-induced hippocampal dysfunction and anxiety-like behavior in mice
Komleva, Y. K., Lopatina, O. L., Валерьевна, Г. Я., Shuvaev, А. N., Chernykh, A., Potapenko, I., & Salmina, A. B. (2020) · Brain Research · doi:10.1016/j.brainres.2020.147220 · Cited by 35 · see citing works
Dynorphin/kappa opioid receptor system regulation on amygdaloid circuitry: Implications for neuropsychiatric disorders
Limoges, A., Yarur, H. E., & Tejeda, H. A. (2022) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2022.963691 · Cited by 33 · see citing works
“Alterations in amygdala activity have been linked to posttraumatic stress disorder (PTSD) as well as substance use disorders in humans (Grillon et al., 1996; Sharp, 2017; Morey et al., 2020; Zhang W.H. et al., 2021; Alexandra Kredlow et al., 2022).”
Background
Know thy SEFL: Fear sensitization and its relevance to stressor-related disorders
Nishimura, K., Poulos, A. M., Drew, M. R., & Rajbhandari, A. K. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104884 · Cited by 33 · see citing works
Therapeutic Effects of Spirulina platensis Against Adolescent Stress-Induced Oxidative Stress, Brain-Derived Neurotrophic Factor Alterations and Morphological Remodeling in the Amygdala of Adult Female Rats
Moradi-Kor, N., Ghanbari, A., Rashidipour, H., Bandegi, A. R., Youseﬁ, B., Barati, M., Kokhaei, P., & Rashidy-Pour, A. (2020) · Journal of Experimental Pharmacology · doi:10.2147/jep.s237378 · 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
Emotion in action: When emotions meet motor circuits
Braine, A., & Georges, F. E. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105475 · Cited by 32 · see citing works
Effects of Cocaine Self-Administration and Its Extinction on the Rat Brain Cannabinoid CB1 and CB2 Receptors
Bystrowska, B., Frankowska, M., Smaga, I., Pomierny-Chamioło, L., & Filip, M. (2018) · Neurotoxicity Research · doi:10.1007/s12640-018-9910-6 · Cited by 30 · see citing works
“…showing that basolateral amygdala integrates and processes emotions such as fear and anxiety that promote survival by warning of potential danger (Sharp 2017) and that basolateral eCB system may be involved in regulating the stress responses, fear, and anxiety (Gorzalka et al. 2008; Hill and…”
Background
Potentiated GABAergic neuronal activities in the basolateral amygdala alleviate stress‐induced depressive behaviors
Asim, M., Wang, H., Chen, X., & He, J. (2023) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.14422 · Cited by 28 · see citing works
“19,59,60 Chemogenetic stimulation of BLA GABA neurons may enhance the inhibition by high-frequency long-term activation of BLA GABAergic neurons.”
Background
Drug-Induced Glucocorticoids and Memory for Substance Use
Goldfarb, E. V., & Sinha, R. (2018) · Trends in Neurosciences · doi:10.1016/j.tins.2018.08.005 · Cited by 29 · see citing works
Coexistence of chronic hyperalgesia and multilevel neuroinflammatory responses after experimental SCI: a systematic approach to profiling neuropathic pain
Wang, L., Gunduz, M. A., Semeano, A. T., Yılmaz, E. C., Alanazi, F. A. H., Imir, O. B., Yener, U., Arbelaez, C. A., Usuga, E., & Teng, Y. D. (2022) · Journal of Neuroinflammation · doi:10.1186/s12974-022-02628-2 · Cited by 28 · see citing works
“Furthermore, the spinoparabrachial pathway projects to BLA via PBN for sensory functions [106], and most BLA neurons innervate the hippocampus and neocortex to form bidirectional communications involved in emotion-related memory concerning depression [107, 108].”
Background
Structural, functional, and behavioral significance of sex and gonadal hormones in the basolateral amygdala: A review of preclinical literature
Price, M. E., & McCool, B. A. (2021) · Alcohol · doi:10.1016/j.alcohol.2021.08.001 · Cited by 28 · see citing works
“Dopamine has an important role in regulating BLA-mediated behaviors like fear conditioning (Greba et al., 2001; Heath et al., 2015; Prager et al., 2016; Sharp, 2017).”
Background
Chronic stress increases pain sensitivity via activation of the rACC–BLA pathway in rats
Liu, L., Zhang, R., Chen, L., Zhao, H., Cai, J., Wang, J., Guo, D., Cui, Y., & Xing, G. (2018) · Experimental Neurology · doi:10.1016/j.expneurol.2018.12.009 · Cited by 27 · see citing works
“Also, the BLA is highly associated with a variety of brain functions and diseases, such as cognitive and emotional functions (Sharp, 2017), and the hyperexcitability of BLA neurons is involved in the pathogenesis of SIH.”
Background
Choose your path: Divergent basolateral amygdala efferents differentially mediate incentive motivation, flexibility and decision-making
Keefer, S. E., Gyawali, U., & Calu, D. J. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113306 · Cited by 27 · see citing works
“In humans, neuroimaging studies indicate amygdala activation when presented with drug- associated cues (reviewed in Jasinska et al., 2014; Sharp, 2017).”
Brain responses to positive and negative events in individuals with internet gaming disorder during real gaming
Zhang, Z., Wang, S., Du, X., Qi, Y., Wang, L., & Dong, G. (2023) · Journal of Behavioral Addictions · doi:10.1556/2006.2023.00039 · Cited by 25 · see citing works
“…negative events, considering that the amygdala was known to be the important role in negative emotions (Koob & Volkow, 2016; Schaefer et al., 2002; Sharp, 2017) and abnormal FC between the amygdala and prefrontal cortex (e.g., DLPFC and orbital front lobe) in IGD have been found in previous…”
Melanin-concentrating hormone promotes anxiety and intestinal dysfunction via basolateral amygdala in mice
He, X., Li, Y., Zhang, N., Huang, J., Ming, X., Guo, R., Hu, Y., Ji, P., & Guo, F. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.906057 · Cited by 25 · see citing works
“The amygdala, located in the medial temporal lobe of most mammals (Sah et al., 2003), plays an important role in processing information about anxiety-inducing stimuli, and modulates emotional and behavioral responses (Delgado et al., 2006; Sharp, 2017).”
Background
Basolateral amygdala, nicotinic cholinergic receptors, and nicotine: Pharmacological effects and addiction in animal models and humans
Sharp, B. M. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.13970 · Cited by 25 · see citing works
Self-citation
Hyperactivation of the amygdala correlates with impaired social play behavior of prepubertal male rats in a maternal immune activation model
Vitor-Vieira, F., Vilela, F. C., & Giusti‐Paiva, A. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113503 · 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
Neurogenetics and Epigenetics of Loneliness
Bowirrat, A., Elman, I., Dennen, C. A., Gondré-Lewis, M. C., Cadet, J. L., Khalsa, J., Baron, D., Soni, D., Gold, M. S., McLaughlin, T., et al. (2023) · Psychology Research and Behavior Management · doi:10.2147/prbm.s423802 · Cited by 23 · see citing works
Alterations in GABAA receptor-mediated inhibition triggered by status epilepticus and their role in epileptogenesis and increased anxiety
Aroniadou‐Anderjaska, V., Figueiredo, T. H., Furtado, M. D. A., Pidoplichko, V. I., Lumley, L. A., & Braga, M. F. M. (2024) · Neurobiology of Disease · doi:10.1016/j.nbd.2024.106633 · Cited by 23 · see citing works
“It is well-known that repeated stress (or one intense stressful experience that can cause PTSD) can result in a hy-perexcitable amygdala and the development of anxiety (Sharp, 2017; Zhang et al., 2018).”
NLRP3 Inflammasome Blocking as a Potential Treatment of Central Insulin Resistance in Early-Stage Alzheimer’s Disease
Komleva, Y. K., Potapenko, I., Lopatina, O. L., Gorina, Y. V., Chernykh, A., Хилажева, Е. Д., Salmina, A. B., & Shuvaev, А. N. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222111588 · Cited by 23 · see citing works
“Previously it was shown, that hyperexcitability of the basolateral nucleus of the amygdala is associated with increased anxiety and often occurs in parallel with various neurodevelopmental, neurodegenerative, and neuropsychiatric disorders [52,53].”
Background
Locus coeruleus-noradrenergic modulation of trigeminal pain: Implications for trigeminal neuralgia and psychiatric comorbidities
Ayaz, B. D., & Caudle, R. M. (2023) · Neurobiology of Pain · doi:10.1016/j.ynpai.2023.100124 · Cited by 24 · see citing works
“Stress may reflect a part of the mechanism underlying these clinical comorbidities as BLA is a key brain region involved in stress and activity of BLA neurons is modulated by NA-mediated stress responses (Sharp, 2017).”
Background
Glial Activation in the Thalamus Contributes to Vestibulomotor Deficits Following Blast-Induced Neurotrauma
Dickerson, M. R., Bailey, Z. S., Murphy, S. F., Urban, M. J., & VandeVord, P. J. (2020) · Frontiers in Neurology · doi:10.3389/fneur.2020.00618 · Cited by 22 · see citing works
Data-driven parcellation and graph theory analyses to study adolescent mood and anxiety symptoms
Ely, B. A., Liu, Q., DeWitt, S. J., Mehra, L. M., Alonso, C. M., & Gabbay, V. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01321-x · Cited by 22 · see citing works
Stress- and drug-induced neuroimmune signaling as a therapeutic target for comorbid anxiety and substance use disorders
Smiley, C. E., & Wood, S. K. (2022) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2022.108212 · Cited by 23 · see citing works
Elevated Level of PKMζ Underlies the Excessive Anxiety in an Autism Model
Gao, X., Zheng, R., Ma, X., Gong, Z., Xia, D., & Zhou, Q. (2019) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2019.00291 · Cited by 22 · see citing works
“Reduced inhibitory function/transmission likely leads to hyperactivity in BLA, which has been reported in various psychiatric disease and stress models (Sharp, 2017).”
Background
The synthetically produced predator odor 2,5-dihydro-2,4,5-trimethylthiazoline increases alcohol self-administration and alters basolateral amygdala response to alcohol in rats
Makhijani, V. H., Franklin, J. P., Voorhies, K. J. V., Fortino, B., & Besheer, J. (2020) · Psychopharmacology · doi:10.1007/s00213-020-05659-w · Cited by 22 · see citing works
Correlation of gut microbiota and neurotransmitters in a rat model of post-traumatic stress disorder
Zhou, Q., Sun, T., Wu, F., Li, F., Liu, Y., Li, W., Dai, N., Tan, L., Li, T., & Song, Y. (2020) · Journal of Traditional Chinese Medical Sciences · doi:10.1016/j.jtcms.2020.10.005 · Cited by 22 · see citing works
Graphene oxide prevents lateral amygdala dysfunctional synaptic plasticity and reverts long lasting anxiety behavior in rats
Biagioni, A. F., Cellot, G., Pati, E., Lozano, N., Ballesteros, B., Casani, R., Coimbra, N. C., Kostarelos, K., & Ballerini, L. (2021) · Biomaterials · doi:10.1016/j.biomaterials.2021.120749 · Cited by 20 · see citing works
Dose mediates the protracted effects of adolescent THC exposure on reward and stress reactivity in males relevant to perturbation of the basolateral amygdala transcriptome
Ferland, J. N., Ellis, R. J., Rompala, G. R., Landry, J. A., Callens, J. E., Ly, A., Frier, M. D., Uzamere, T. O., & Hurd, Y. L. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01467-0 · Cited by 21 · see citing works
“Dopamine receptors in the BLA mediate incentive learning, stress reactivity, and social recognition [73, 74] and the interaction between dopamine and CRF regulates amygdala function [75].”
Background
Altered amygdala volumes and microstructure in focal epilepsy patients with tonic–clonic seizures, ictal, and post‐convulsive central apnea
Zeicu, C., Legouhy, A., Scott, C. A., Oliveira, J. F. A., Winston, G. P., Duncan, J. S., Vos, S. B., Thom, M., Lhatoo, S. D., Zhang, H. G., et al. (2023) · Epilepsia · doi:10.1111/epi.17804 · Cited by 20 · see citing works
“31,32 The neural processes accompanying the altered volumes may directly influence the amygdala's control on both respiratory action and cardiovascular instability as shown here and elsewhere.”
Background
α7 nicotinic receptor full agonist reverse basolateral amygdala hyperactivity and attenuation of dopaminergic neuron activity in rats exposed to chronic mild stress
Neves, G. A., & Grace, A. A. (2019) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2019.09.009 · Cited by 22 · see citing works
Anxiety in children and youth with autism spectrum disorder and the association with amygdala subnuclei structure
Hennessy, A., Séguin, D., Correa, S., Wang, J., Martínez-Trujillo, J., Nicolson, R., & Duerden, E. G. (2022) · Autism · doi:10.1177/13623613221127512 · Cited by 20 · see citing works
“It has been postulated that chronic stress causes BLA neurons to become hyperexcitable (Sharp, 2017).”
Background
Disrupting astrocyte-neuron lactate transport prevents cocaine seeking after prolonged withdrawal
Chen, W., Zhang, Y., Liang, J., Zhang, Z., Zhang, L., Huang, E., Zhang, G., Lü, L., Han, Y., & Shi, J. (2023) · Science Advances · doi:10.1126/sciadv.adi4462 · Cited by 19 · see citing works
“Specifically, BLA is critical for cue-induced drug seeking and drug taking behaviors ( 25 , 34 , 35 ), while CeA mediates long-lasting negative affective states during withdrawal and incubation of drug craving ( 27 , 36 ).”
Background
Cocaine and chronic stress exposure produce an additive increase in neuronal activity in the basolateral amygdala
Munshi, S., Rosenkranz, J. A., Caccamise, A. J., Wolf, M. E., Corbett, C. M., & Loweth, J. A. (2019) · Addiction Biology · doi:10.1111/adb.12848 · Cited by 18 · see citing works
Physiological and cognitive changes after treatments of cyclophosphamide, methotrexate, and fluorouracil: implications of the gut microbiome and depressive-like behavior
Corley, C. L., McElroy, T., Sridharan, B., Trujillo, M., Simmons, P., Kandel, S., Sykes, D. J., Robeson, M. S., & Allen, A. R. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1212791 · Cited by 17 · see citing works
“…the basolateral amygdala resulted in interrupted excitatory synaptic transmission causing behavior deficiencies and upregulated immune response seen in these studies (Felix-Ortiz and Tye, 2014; Sharp, 2017; Hu et al., 2022) as well as the hippocampus (Carvajal et al., 2016; Gabrieli et al., 2021).”
Background
Potentially addictive behaviours increase during the first six months of the Covid-19 pandemic
Maráz, A., Katzinger, E., & Yi, S. (2021) · Journal of Behavioral Addictions · doi:10.1556/2006.2021.00079 · Cited by 17 · see citing works
Breakdown of utilitarian moral judgement after basolateral amygdala damage
van Honk, J., Terburg, D., Montoya, E. R., Grafman, J. H., Stein, D. J., & Morgan, B. E. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2119072119 · Cited by 18 · see citing works
“Human lesion, neuroimaging, and intracranial electroencephalography studies have implicated the amygdala, the nucleus accumbens (NAc), and most prominently the ventral medial prefrontal cortex (vmPFC) as key structures in the neural network of moral decision-making (18, 19, 23–26).”
BackgroundInfluential
The basolateral amygdala regulation of complex cognitive behaviours in the five-choice serial reaction time task
Yin, F., Guo, H., Cui, J., Shi, Y., Su, R., Xie, Q., Chang, J.-R., Wang, Y., & Lai, J. (2019) · Psychopharmacology · doi:10.1007/s00213-019-05260-w · Cited by 16 · see citing works
The stressed orbitofrontal cortex.
Sequeira, M. K., & Gourley, S. L. (2021) · Behavioral Neuroscience · doi:10.1037/bne0000456 · Cited by 16 · see citing works
“For example, the basolateral amygdala projects to multiple layers of the prefrontal cortex, including the OFC (Kita and Kitai, 1990) and is itself subject to structural modification and hyper-excitability due to stressor exposure (Sharp, 2017; Vyas et al., 2002).”
Background
Mechanism of Chronic Stress-Induced Glutamatergic Neuronal Damage in the Basolateral Amygdaloid Nucleus
Wang, S., Liu, X., Shi, W., Qian, Q., Zhang, G., Li, Y., Cong, B., & Zuo, M. (2021) · Analytical Cellular Pathology · doi:10.1155/2021/8388527 · Cited by 16 · see citing works
“As a key component of the limbic system, the amygdala plays a crucial role in the onset and progression of stressinduced phobic anxiety and affective disorders [9, 10].”
Background
A prolonged stress rat model recapitulates some PTSD-like changes in sleep and neuronal connectivity
Lo, Y., Yi, P.-L., Hsiao, Y., Lee, T.-Y., & Chang, F. (2023) · Communications Biology · doi:10.1038/s42003-023-05090-9 · Cited by 16 · see citing works
Dysregulation of Serum Exosomal Lipid Metabolism in Schizophrenia: A Biomarker Perspective
Xu, C.-X., Huang, W., Shi, X., Du, Y., Liang, J., Fang, X., Chen, H.-Y., & Cheng, Y. (2024) · Molecular Neurobiology · doi:10.1007/s12035-024-04477-x · Cited by 16 · see citing works
Histone Deacetylase 2-Mediated Epigenetic Regulation is Involved in the Early Isoflurane Exposure-Related Increase in Susceptibility to Anxiety-Like Behaviour Evoked by Chronic Variable Stress in Mice
Peng, L., Liu, X., Yang, Y., Guo, Q., & Zhong, T. (2021) · Neurochemical Research · doi:10.1007/s11064-021-03368-0 · Cited by 16 · see citing works
Regional gray matter volume associated with exercise dependence: A voxel‐based morphometry study
Zhang, F., Wang, S., Feng, Y., Qin, K., Li, H., Wu, B., Jia, Z., & Gong, Q. (2021) · Human Brain Mapping · doi:10.1002/hbm.25585 · Cited by 15 · see citing works
“This process may in some way support the idea that stress plays a role in developing addictions (Ruisoto & Contador, 2019) and in addiction relapse (Sharp, 2017; Sinha & Jastreboff, 2013).”
Background
Optogenetically-induced long term depression in the rat orbitofrontal cortex ameliorates stress-induced reversal learning impairment
Adler, S. M., Girotti, M., & Morilak, D. A. (2020) · Neurobiology of Stress · doi:10.1016/j.ynstr.2020.100258 · Cited by 15 · see citing works
GnRH pulse generator frequency is modulated by kisspeptin and GABA ‐glutamate interactions in the posterodorsal medial amygdala in female mice
Lass, G., Li, X. F., Voliotis, M., Wall, E., de Burgh, R., Ivanova, D., McIntyre, C., Lin, X., Colledge, W. H., Lightman, S. L., et al. (2022) · Journal of Neuroendocrinology · doi:10.1111/jne.13207 · Cited by 15 · see citing works
Sex-dependent effects of early life stress on reinforcement learning and limbic cortico-striatal functional connectivity
Zühlsdorff, K., López‐Cruz, L., Dutcher, E. G., Jones, J. A., Pama, C., Sawiak, S. J., Khan, S. A., Milton, A. L., Robbins, T. W., Bullmore, E. T., et al. (2022) · Neurobiology of Stress · doi:10.1016/j.ynstr.2022.100507 · Cited by 15 · see citing works
“In rodents, fronto-striatal reorganization results from chronic stress, which leads to a shift from goal-directed actions to habitual behaviours (Dias-Ferreira et al., 2009; Sharp, 2017).”
Electroacupuncture alleviates perioperative hypothalamus-pituitary-adrenal axis dysfunction via circRNA-miRNA-mRNA networks
Wang, Y., Hu, W., Han, J., Zheng, J., Jiang, N., Feng, Y., & Tian, Z. (2023) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2023.1115569 · Cited by 15 · see citing works
“In addition to the PVN, the central nucleus of the amygdala (CEA) acts as the physiological response center and also plays a major role in stress mainly through changes in GABAergic neurons (Sharp, 2017).”
Background
Neuroprotective actions of norepinephrine in neurological diseases
Ghasemi, M., & Mehranfard, N. (2024) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-024-02999-w · Cited by 15 · see citing works
“…nerve injury and epilepsy, possibly via facilitating GABAergic neurotransmission and/or suppressing glutamatergic signaling in a variety of circuits and synapses [18, 21, 29, 62, 68, 69, 104, 112, 150, 163, 175, 188, 203]. α1-ARs have been shown to modulate GABA neurotransmission in the brain.”
The neural, behavioral, and epidemiological underpinnings of comorbid alcohol use disorder and post-traumatic stress disorder
Carlson, H. N., & Weiner, J. L. (2020) · International review of neurobiology · doi:10.1016/bs.irn.2020.09.006 · Cited by 14 · see citing works
Effects of combined brief etomidate anesthesia and postnatal stress on amygdala expression of Cl− cotransporters and corticotropin-releasing hormone and alcohol intake in adult rats
Yang, J., Ju, L.-S., Yang, C., Xue, J., Setlow, B., Morey, T. E., Gravenstein, N. L., Seubert, C. N., Vasilopoulos, T., & Martynyuk, A. E. (2018) · Neuroscience Letters · doi:10.1016/j.neulet.2018.08.019 · Cited by 14 · see citing works
Risk for opioid misuse in chronic pain patients is associated with endogenous opioid system dysregulation
Ballester, J., Baker, A. K., Martikainen, I. K., Koppelmans, V., Zubieta, J.-K., & Love, T. (2022) · Translational Psychiatry · doi:10.1038/s41398-021-01775-z · Cited by 13 · see citing works
“We focused on the NAc and amygdala due to their corresponding functionality in pain, negative affect and, more broadly, their prominent roles in addiction [7, 25, 30, 48, 49].”
Background
Basolateral Amygdala Hyperexcitability Is Associated with Precocious Developmental Emergence of Fear-Learning in Fragile X Syndrome
Svalina, M. N., Rio, C. A. C.-D., Kushner, J. K., Levy, A., Baca, S. M., Guthman, E. M., Opendak, M. M., Sullivan, R. M., Restrepo, D., & Huntsman, M. M. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.1776-21.2022 · Cited by 13 · see citing works
Early life exposure to high fructose diet induces metabolic dysregulation associated with sex-specific cognitive impairment in adolescent rats
Barrett, C. E., Jiang, M., O'Flaherty, B. G., Dias, B. G., Rainnie, D. G., Young, L. J., & Menigoz, A. (2021) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2022.109220 · Cited by 13 · see citing works
Cocaine Exposure Increases Excitatory Synaptic Transmission and Intrinsic Excitability in the Basolateral Amygdala in Male and Female Rats and Across the Estrous Cycle
Corbett, C. M., Miller, E. N., Wannen, E. E., Rood, B. D., Chandler, D. J., & Loweth, J. A. (2023) · Neuroendocrinology · doi:10.1159/000531351 · Cited by 13 · see citing works
“Importantly, dopaminergic activity in the VTA can in ﬂ uence glutamatergic projections between the BLA and the medial prefrontal cortex [38], which is one of the major sources of glutamatergic input to the BLA [10].”
BackgroundInfluential
The presence of a social stimulus reduces cocaine-seeking in a place preference conditioning paradigm
Sampedro‐Piquero, P., Ávila‐Gámiz, F., Moreno‐Fernández, R. D., Castilla‐Ortega, E., & Santín, L. J. (2019) · Journal of Psychopharmacology · doi:10.1177/0269881119874414 · Cited by 13 · see citing works
“…in the hippocampus and the amygdala not only take part in the cocaine CPP acquisition, but also in the retrieval of drugrelated memories (Castilla-Ortega et al., 2017; Gremel and Cunningham, 2008), the reconsolidation (Wells et al., 2011) and the reinstatement (Bossert et al., 2013; Sharp, 2017).”
Background
Molecular taxonomy of the primate amygdala via single-nucleus RNA sequencing analysis
Zhang, L., Cheng, Y., Wu, S., Lu, Y., Xue, Z., Chen, X., Chen, D., Zhang, B., Qiu, Z., & Jiang, H. (2021) · 中国科学通报：英文版 · doi:10.1016/j.scib.2021.01.017 · Cited by 13 · see citing works
Identifying the neurophysiological effects of memory-enhancing amygdala stimulation using interpretable machine learning
Sendi, M. S. E., Inman, C. S., Bijanki, K. R., Blanpain, L. T., Park, J. K., Hamann, S. B., Gross, R. E., Willie, J. T., & Mahmoudi, B. (2021) · Brain stimulation · doi:10.1016/j.brs.2021.09.009 · Cited by 13 · see citing works
High-fructose diet initiated during adolescence does not affect basolateral amygdala excitability or affective-like behavior in Sprague Dawley rats
O’Flaherty, B., Neigh, G. N., & Rainnie, D. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.02.042 · Cited by 12 · see citing works
“Furthermore the BLA is hyperactive during MDD, which then normalizes with successful pharmacotherapy [18].”
Influential
Molecular Mechanisms Underlying the Retrieval and Extinction of Morphine Withdrawal-Associated Memories in the Basolateral Amygdala and Dentate Gyrus
Franco‐García, A., Fernández-Gómez, F.-J., Gómez‐Murcia, V., Hidalgo, J. M., Núñez, C., & Milanés, M. V. (2022) · Biomedicines · doi:10.3390/biomedicines10030588 · Cited by 12 · see citing works
“The BLA is involved in the codification of conditioned stimuli’s emotional value, therefore playing a critical role in goal directed behaviours [16,37,54].”
Background
Traumatic Brain Injury and Alcohol Drinking Alter Basolateral Amygdala Endocannabinoids in Female Rats
Stielper, Z. F., Fucich, E. A., Middleton, J. W., Hillard, C. J., Edwards, S., Molina, P. E., & Gilpin, N. W. (2020) · Journal of Neurotrauma · doi:10.1089/neu.2020.7175 · Cited by 12 · see citing works

Basolateral amygdala, nicotinic cholinergic receptors, and nicotine: Pharmacological effects and addiction in animal models and humans
Sharp, B. M. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.13970 · Cited by 25 · see citing works
Self-citation
Amygdala and bed nucleus of the stria terminalis circuitry: Implications for addiction-related behaviors
Stamatakis, A. M., Sparta, D. R., Jennings, J. H., McElligott, Z. A., Decot, H., & Stuber, G. D. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.05.046 · Cited by 132 · see citing works
Basolateral amygdala and ventral hippocampus in stress-induced amplification of nicotine self-administration during reacquisition in rat
Yu, G., & Sharp, B. M. (2015) · Psychopharmacology · doi:10.1007/s00213-015-3911-4 · Cited by 21 · see citing works
Self-citation
Cocaine and chronic stress exposure produce an additive increase in neuronal activity in the basolateral amygdala
Munshi, S., Rosenkranz, J. A., Caccamise, A. J., Wolf, M. E., Corbett, C. M., & Loweth, J. A. (2019) · Addiction Biology · doi:10.1111/adb.12848 · Cited by 18 · see citing works
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Authors: Sharp, B. M.
Affiliations: University of Tennessee Health Science Center (US)
Corresponding author: Sharp, B M
ORCID: Sharp, B M
Venue: Translational Psychiatry
Publisher: Springer Science and Business Media LLC
Published: 2017-08-08
Volume: 7
Issue: 8
Pages: e1194-e1194
ISSN: 2158-3188 (ISSN-L)
DOI: 10.1038/tp.2017.161
PMC: PMC5611728
OpenAlex: W2743494055
Cited by: 244
References: 160
Citations by year: 2026: 19 · 2025: 26 · 2024: 31 · 2023: 34 · 2022: 33 · 2021: 41 · 2020: 30 · 2019: 19 · 2018: 10 · 2017: 1
FWCI: 2.02
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by-nc-nd
creativecommons.org/licenses/by-nc-nd/4.0 (tdm)
creativecommons.org/licenses/by-nc-nd/4.0 (vor)
Locations: Translational Psychiatry (publishedVersion, cc-by-nc-nd)
Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
PubMed Central (publishedVersion, cc-by-nc-nd)
PubMed (publishedVersion)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: basolateral amygdala, motivated behavior, addiction, nicotine dependence, drug-seeking behavior, drug relapse, chronic stress, principal neurons, GABAergic circuits, anxiety, fear, post-traumatic stress disorder, autism spectrum disorder, attention deficit hyperactivity disorder, cue reactivity
MeSH terms: Animals, Humans, Motivation, Neurons, Stress, Psychological, Behavior, Addictive, Drug-Seeking Behavior, Basolateral Nuclear Complex

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Basolateral amygdala and stress-induced hyperexcitability affect motivated behaviors and addiction

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