Differential effects of predator stress and the antidepressant tianeptine on physiological plasticity in the hippocampus and basolateral amygdala

Vouimba, Rose-Marie; Muñoz, Carmen; Diamond, David M.

doi:10.1080/10253890600610973

Cited by 96Memory and Neural MechanismsNeuroscience and Neuropharmacology ResearchStress Responses and Cortisol

Differential effects of predator stress and the antidepressant tianeptine on physiological plasticity in the hippocampus and basolateral amygdala

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Vouimba, Rose-Marie, Muñoz, Carmen, Diamond, David M.·2006·Stress

DOI 10.1080/10253890600610973

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Abstract

Stress can profoundly affect memory and alter the functioning of the hippocampus and amygdala. Studies have also shown that the antidepressant tianeptine can block the effects of stress on hippocampal and amygdala morphology and synaptic plasticity. We examined the effects of acute predator stress and tianeptine on long-term potentiation (LTP; induced by 100 pulses in 1 s) and primed burst potentiation (PB; a low threshold form of LTP induced by only five physiologically patterned pulses) in CA1 and in the basolateral nucleus (BLA) of the amygdala in anesthetized rats. Predator stress blocked the induction of PB potentiation in CA1 and enhanced LTP in BLA. Tianeptine blocked the stress-induced suppression of PB potentiation in CA1 without affecting the stress-induced enhancement of LTP in BLA. In addition, tianeptine administered under non-stress conditions enhanced PB potentiation in the hippocampus and LTP in the amygdala. These findings support the hypothesis that acute stress impairs hippocampal functioning and enhances amygdaloid functioning. The work also provides insight into the actions of tianeptine with the finding that it enhanced electrophysiological measures of plasticity in the hippocampus and amygdala under stress, as well as non-stress, conditions.

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Stress blocked the induction of PB potentiation in vivo and in vitro.
“and blocked the induction of PB potentiation in vivo (Diamond et al. [139]; Vouimba et al. [140]) and in vitro (Mesches et al. [51]).”
From The Temporal Dynamics Model of Emotional Memory Processing: A Synthesis on the Neurobiological Basis of Stress-Induced Amnesia, Flashbulb and Traumatic Memories, and the Yerkes-Dodson Law (2007) · cites this paper as Vouimba et al. [140]
Predator stress blocked PB potentiation in CA1 and enhanced LTP in the basolateral nucleus of the amygdala.
“our group has shown that predator stress blocked PB potentiation in CA1 and enhanced LTP in the basolateral nucleus of the amygdala (Vouimba et al. [140]).”
From The Temporal Dynamics Model of Emotional Memory Processing: A Synthesis on the Neurobiological Basis of Stress-Induced Amnesia, Flashbulb and Traumatic Memories, and the Yerkes-Dodson Law (2007) · cites this paper as Vouimba et al. [140]
Acute stress simultaneously enhances plasticity in the amygdala and impairs plasticity in the hippocampus.
“Elsewhere, we have commented on the functional consequences of how acute stress appears to simultaneously enhance plasticity in the amygdala and impair plasticity in the hippocampus (Vouimba et al. [140]).”
From The Temporal Dynamics Model of Emotional Memory Processing: A Synthesis on the Neurobiological Basis of Stress-Induced Amnesia, Flashbulb and Traumatic Memories, and the Yerkes-Dodson Law (2007) · cites this paper as Vouimba et al. [140]

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Memories of Things Unseen
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Exposure to a novel environment interferes with the induction of hippocampal primed burst potentiation in the behaving rat
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Neural plasticity and stress induced changes in defense in the rat
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The Relationship between Acute Glucocorticoid Levels and Hippocampal Function Depends upon Task Aversiveness and Memory Processing Stage
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Is major depression a neurologic disorder with psychiatric symptoms?
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Preclinical research on stress, memory, and the brain in the development of pharmacotherapy for depression
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Hormetic Influence of Glucocorticoids on Human Memory
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Simultaneous induction of long-term potentiation in the hippocampus and the amygdala by entorhinal cortex activation: mechanistic and temporal profiles
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Placebo-Controlled Study of Tianeptine in Major Depressive Episodes
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Mechanisms underlying the inhibition of long-term potentiation by preconditioning stimulation in the hippocampus in vitro
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Neurochemical and Pharmacological Properties of Tianeptine, A Novel Antidepressant
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Investigation of the effects of tianeptine and fluoxetine on pentylenetetrazole-induced seizures in rats
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Footshock stress but not contextual fear conditioning induces long‐term enhancement of auditory‐evoked potentials in the basolateral amygdala of the freely behaving rat
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Effects of tianeptine in animal models of anxiety and on learning and memory
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Synaptic plasticity and tianeptine: structural regulation
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Neuronal Mechanisms of Memory Formation
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Action potential broadening induced by lithium may cause a presynaptic enhancement of excitatory synaptic transmission in neonatal rat hippocampus
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The relationship between episodic memory and context: clues from memory errors made while under stress
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The Enhancement of Hippocampal Primed Burst Potentiation by Dehydroepiandrosterone Sulfate (DHEAS) is Blocked by Psychological Stress
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Lithium enhances synaptic transmission in neonatal rat hippocampus
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Tianeptine as a Slightly Effective Therapeutic Option for Attention-Deficit Hyperactivity Disorder
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Differential Effects of Stress on Hippocampal and Amygdaloid LTP: Insight Into the Neurobiology of Traumatic Memories
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Effects of Novel versus Repeated Mild Stressful Experiences on Long‐Term Potentiation Induced Simultaneously in the Amygdala and Hippocampus in Freely Behaving Rats
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Serotonin Release in Rat Hippocampus Examined by in Vivo Voltammetry: Serotonergic Function and Tryptophan Availability
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Preclinical studies with tianeptine reinforce the neuroplasticity approach to the pathophysiology of major depression
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Untitled work
(1999) · doi:10.1002/(sici)1098-1063(1999)9:5
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Stress, Depression, and Neuroplasticity: A Convergence of Mechanisms
Pittenger, C., & Duman, R. S. (2008) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301574 · Cited by 1,795 · see citing works
“…antidepressant medications with less anticholinergic effect, have suggested that chronic administration of an SSRI or an atypical antidepressant (tianeptine) increases LTP and blocks the stress-induced impairment of LTP and enhancement of LTD in CA1 (Vouimba et al, 2006; Holderbach et al, 2007).”
BackgroundInfluential
The Temporal Dynamics Model of Emotional Memory Processing: A Synthesis on the Neurobiological Basis of Stress-Induced Amnesia, Flashbulb and Traumatic Memories, and the Yerkes-Dodson Law
Diamond, D. M., Campbell, A. M., Park, C. R., Halonen, J., & Zoladz, P. R. (2007) · Neural Plasticity · doi:10.1155/2007/60803 · Cited by 762 · see citing works
“…impaired hippocampus-dependent memory (Diamond et al. [134]; Diamond et al. [52]; Woodson et al. [135]; Sandi et al. [136]; Diamond et al. [137]; Park et al. [138]) and blocked the induction of PB potentiation in vivo (Di-amond et al. [139]; Vouimba et al. [140]) and in vitro (Mesches et al. [51]).”
BackgroundSelf-citation
The Influence of Stress Hormones on Fear Circuitry
Rodrigues, S. M., LeDoux, J. E., & Sapolsky, R. M. (2009) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.051508.135620 · Cited by 556 · see citing works
The neurobiological properties of tianeptine (Stablon): from monoamine hypothesis to glutamatergic modulation
McEwen, B. S., Chattarji, S., Diamond, D. M., Jay, T. M., Reagan, L. P., Svenningsson, P., & Fuchs, E. (2010) · Molecular Psychiatry · doi:10.1038/mp.2009.80 · Cited by 406 · see citing works
“Recently, Vouimba and coworkers (56) reported that tianeptine blocked the stress-induced suppression of primed burst potentiation in CA1 of rat hippocampus without affecting the stress induced enhancement of LTP in the BLA.”
BackgroundSelf-citation
A potential role for pro-inflammatory cytokines in regulating synaptic plasticity in major depressive disorder
Khairova, R. A., Machado-Vieira, R., Du, J., & Manji, H. K. (2009) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145709009924 · Cited by 350 · see citing works
“Recent studies also suggest that chronic administration of a selective serotonin reuptake inhibitor (SSRI) or an atypical antidepressant (tianeptine) increases LTP and blocks the stress-induced impairment of LTP and enhancement of LTD in the CA1 region (Holderbach et al. 2007; Vouimba et al. 2006).”
Background
Chronic stress and brain plasticity: Mechanisms underlying adaptive and maladaptive changes and implications for stress-related CNS disorders
Radley, J., Morilak, D., Viau, V., & Campeau, S. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.06.018 · Cited by 339 · see citing works
“…excitatory, although some studies suggest inhibitory effects (Buffalari and Grace, 2007; Chen and Sara, 2007; Correll et al., 2005; Garcia et al., 1998; Kavushansky and Richter-Levin, 2006; Kavushansky et al., 2006; Pelletier et al., 2005; Shors, 1999; Vouimba et al., 2006; Vouimba et al., 2004).”
Background
Epigenetic modification of hippocampal Bdnf DNA in adult rats in an animal model of post-traumatic stress disorder
Roth, T. L., Zoladz, P. R., Sweatt, J. D., & Diamond, D. M. (2011) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2011.01.013 · Cited by 321 · see citing works
Self-citation
Neurobiological and clinical effects of the antidepressant tianeptine
Kasper, S., & McEwen, B. S. (2008) · CNS Drugs · doi:10.2165/00023210-200822010-00002 · Cited by 302 · see citing works
“[12] Although acute administration of tianeptine did not alter stress-induced enhancement of amygdala function in this study,[12] in another animal study, long-term tianeptine administration had an effect on fear circuitry in the amygdala.”
Influential
Neighborhood matters: divergent patterns of stress-induced plasticity across the brain
Chattarji, S., Tomar, A., Suvrathan, A., Ghosh, S., & Rahman, M. M. (2015) · Nature Neuroscience · doi:10.1038/nn.4115 · Cited by 248 · see citing works
Neuroactive steroids: State of the art and new perspectives
Melcangi, R. C., García‐Segura, L. M., & Mensah‐Nyagan, A. G. (2007) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-007-7403-5 · Cited by 232 · see citing works
Understanding stress: Insights from rodent models
Atrooz, F., Alkadhi, K. A., & Salim, S. (2021) · Current Research in Neurobiology · doi:10.1016/j.crneur.2021.100013 · Cited by 201 · see citing works
Acute episodes of predator exposure in conjunction with chronic social instability as an animal model of post-traumatic stress disorder
Zoladz, P. R., Conrad, C. D., Fleshner, M., & Diamond, D. M. (2008) · Stress · doi:10.1080/10253890701768613 · Cited by 162 · see citing works
“…Chattarji 2004; Mitra et al. 2005; Vyas et al. 2002, 2003, 2006) or stress-induced LTP (Kavushansky and Richter-Levin 2006; Manzanares et al. 2005; Vouimba et al. 2004, 2006), lends itself to experimentation via pharmacological manipulations of the reconsolidation process, which is likely to…”
Self-citation
Learning as a Model for Neural Plasticity in Major Depression
Nissen, C., Holz, J., Jens Blechert, A., Feige, B., Riemann, D. W., Voderholzer, U., & Normann, C. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.05.026 · Cited by 125 · see citing works
Psychosocial animal model of PTSD produces a long-lasting traumatic memory, an increase in general anxiety and PTSD-like glucocorticoid abnormalities
Zoladz, P. R., Fleshner, M., & Diamond, D. M. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.02.007 · Cited by 120 · see citing works
“We have also demonstrated that cat exposure impaired memory-related functions of the hippocampus (Diamond et al., 1999, 2007; Mesches et al., 1999; Vanelzakker et al., 2011; Vouimba et al., 2006), and, conversely, enhanced synaptic plasticity (Vouimba et al.”
InfluentialSelf-citation
Animal models in translational studies of PTSD
Daskalakis, N. P., Yehuda, R., & Diamond, D. M. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.06.006 · Cited by 116 · see citing works
“Extensive preclinical research has shown that tianeptine reverses stress-induced alterations of neuronal morphology and synaptic plasticity and blocks the effects of stress on learning and memory (Shakesby et al., 2002; Diamond et al., 2004; Vouimba et al., 2006; Campbell et al., 2008; Kasper and McEwen, 2008; Zoladz…”
Self-citation
Cellular and Molecular Differences Between Area CA1 and the Dentate Gyrus of the Hippocampus
Alkadhi, K. A. (2019) · Molecular Neurobiology · doi:10.1007/s12035-019-1541-2 · Cited by 113 · see citing works
The As and Ds of stress: Metabolic, morphological and behavioral consequences
Reagan, L. P., Grillo, C. A., & Piroli, G. G. (2008) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2008.02.050 · Cited by 111 · see citing works
Stress enhances fear by forming new synapses with greater capacity for long-term potentiation in the amygdala
Suvrathan, A., Bennur, S., Ghosh, S., Tomar, A., Anilkumar, S., & Chattarji, S. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0151 · Cited by 110 · see citing works
Animal Models of PTSD: A Critical Review
Flandreau, E. I., & Tóth, M. (2017) · Current topics in behavioral neurosciences · doi:10.1007/7854_2016_65 · Cited by 108 · see citing works
“In support of the predictive validity of predator stress paradigms, benzodiazepines, SSRIs, and the tricyclic antidepressant tianeptine have all been shown to efficiently reduce some PTSD-like symptoms of predator exposure [89, 107, 108].”
Neuroplasticity and major depression, the role of modern antidepressant drugs
Serafini, G. (2012) · World Journal of Psychiatry · doi:10.5498/wjp.v2.i3.49 · Cited by 103 · see citing works
Effects of fluoxetine, tianeptine and olanzapine on unpredictable chronic mild stress-induced depression-like behavior in mice
Mutlu, O., Gumuslu, E., Ulak, G., Celikyurt, I. K., Kokturk, S., Kır, H. M., Akar, F., & Erden, F. (2012) · Life Sciences · doi:10.1016/j.lfs.2012.09.023 · Cited by 97 · see citing works
Regulation of AMPA receptor surface trafficking and synaptic plasticity by a cognitive enhancer and antidepressant molecule
Zhang, H., Etherington, L.-A., Hafner, A., Belelli, D., Coussen, F., Delagrange, P., Chaouloff, F., Spedding, M., Lambert, J. J., Choquet, D., et al. (2012) · Molecular Psychiatry · doi:10.1038/mp.2012.80 · Cited by 92 · see citing works
Antidepressants reverse the attenuation of the neurotrophic MEK/MAPK cascade in frontal cortex by elevated platform stress; reversal of effects on LTP is associated with GluA1 phosphorylation
Qi, H., Mailliet, F., Spedding, M., Rocher, C., Zhang, X., Delagrange, P., McEwen, B. S., Jay, T. M., & Svenningsson, P. (2008) · Neuropharmacology · doi:10.1016/j.neuropharm.2008.06.068 · Cited by 91 · see citing works
“…on the key cognitive circuits connecting the hippocampus and prefrontal cortex (H-PFC) while increasing the measures of plasticity in the amygdala subserving fear and emotional memories (Rocher et al., 2004; Cerqueira et al., 2007; Vouimba et al., 2006; Vyas et al., 2006; McEwen, 2007).”
Neuropeptides in depression: Role of VGF
Thakker‐Varia, S., & Alder, J. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.10.006 · Cited by 86 · see citing works
Depressive behavior and activation of the orexin/hypocretin system.
Arendt, D. H., Ronan, P. J., Oliver, K. D., Callahan, L. B., Summers, T. R., & Summers, C. H. (2013) · Behavioral Neuroscience · doi:10.1037/a0031442 · Cited by 84 · see citing works
Differential expression of molecular markers of synaptic plasticity in the hippocampus, prefrontal cortex, and amygdala in response to spatial learning, predator exposure, and stress‐induced amnesia
Zoladz, P. R., Park, C. R., Halonen, J. D., Salim, S., Alzoubi, K. H., Srivareerat, M., Fleshner, M., Alkadhi, K. A., & Diamond, D. M. (2011) · Hippocampus · doi:10.1002/hipo.20922 · Cited by 79 · see citing works
“led to increased p-CaMKII in the BLA is consistent with previous research revealing that acute stress enhances synaptic plasticity in the amygdala (Vouimba et al., 2004; Vouimba et al., 2006).”
ResultSelf-citation
Amygdala modulation of memory-related processes in the hippocampus: potential relevance to PTSD
Tsoory, M. M., Vouimba, R. M., Akirav, I., Kavushansky, A., Avital, A., & Richter-Levin, G. (2007) · Progress in Brain Research · doi:10.1016/s0079-6123(07)67003-4 · Cited by 78 · see citing works
“BLA basolateral amygdala CA1 cornu ammonis field 1 CAM-L1 cell adhesion molecule L1 CORT corticosterone DG dentate gyrus DSM-IV diagnostic and statistical manual of mental disorders, 4th edition EC entorhinal cortex ELS early-life stress ERK2 extracellular signal-regulated kin- ases HPA hypothalamic-pituitary-adrenal…”
BackgroundInfluentialSelf-citation
Repeated restraint stress increases basolateral amygdala neuronal activity in an age-dependent manner
Zhang, W., & Rosenkranz, J. A. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.08.051 · Cited by 77 · see citing works
“While there is much known about the impact of acute stressors on BLA physiology (e.g Shors, 1999; Vouimba et al, 2004, 2006; Pelletier et al, 2005; Kavushansky et al, 2006; Isoardi et al, 2007; Karst et al, 2010), much less is known about the effects of chronic stressors on BLA physiology.”
Background
Effects of repeated stress on excitatory drive of basal amygdala neurons in vivo
Padival, M., Quinette, D., & Rosenkranz, J. A. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.74 · Cited by 75 · see citing works
Differential effectiveness of tianeptine, clonidine and amitriptyline in blocking traumatic memory expression, anxiety and hypertension in an animal model of PTSD
Zoladz, P. R., Fleshner, M., & Diamond, D. M. (2013) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2013.01.001 · Cited by 73 · see citing works
“Indeed, we have reported that tianeptine enhanced spatial memory and synaptic plasticity by blocking the adverse effects of acute stress on both measures (Campbell et al., 2008; Diamond et al., 2004; Vouimba et al., 2006; Zoladz and Diamond, 2010; Zoladz et al., 2008b).”
InfluentialSelf-citation
Antidepressants are a rational complementary therapy for the treatment of Alzheimer's disease
Aboukhatwa, M. A., Dosanjh, L. E., & Luo, Y. (2010) · Molecular Neurodegeneration · doi:10.1186/1750-1326-5-10 · Cited by 69 · see citing works
“As a proof of concept, chronic treatment with atypical antidepressant (tiapentine) or SSRIs that have less anticholinergic properties in comparison to TCAs increase LTP and prevent stress induced reduction in LTP [98,99].”
Influential
The antidepressant agomelatine blocks the adverse effects of stress on memory and enables spatial learning to rapidly increase neural cell adhesion molecule (NCAM) expression in the hippocampus of rats
Conboy, L., Tanrıkut, C., Zoladz, P. R., Campbell, A. M., Park, C. R., Gabriel, C., Mocaër, E., Sandi, C., & Diamond, D. M. (2008) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145708009255 · Cited by 66 · see citing works
Self-citation
The role of serotonin in the enhancement of long-term memory resulting from predator detection in Lymnaea
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Pre-training administration of tianeptine, but not propranolol, protects hippocampus-dependent memory from being impaired by predator stress
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Self-citation

Authors: Vouimba, R.-M., Muñoz, C., & Diamond, D. M.
Affiliations: University of South Florida (US)
Corresponding author: Diamond, David M.
ORCID: Vouimba, Rose-Marie
Diamond, David M.
Venue: Stress
Publisher: Informa UK Limited
Published: 2006-01
Volume: 9
Issue: 1
Pages: 29-40
ISSN: 1025-3890 (ISSN-L)
1607-8888
DOI: 10.1080/10253890600610973
OpenAlex: W1963799398
Cited by: 96
References: 135
Citations by year: 2026: 2 · 2022: 1 · 2021: 2 · 2020: 3 · 2019: 4 · 2018: 3 · 2017: 2 · 2016: 6 · 2015: 6 · 2014: 5 · 2013: 8 · 2012: 12
FWCI: 4.83
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Stress (publishedVersion)
PubMed (publishedVersion)
Digital Commons - University of South Florida (University of South Florida) (submittedVersion)
Funders: Servier
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Keywords: predator stress, tianeptine, hippocampus, basolateral amygdala, long-term potentiation, synaptic plasticity, acute stress, antidepressants, CA1, memory
MeSH terms: Amygdala, Animals, Antidepressive Agents, Tricyclic, Cats, Evoked Potentials, Hippocampus, Male, Neuronal Plasticity, Stress, Psychological, Thiazepines, Long-Term Potentiation, Rats

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Differential effects of predator stress and the antidepressant tianeptine on physiological plasticity in the hippocampus and basolateral amygdala

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