Effects of repeated stress on excitatory drive of basal amygdala neurons in vivo

Padival, Mallika; Quinette, Danielle; Rosenkranz, J Amiel

doi:10.1038/npp.2013.74

Cited by 75Neuroscience and Neuropharmacology ResearchStress Responses and CortisolMemory and Neural Mechanisms

Effects of repeated stress on excitatory drive of basal amygdala neurons in vivo

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Padival, Mallika, Quinette, Danielle, Rosenkranz, J Amiel·2013·Neuropsychopharmacology

DOI 10.1038/npp.2013.74PMC PMC3717551

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Abstract

Chronic stress leads to heightened affective behaviors, and can precipitate the emergence of depression and anxiety. These disorders are associated with increased amygdala activity. In animal models, chronic stress leads to increased amygdala-dependent behaviors, as well as hyperactivity of amygdala neurons. However, it is not known whether increased excitatory synaptic drive after chronic stress contributes to hyperactivity of basolateral amygdala (BLA; comprised of basal, lateral, and accessory basal nuclei) neurons. This study tested whether repeated stress causes an increase in excitatory drive of basal amygdala (BA) neurons in vivo, and whether this is correlated with an increase in the number of dendritic spines and a shift in dendritic distribution. Using in vivo intracellular recordings, this study found that repeated restraint stress caused an increase in the frequency of spontaneous excitatory synaptic events in vivo, which correlated with the number of dendritic spines in reconstructed neurons. Furthermore, parallel changes in the kinetics of the synaptic events and the distribution of spines indicated a more prominent functional contribution of synaptic inputs from across the dendritic tree. The shift in spine distribution across the dendritic tree was further confirmed with the examination of Golgi-stained tissue. This abnormal physiological drive of BA neurons after repeated stress may contribute to heightened affective responses after chronic stress. A reduction in the impact of excitatory drive in the BA may therefore be a potential treatment for the harmful effects of chronic stress in psychiatric disorders.

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Chronic stress results in an increase in dendritic arborization and spinogenesis on BLA pyramidal neurons, increasing their intrinsic excitability and afferent stimulation in a manner that correlates with heightened anxiety-like behavior.
“Additionally, multiple studies have found that chronic stress results in an increase in dendritic arborization and spinogenesis on BLA pyramidal neurons, increasing their intrinsic excitability and afferent stimulation in a manner that correlates with heightened anxiety-like behavior [70–72].”
From Amygdala FAAH and anandamide: mediating protection and recovery from stress (2013) · cites this paper as [72]

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Effects of stress throughout the lifespan on the brain, behaviour and cognition
Lupien, S. J., McEwen, B. S., Gunnar, M. R., & Heim, C. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2639 · Cited by 6,256 · see citing works
Thalamocortical oscillations in the sleeping and aroused brain
Steriade, M., McCormick, D. A., & Sejnowski, T. J. (1993) · Science · doi:10.1126/science.8235588 · Cited by 3,564 · see citing works
The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies
Heim, C., & Nemeroff, C. B. (2001) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01157-x · Cited by 2,791 · see citing works
The three-dimensional organization of the hippocampal formation: A review of anatomical data
Amaral, D. G., & Witter, M. P. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90424-7 · Cited by 2,180 · see citing works
Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons
Vyas, A., Mitra, R., Shankaranarayana Rao, B. S., & Chattarji, S. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-15-06810.2002 · Cited by 1,662 · see citing works
Cellular and network mechanisms of rhythmic recurrent activity in neocortex
Sanchez-Vives, M. V., & McCormick, D. A. (2000) · Nature Neuroscience · doi:10.1038/79848 · Cited by 1,539 · see citing works
A functional anatomical study of unipolar depression
Drevets, W., Videen, T., Price, J., Preskorn, S., Carmichael, S., & Raichle, M. (1992) · The Journal of Neuroscience · doi:10.1523/jneurosci.12-09-03628.1992 · Cited by 1,266 · see citing works
Influence of dendritic structure on firing pattern in model neocortical neurons
Mainen, Z. F., & Sejnowski, T. J. (1996) · Nature · doi:10.1038/382363a0 · Cited by 1,231 · see citing works
Increased amygdala response to masked emotional faces in depressed subjects resolves with antidepressant treatment: an fMRI study
Sheline, Y. I., Barch, D. M., Donnelly, J. M., Ollinger, J. M., Snyder, A. Z., & Mintun, M. A. (2001) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01263-x · Cited by 1,191 · see citing works
Neocortical Network ActivityIn VivoIs Generated through a Dynamic Balance of Excitation and Inhibition
Haider, B., Duque, A., Hasenstaub, A. R., & McCormick, D. A. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.5297-05.2006 · Cited by 962 · see citing works
Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex.
Markram, H., Lübke, J., Frotscher, M., Roth, A., & Sakmann, B. (1997) · The Journal of Physiology · doi:10.1113/jphysiol.1997.sp022031 · Cited by 960 · see citing works
Limbic scars: long-term consequences of childhood maltreatment revealed by functional and structural magnetic resonance imaging
Dannlowski, U., Stuhrmann, A., Beutelmann, V., Zwanzger, P., Lenzen, T., Grotegerd, D., Domschke, K., Hohoff, C., Ohrmann, P., Bauer, J., et al. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.10.021 · Cited by 954 · see citing works
Intracellular analysis of relations between the slow (< 1 Hz) neocortical oscillation and other sleep rhythms of the electroencephalogram
Steriade, M., Nunez, A., & Amzica, F. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-08-03266.1993 · Cited by 894 · see citing works
Topographic organization of the projections from the entorhinal area to the hippocampal formation of the rat
Steward, O. (1976) · The Journal of Comparative Neurology · doi:10.1002/cne.901670303 · Cited by 883 · see citing works
Chronic Psychosocial Stress Causes Apical Dendritic Atrophy of Hippocampal CA3 Pyramidal Neurons in Subordinate Tree Shrews
Magariños, A. M., McEwen, B. S., Flügge, G., & Fuchs, E. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-10-03534.1996 · Cited by 864 · see citing works
Can’t shake that feeling: event-related fMRI assessment of sustained amygdala activity in response to emotional information in depressed individuals
Siegle, G. J., Steinhauer, S. R., Thase, M. E., Stenger, V. A., & Carter, C. S. (2002) · Biological Psychiatry · doi:10.1016/s0006-3223(02)01314-8 · Cited by 859 · see citing works
Genetic dissection of an amygdala microcircuit that gates conditioned fear
Haubensak, W., Kunwar, P. S., Cai, H., Ciocchi, S., Wall, N. R., Ponnusamy, R., Biag, J., Dong, H.-W., Deisseroth, K., Callaway, E. M., et al. (2010) · Nature · doi:10.1038/nature09553 · Cited by 840 · see citing works
Internal brain state regulates membrane potential synchrony in barrel cortex of behaving mice
Poulet, J. F. A., & Petersen, C. C. H. (2008) · Nature · doi:10.1038/nature07150 · Cited by 796 · see citing works
Dendritic integration of excitatory synaptic input
Magee, J. C. (2000) · Nature reviews. Neuroscience · doi:10.1038/35044552 · Cited by 737 · see citing works
Cellular basis of EEG slow rhythms: a study of dynamic corticothalamic relationships
Contreras, D., & Steriade, M. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-01-00604.1995 · Cited by 700 · see citing works
Repeated restraint stress facilitates fear conditioning independently of causing hippocampal CA3 dendritic atrophy
Conrad, C. D., Magariños, A. M., LeDoux, J. E., & McEwen, B. S. (1999) · Behavioral Neuroscience · doi:10.1037/0735-7044.113.5.902 · Cited by 664 · see citing works
Repeated restraint stress facilitates fear conditioning independently of causing hippocampal CA3 dendritic atrophy.
Conrad, C. D., Magariños, A. M., LeDoux, J. E., & McEwen, B. S. (1999) · Behavioral Neuroscience · doi:10.1037//0735-7044.113.5.902 · Cited by 663 · see citing works
Stress duration modulates the spatiotemporal patterns of spine formation in the basolateral amygdala
Mitra, R., Jadhav, S., McEwen, B. S., Vyas, A., & Chattarji, S. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504011102 · Cited by 663 · see citing works
Somatic EPSP amplitude is independent of synapse location in hippocampal pyramidal neurons
Magee, J. C., & Cook, E. P. (2000) · Nature Neuroscience · doi:10.1038/78800 · Cited by 646 · see citing works
Functional magnetic resonance imaging of symptom provocation in obsessive-compulsive disorder
Breiter, H. C. (1996) · Archives of General Psychiatry · doi:10.1001/archpsyc.1996.01830070041008 · Cited by 626 · see citing works
Impact of Network Activity on the Integrative Properties of Neocortical Pyramidal Neurons In Vivo
Alain Destexhe, A., & Paré, D. (1999) · Journal of Neurophysiology · doi:10.1152/jn.1999.81.4.1531 · Cited by 621 · see citing works
Propagation of action potentials in dendrites depends on dendritic morphology
Vetter, P., Roth, A., & Häusser, M. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.85.2.926 · Cited by 598 · see citing works
Amygdala Response to Fearful Faces in Anxious and Depressed Children
Thomas, K. M. (2001) · Archives of General Psychiatry · doi:10.1001/archpsyc.58.11.1057 · Cited by 582 · see citing works
Neuroanatomical basis for facilitation of hypothalamic-pituitary-adrenal responses to a novel stressor after chronic stress
Bhatnagar, S., & Dallman, M. (1998) · Neuroscience · doi:10.1016/s0306-4522(97)00577-0 · Cited by 511 · see citing works
Dendritic organization of sensory input to cortical neurons in vivo
Jia, H., Rochefort, N. L., Chen, X., & Konnerth, A. (2010) · Nature · doi:10.1038/nature08947 · Cited by 508 · see citing works
Sex Differences and Opposite Effects of Stress on Dendritic Spine Density in the Male Versus Female Hippocampus
Shors, T. J., Chua, C., & Falduto, J. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-16-06292.2001 · Cited by 496 · see citing works
The neural substrates of affective processing in depressed patients treated with venlafaxine
Davidson, R. J., Irwin, W., Anderle, M. J., & Kalin, N. H. (2003) · American Journal of Psychiatry · doi:10.1176/appi.ajp.160.1.64 · Cited by 487 · see citing works
Visual Imagery and Perception in Posttraumatic Stress Disorder
Shin, L. M. (1997) · Archives of General Psychiatry · doi:10.1001/archpsyc.1997.01830150057010 · Cited by 446 · see citing works
Somatosensory and auditory convergence in the lateral nucleus of the amygdala.
Romanski, L. M., Clugnet, M.-C., Bordi, F., & LeDoux, J. E. (1993) · Behavioral Neuroscience · doi:10.1037/0735-7044.107.3.444 · Cited by 446 · see citing works
Recovery after chronic stress fails to reverse amygdaloid neuronal hypertrophy and enhanced anxiety-like behavior
Vyas, A., Pillai, A. G., & Chattarji, S. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.07.013 · Cited by 445 · see citing works
Synchronous Membrane Potential Fluctuations in Neurons of the Cat Visual Cortex
Lampl, I., Reichova, I., & Ferster, D. (1999) · Neuron · doi:10.1016/s0896-6273(00)81096-x · Cited by 434 · see citing works
Spatiotemporal Dynamics of Sensory Responses in Layer 2/3 of Rat Barrel Cortex MeasuredIn Vivoby Voltage-Sensitive Dye Imaging Combined with Whole-Cell Voltage Recordings and Neuron Reconstructions
Petersen, C. C. H., Grinvald, A., & Sakmann, B. J. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-04-01298.2003 · Cited by 423 · see citing works
Cellular Mechanisms of Infralimbic and Prelimbic Prefrontal Cortical Inhibition and Dopaminergic Modulation of Basolateral Amygdala NeuronsIn Vivo
Rosenkranz, J. A., & Grace, A. A. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-01-00324.2002 · Cited by 392 · see citing works
Self-citation
Dependence of EPSP Efficacy on Synapse Location in Neocortical Pyramidal Neurons
Williams, S. R., & Stuart, G. J. (2002) · Science · doi:10.1126/science.1067903 · Cited by 378 · see citing works
Repeated stress alters dendritic spine morphology in the rat medial prefrontal cortex
Radley, J. J., Rocher, A. B., Rodriguez, A., Ehlenberger, D. B., Dammann, M., McEwen, B. S., Morrison, J. H., Wearne, S. L., & Hof, P. R. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21588 · Cited by 374 · see citing works
Neurons of the lateral and basolateral amygdaloid nuclei: A golgi study in the rat
McDonald, A. J. (1982) · The Journal of Comparative Neurology · doi:10.1002/cne.902120307 · Cited by 371 · see citing works
Top-down Dendritic Input Increases the Gain of Layer 5 Pyramidal Neurons
Larkum, M. E. (2004) · Cerebral Cortex · doi:10.1093/cercor/bhh065 · Cited by 366 · see citing works
Metaplasticity of amygdalar responses to the stress hormone corticosterone
Karst, H., Berger, S., Erdmann, G., Schütz, G., & Joëls, M. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0914381107 · Cited by 342 · see citing works
Prolonged behavioral stress enhances synaptic connectivity in the basolateral amygdala
Vyas, A., Jadhav, S., & Chattarji, S. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.08.003 · Cited by 299 · see citing works
Precise Long-Range Synchronization of Activity and Silence in Neocortical Neurons during Slow-Wave Sleep
Volgushev, M., Chauvette, S., Mukovski, M., & Timofeev, I. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.0279-06.2006 · Cited by 289 · see citing works
Chronic Stress Causes Amygdala Hyperexcitability in Rodents
Rosenkranz, J. A., Venheim, E. R., & Padival, M. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.02.008 · Cited by 284 · see citing works
Self-citation
Differential time courses and specificity of amygdala activity in posttraumatic stress disorder subjects and normal control subjects
Protopopescu, X., Pan, H., Tüscher, O., Cloître, M., Goldstein, M., Engelien, W., Epstein, J., Yang, Y., Gorman, J. M., LeDoux, J. E., et al. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2004.12.026 · Cited by 276 · see citing works
IκB Kinase Regulates Social Defeat Stress-Induced Synaptic and Behavioral Plasticity
Christoffel, D. J., Golden, S. A., Dumitriu, D., Robison, A. J., Janssen, W. G., Ahn, H. F., Krishnan, V., Reyes, C. M., Han, M.-H., Ables, J. L., et al. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.4763-10.2011 · Cited by 267 · see citing works
Coincidence Detection in Pyramidal Neurons Is Tuned by Their Dendritic Branching Pattern
Schaefer, A. T., Larkum, M. E., Sakmann, B. J., & Roth, A. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00046.2003 · Cited by 267 · see citing works
Previous Stress Facilitates Fear Memory, Attenuates GABAergic Inhibition, and Increases Synaptic Plasticity in the Rat Basolateral Amygdala
Manzanares, P. A. R., Isoardi, N. A., Carrer, H. F., & Molina, V. A. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.2260-05.2005 · Cited by 262 · see citing works
Amygdala Response in Patients With Acute PTSD to Masked and Unmasked Emotional Facial Expressions
Armony, J. L., Corbo, V., Clément, M.-H., & Brunet, A. (2005) · American Journal of Psychiatry · doi:10.1176/appi.ajp.162.10.1961 · Cited by 239 · see citing works
Strain Differences in Stress Responsivity Are Associated with Divergent Amygdala Gene Expression and Glutamate-Mediated Neuronal Excitability
Mozhui, K., Karlsson, R.-M., Kash, T. L., Ihne, J., Norcross, M., Patel, S., Farrell, M. R., Hill, E. E., Graybeal, C., Martin, K. P., et al. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.5017-09.2010 · Cited by 226 · see citing works
Habituation to repeated stress is stressor specific
Jean Kant, G., Eggleston, T., Landman-Roberts, L., Kenion, C. C., Driver, G. C., & Meyerhoff, J. L. (1985) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(85)90286-2 · Cited by 225 · see citing works
Disruption of fatty acid amide hydrolase activity prevents the effects of chronic stress on anxiety and amygdalar microstructure
Hill, M. N., Kumar, S. A., Filipski, S. B., Iverson, M., Stuhr, K. L., Keith, J. M., Cravatt, B. F., Hillard, C. J., Chattarji, S., & McEwen, B. S. (2013) · Molecular Psychiatry · doi:10.1038/mp.2012.90 · Cited by 222 · see citing works
Signal enhancement in distal cortical dendrites by means of interactions between active dendritic spines
Shepherd, G. M., Brayton, R. K., Miller, J. P., Segev, I., Rinzel, J., & Rall, W. (1985) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.82.7.2192 · Cited by 220 · see citing works
Computational study of an excitable dendritic spine
Segev, I., & Rall, W. (1988) · Journal of Neurophysiology · doi:10.1152/jn.1988.60.2.499 · Cited by 217 · see citing works
Mechanism of the distance-dependent scaling of Schaffer collateral synapses in rat CA1 pyramidal neurons
Smith, M. A., Ellis‐Davies, G. C. R., & Magee, J. C. (2003) · The Journal of Physiology · doi:10.1111/j.1469-7793.2003.00245.x · Cited by 214 · see citing works
Pyramidal cells of the rat basolateral amygdala: Synaptology and innervation by parvalbumin‐immunoreactive interneurons
Muller, J. F., Mascagni, F., & McDonald, A. J. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20832 · Cited by 203 · see citing works
Central Amygdala Activity during Fear Conditioning
Duvarci, S., Popa, D., & Paré, D. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.4985-10.2011 · Cited by 202 · see citing works
Hippocampal and prefrontal cortical inputs monosynaptically converge with individual projection neurons of the nucleus accumbens
French, S. J., & Totterdell, S. (2002) · The Journal of Comparative Neurology · doi:10.1002/cne.10191 · Cited by 202 · see citing works
Distance-Dependent Increase in AMPA Receptor Number in the Dendrites of Adult Hippocampal CA1 Pyramidal Neurons
Andrásfalvy, B. K., & Magee, J. C. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-23-09151.2001 · Cited by 200 · see citing works
Mechanism of the distance-dependent scaling of Schaffer collateral synapses in rat CA1 pyramidal neurons
Smith, M. A., Ellis‐Davies, G. C. R., & Magee, J. C. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2002.036376 · Cited by 186 · see citing works
Perceived threat predicts the neural sequelae of combat stress
van Wingen, G. A., Geuze, E., Vermetten, E., & Fernández, G. (2011) · Molecular Psychiatry · doi:10.1038/mp.2010.132 · Cited by 173 · see citing works
Mineralocorticoid receptor Iso/Val (rs5522) genotype moderates the association between previous childhood emotional neglect and amygdala reactivity
Bogdan, R., Williamson, D. E., & Hariri, A. R. (2012) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2011.11060855 · Cited by 165 · see citing works
Noradrenergic Modulation of Basolateral Amygdala Neuronal Activity: Opposing Influences of α-2 and β Receptor Activation
Buffalari, D., & Grace, A. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.2007-07.2007 · Cited by 157 · see citing works
Postsynaptic targets of somatostatin‐containing interneurons in the rat basolateral amygdala
Muller, J. F., Mascagni, F., & McDonald, A. J. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.21185 · Cited by 153 · see citing works
Passive Normalization of Synaptic Integration Influenced by Dendritic Architecture
Jaffe, D. B., & Carnevale, N. T. (1999) · Journal of Neurophysiology · doi:10.1152/jn.1999.82.6.3268 · Cited by 151 · see citing works
Dendritic Spine Heterogeneity Determines Afferent-Specific Hebbian Plasticity in the Amygdala
Humeau, Y., Herry, C., Kemp, N., Shaban, H., Fourcaudot, E., Bissière, S., & Lüthi, A. (2005) · Neuron · doi:10.1016/j.neuron.2004.12.019 · Cited by 148 · see citing works
Bursting and oscillating neurons of the cat basolateral amygdaloid complex in vivo: electrophysiological properties and morphological features
Paré, D., Pape, H., & Dong, J. (1995) · Journal of Neurophysiology · doi:10.1152/jn.1995.74.3.1179 · Cited by 147 · see citing works
Stress during development alters dendritic morphology in the nucleus accumbens and prefrontal cortex
Muhammad, A., Carroll, C., & Kolb, B. E. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.04.041 · Cited by 146 · see citing works
Multiple immediate-early gene expression during physiological and endocrine adaptation to repeated stress
Stamp, J. A., & Herbert, J. (1999) · Neuroscience · doi:10.1016/s0306-4522(99)00368-1 · Cited by 145 · see citing works
Lasting increases in basolateral amygdala activity after emotional arousal: implications for facilitated consolidation of emotional memories.Preprint
Pelletier, J., Likhtik, E., Filali, M., & Paré, D. (2005) · Learning & memory (Cold Spring Harbor, N.Y.) · doi:10.1101/lm.88605 · Cited by 145 · see citing works
Stress Impairs α1A Adrenoceptor-Mediated Noradrenergic Facilitation of GABAergic Transmission in the Basolateral Amygdala
Braga, M. F. M., Aroniadou‐Anderjaska, V., Manion, S. T., Hough, C. J., & Li, H. (2003) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300297 · Cited by 141 · see citing works
Activity and plasticity in the CA1, the dentate gyrus, and the amygdala following controllable vs. uncontrollable water stress
Kavushansky, A., Vouimba, R., Cohen, H., & Richter‐Levin, G. (2006) · Hippocampus · doi:10.1002/hipo.20130 · Cited by 141 · see citing works
Modulation of Different States of Anxiety-Like Behavior by Chronic Stress.
Vyas, A., & Chattarji, S. (2004) · Behavioral Neuroscience · doi:10.1037/0735-7044.118.6.1450 · Cited by 136 · see citing works
GABAergic innervation of alpha type II calcium/calmodulin‐dependent protein kinase immunoreactive pyramidal neurons in the rat basolateral amygdala
McDonald, A. J., Muller, J. F., & Mascagni, F. (2002) · The Journal of Comparative Neurology · doi:10.1002/cne.10204 · Cited by 132 · see citing works
Alterations in Corticolimbic Dendritic Morphology and Emotional Behavior in Cannabinoid CB1 Receptor-Deficient Mice Parallel the Effects of Chronic Stress
Hill, M. N., Hillard, C. J., & McEwen, B. S. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhq280 · Cited by 127 · see citing works
Propagation of dendritic spikes mediated by excitable spines: a continuum theory
Baer, S. M., & Rinzel, J. (1991) · Journal of Neurophysiology · doi:10.1152/jn.1991.65.4.874 · Cited by 124 · see citing works
Locus coeruleus activation by foot shock or electrical stimulation inhibits amygdala neurons
Chen, F.-J., & Sara, S. J. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.09.037 · Cited by 123 · see citing works
Retinal input instructs alignment of visual topographic maps
Triplett, J. W., Owens, M. T., Yamada, J., Lemke, G., Cang, J., Stryker, M. P., & Feldheim, D. A. (2009) · Cell · doi:10.1016/j.cell.2009.08.028 · Cited by 123 · see citing works
Rat amygdaloid neuron responses during auditory discrimination
Muramoto, K., Ono, T., Nishijo, H., & Fukuda, M. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90411-8 · Cited by 121 · see citing works
Effects of inescapable stress on LTP in the amygdala versus the dentate gyrus of freely behaving rats
Vouimba, R., Yaniv, D., Diamond, D., & Richter‐Levin, G. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03294.x · Cited by 114 · see citing works
Chronic immobilization stress alters aspects of emotionality and associative learning in the rat.
Wood, G. E., Norris, E. H., Waters, E. M., Stoldt, J. T., & McEwen, B. S. (2008) · Behavioral Neuroscience · doi:10.1037/0735-7044.122.2.282 · Cited by 107 · see citing works
Chronic Cold Stress Alters Prefrontal Cortical Modulation of Amygdala Neuronal Activity in Rats
Correll, C. M., Rosenkranz, J. A., & Grace, A. A. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.04.009 · Cited by 106 · see citing works
Self-citation
Effects of stress and corticosterone on activity and plasticity in the amygdala
Kavushansky, A., & Richter‐Levin, G. (2006) · Journal of Neuroscience Research · doi:10.1002/jnr.21058 · Cited by 106 · see citing works
UNITARY RESPONSES TO AFFERENT VOLLEYS IN AMYGDALOID COMPLEX
Machne, X., & Segundo, J. P. (1956) · Journal of Neurophysiology · doi:10.1152/jn.1956.19.3.232 · Cited by 103 · see citing works
Similar Inhibitory Processes Dominate the Responses of Cat Lateral Amygdaloid Projection Neurons to Their Various Afferents
Lang, E. J., & Paré, D. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.77.1.341 · Cited by 100 · see citing works
Differential effects of predator stress and the antidepressant tianeptine on physiological plasticity in the hippocampus and basolateral amygdala
Vouimba, R.-M., Muñoz, C., & Diamond, D. M. (2006) · Stress · doi:10.1080/10253890600610973 · Cited by 96 · see citing works
The integrative properties of spiny distal dendrites
Jaslove, S. W. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90161-t · Cited by 86 · see citing works
α2‐Adrenoreceptor activation inhibits LTP and LTD in the basolateral amygdala: involvement of Gi/o‐protein‐mediated modulation of Ca2+‐channels and inwardly rectifying K+‐channels in LTD
DeBock, F., Kurz, J., Azad, S. C., Parsons, C. G., Hapfelmeier, G., Zieglgänsberger, W., & Rammes, G. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02544.x · Cited by 81 · see citing works
Glutamate immunoreactive terminals in the lateral amygdaloid nucleus: a possible substrate for emotional memory
Farb, C. R., Aoki, C. J., Milner, T. A., Kaneko, T., & LeDoux, J. E. (1992) · Brain Research · doi:10.1016/0006-8993(92)91303-v · Cited by 80 · see citing works
Amygdalo-entorhinal relations and their reflection in the hippocampal formation: generation of sharp sleep potentials
Paré, D., Dong, J., & Gaudreau, H. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-03-02482.1995 · Cited by 78 · see citing works
Subcellular Topography of Visually Driven Dendritic Activity in the Vertebrate Visual System
Bollmann, J. H., & Engert, F. (2009) · Neuron · doi:10.1016/j.neuron.2009.01.018 · Cited by 78 · see citing works
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
Self-citation
Dendritic morphology of amygdala and hippocampal neurons in more and less predator stress responsive rats and more and less spontaneously anxious handled controls
Adamec, R., Hebert, M., Blundell, J., & Mervis, R. F. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.09.009 · Cited by 74 · see citing works
The aftermath of 9/11: Effect of intensity and recency of trauma on outcome.
Ganzel, B., Casey, B. J., Glover, G., Voss, H. U., & Temple, E. (2007) · Emotion · doi:10.1037/1528-3542.7.2.227 · Cited by 72 · see citing works
Reciprocal Changes in the Firing Probability of Lateral and Central Medial Amygdala Neurons
Collins, D. R., & Paré, D. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-02-00836.1999 · Cited by 70 · see citing works
Role of NMDA receptors in the lateralized potentiation of amygdala afferent and efferent neural transmission produced by predator stress
Adamec, R. E., Blundell, J. J., & Burton, P. (2005) · Physiology & Behavior · doi:10.1016/j.physbeh.2005.06.026 · Cited by 66 · see citing works
Waveform and amplitude characteristics of evoked responses to dendritic stimulation of CA1 guinea‐pig pyramidal cells.
Turner, D. A. (1988) · The Journal of Physiology · doi:10.1113/jphysiol.1988.sp016927 · Cited by 52 · see citing works
Chronic cold stress increases excitatory effects of norepinephrine on spontaneous and evoked activity of basolateral amygdala neurons
Buffalari, D. M., & Grace, A. A. (2008) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145708009140 · Cited by 51 · see citing works
Lack of feedback inhibition on rat basolateral amygdala following stress or withdrawal from sedative‐hypnotic drugs
Isoardi, N. A., Bertotto, M. E., Martijena, I. D., Molina, V. A., & Carrer, H. F. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05714.x · Cited by 50 · see citing works
Morphology, PKCδ expression, and synaptic responsiveness of different types of rat central lateral amygdala neurons
Amano, T., Amir, A., Goswami, S., & Paré, D. (2012) · Journal of Neurophysiology · doi:10.1152/jn.00514.2012 · Cited by 47 · see citing works
The neural consequences of combat stress: long-term follow-up
van Wingen, G. A., Geuze, E., Vermetten, E. H. G. J. M., & Fernández, G. (2011) · Molecular Psychiatry · doi:10.1038/mp.2011.110 · Cited by 47 · see citing works
Factors determining the efficacy of distal excitatory synapses in rat hippocampal CA1 pyramidal neurones
Andreasen, M., & Lambert, J. D. C. (1998) · The Journal of Physiology · doi:10.1111/j.1469-7793.1998.441bt.x · Cited by 45 · see citing works
Projection neurons of the lateral amygdaloid nucleus are virtually silent throughout the sleep--waking cycle
Gaudreau, H., & Paré, D. (1996) · Journal of Neurophysiology · doi:10.1152/jn.1996.75.3.1301 · Cited by 45 · see citing works
Opposing Influence of Basolateral Amygdala and Footshock Stimulation on Neurons of the Central Amygdala
Rosenkranz, J. A., Buffalari, D. M., & Grace, A. A. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.09.013 · Cited by 43 · see citing works
Self-citation
Lasting changes in social behavior and amygdala function following traumatic experience induced by a single series of foot-shocks
Mikics, É., Tóth, M., Varjú, P., Gereben, B., Liposits, Z., Ashaber, M., Halász, J., Barna, I., Farkas, I., & Haller, J. (2008) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2008.06.006 · Cited by 43 · see citing works
Amphetamine-Associated Contextual Learning Is Accompanied by Structural and Functional Plasticity in the Basolateral Amygdala
Rademacher, D. J., Rosenkranz, J. A., Morshedi, M. M., Sullivan, E. M., & Meredith, G. E. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.6165-09.2010 · Cited by 38 · see citing works
Self-citation
Encoding and Decoding of Dendritic Excitation during Active States in Pyramidal Neurons
Williams, S. R. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.0502-05.2005 · Cited by 36 · see citing works
Variation of Input-Output Properties along the Somatodendritic Axis of Pyramidal Neurons
Oviedo, H. V., & Reyes, A. D. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.0562-05.2005 · Cited by 35 · see citing works
Footshock stress but not contextual fear conditioning induces long‐term enhancement of auditory‐evoked potentials in the basolateral amygdala of the freely behaving rat
Garcia, R., Paquereau, J., Vouimba, R. M., & Jaffard, R. (1998) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1998.00027.x · Cited by 32 · see citing works
N-methyl-d-aspartic acid receptors are altered by stress and alcohol in Wistar–Kyoto rat brain
Lei, Y., & Tejani‐Butt, S. M. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.05.003 · Cited by 29 · see citing works
Acute stress and re-exposure to the stressful context suppress spontaneous unit activity in the basolateral amygdala via NMDA receptor activation
Shors, T. J. (1999) · Neuroreport · doi:10.1097/00001756-199909090-00021 · Cited by 27 · see citing works
State-Dependent Modulation of Amygdala Inputs by Dopamine-Induced Enhancement of Sodium Currents in Layer V Entorhinal Cortex
Rosenkranz, J. A., & Johnston, D. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.1744-07.2007 · Cited by 22 · see citing works
Self-citation
Pharmacological enhancement of calcium-activated potassium channel function reduces the effects of repeated stress on fear memory
Atchley, D., Hankosky, E. R., Gasparotto, K., & Rosenkranz, J. A. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.03.037 · Cited by 21 · see citing works
Self-citation
Inhibition Dominates the Early Phase of Up-States in the Basolateral Amygdala
Windels, F., Crane, J. W., & Sah, P. (2010) · Journal of Neurophysiology · doi:10.1152/jn.00531.2010 · Cited by 17 · see citing works
Oscillations in the Basolateral Amygdala: Aversive Stimulation Is State Dependent and Resets the Oscillatory Phase
Crane, J. W., Windels, F., & Sah, P. (2009) · Journal of Neurophysiology · doi:10.1152/jn.00438.2009 · Cited by 12 · see citing works
Neuronal Activity Causes Rapid Changes of Lateral Amygdala Neuronal Membrane Properties and Reduction of Synaptic Integration and Synaptic PlasticityIn Vivo
Rosenkranz, J. A. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.0690-11.2011 · Cited by 10 · see citing works
Self-citation
In vivo voltage-dependent influences on summation of synaptic potentials in neurons of the lateral nucleus of the amygdala
Rosenkranz, J. A. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.09.012 · Cited by 4 · see citing works
Self-citation
Distribution of NMDA and AMPA receptor subunits at thalamo-amygdaloid dendritic spines
Radley, J. J., Farb, C. R., He, Y., Janssen, W. G. M., Rodrigues, S. M., Johnson, L. R., Hof, P. R., LeDoux, J. E., & Morrison, J. H. (2007) · Brain Research · doi:10.1016/j.brainres.2006.11.045

Flagged first, then by citations

Research works printed but not linked: 1

Paxinos G, Watson C (1998). The rat brain in stereotaxic coordinates, spiral bound. Academic Press: New York.

Sorted by citations

Behavioral problems after early life stress: contributions of the hippocampus and amygdala
Hanson, J. L., Nacewicz, B. M., Sutterer, M. J., Cayo, A. A., Schaefer, S. M., Rudolph, K. D., Shirtcliff, E. A., Pollak, S. D., & Davidson, R. J. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.04.020 · Cited by 627 · see citing works
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
Amygdala FAAH and anandamide: mediating protection and recovery from stress
Gunduz-Cinar, O., Hill, M. N., McEwen, B. S., & Holmes, A. (2013) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2013.08.008 · Cited by 229 · see citing works
Stress increases GABAergic neurotransmission in CRF neurons of the central amygdala and bed nucleus stria terminalis
Partridge, J. G., Forcelli, P. A., Luo, R., Cashdan, J. M., Schulkin, J., Valentino, R. J., & Vicini, S. (2016) · Neuropharmacology · doi:10.1016/j.neuropharm.2016.03.029 · Cited by 81 · see citing works
Disruptive effects of repeated stress on basolateral amygdala neurons and fear behavior across the estrous cycle in rats
Blume, S. R., Padival, M., Urban, J. H., & Rosenkranz, J. A. (2019) · Scientific Reports · doi:10.1038/s41598-019-48683-3 · Cited by 71 · see citing works
Self-citation
Distinct Effects of Repeated Restraint Stress on Basolateral Amygdala Neuronal Membrane Properties in Resilient Adolescent and Adult Rats
Hetzel, A., & Rosenkranz, J. A. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.60 · Cited by 62 · see citing works
Self-citation
Chronic stress-induced dendritic reorganization and abundance of synaptosomal PKA-dependent CP-AMPA receptor in the basolateral amygdala in a mouse model of depression
Yi, E.-S., Oh, S., Lee, J.-K., & Leem, Y.-H. (2017) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2017.03.093 · Cited by 45 · see citing works

17β-Estradiol reduces excitatory postsynaptic potential (EPSP) amplitude in rat basolateral amygdala neurons
Womble, M. D., Andrew, J. A., & Crook, J. J. (2002) · Neuroscience Letters · doi:10.1016/s0304-3940(02)00871-6 · Cited by 44 · see citing works
Dysfunction of Ca2+/CaM kinase IIα cascades in the amygdala in post-traumatic stress disorder
Shi (2009) · International Journal of Molecular Medicine · doi:10.3892/ijmm_00000294 · Cited by 17 · see citing works
Fear, Anxiety, and the Amygdala
Sah, P. (2017) · Neuron · doi:10.1016/j.neuron.2017.09.013 · Cited by 137 · see citing works
Stress duration modulates the spatiotemporal patterns of spine formation in the basolateral amygdala
Mitra, R., Jadhav, S., McEwen, B. S., Vyas, A., & Chattarji, S. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504011102 · Cited by 663 · see citing works
Effects of lesions in different nuclei of the amygdala on conditioned taste aversion
Molero‐Chamizo, A., & Urbina, G. N. R. (2017) · Experimental Brain Research · doi:10.1007/s00221-017-5078-1 · Cited by 13 · see citing works

Authors: Padival, M., Quinette, D., & Rosenkranz, J. A.
Affiliations: Rosalind Franklin University of Medicine and Science (US)
Corresponding author: Rosenkranz, J Amiel
ORCID: Rosenkranz, J Amiel
Venue: Neuropsychopharmacology
Publisher: Springer Science and Business Media LLC
Published: 2013-03-27
Volume: 38
Issue: 9
Pages: 1748-1762
ISSN: 0893-133X (ISSN-L)
1740-634X
DOI: 10.1038/npp.2013.74
PMC: PMC3717551
OpenAlex: W2161838364
Cited by: 75
References: 120
Citations by year: 2026: 4 · 2025: 1 · 2024: 1 · 2023: 3 · 2022: 4 · 2021: 8 · 2020: 6 · 2019: 5 · 2018: 9 · 2017: 10 · 2016: 8 · 2015: 8 · 2014: 5 · 2013: 2 · 2012: 1
FWCI: 3.76
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: Brain Research Foundation
National Institutes of Health
National Institute of Mental Health (MH084970, R01MH084970)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords: chronic stress, basal amygdala, dendritic spines, restraint stress, amygdala hyperactivity, depression, anxiety, dendritic trees, Golgi staining
MeSH terms: Amygdala, Animals, Dendrites, Male, Neurons, Stress, Psychological, Excitatory Postsynaptic Potentials, Dendritic Spines, Rats

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Effects of repeated stress on excitatory drive of basal amygdala neurons in vivo

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