Lateral amygdaloid nucleus expansion in adult rats is associated with exposure to prenatal stress

Salm, A.K.; Pavelko, Michelle; Krouse, E.Marshall; Webster, Wendy; Kraszpulski, Michał; Birkle, Dale L.

doi:10.1016/j.devbrainres.2003.11.005

Cited by 125Stress Responses and CortisolMemory and Neural MechanismsMaternal Mental Health During Pregnancy and Postpartum

Lateral amygdaloid nucleus expansion in adult rats is associated with exposure to prenatal stress

Salm, A.K., Pavelko, Michelle, Krouse, E.Marshall, Webster, Wendy, Kraszpulski, Michał, Birkle, Dale L.·2004·Developmental Brain Research

DOI 10.1016/j.devbrainres.2003.11.005

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Abstract

Anxiety disorders in humans have been associated with chronic activation of the hypothalamic-pituitary-adrenal axis and changes in the volume of the amygdala. Interest in the etiology of anxiety disorders has led us and others to investigate the effects of prenatal stress on the brain development of adult male rat offspring. Prenatally stressed rats represent a promising animal model for anxiety disorders in that they have already been characterized as having both upregulated corticotropin-releasing factor (CRF) brain biochemistry and altered, more fearful, behaviors. Consistent with this, there is now evidence that prenatal stress also has an impact on the development of CRFergic neurons in the hypothalamic paraventricular nucleus and neurogenesis in the hippocampus. At this time, little information about the impact of prenatal stress on amygdala anatomy has been presented. Here we asked whether prenatal stress also has an impact on the development of the amygdala, because this structure plays a direct role in the emotions of anxiety and fear. Stereological measures of well-defined subregions of amydgdaloid nuclei revealed significantly expanded dimensions of the lateral nucleus in prenatally stressed offspring, due, in part, to more neurons and glia. These data may have direct import for the effect of adverse early life experiences and the etiology of anxiety disorders in humans. They also imply that early experiences may not be "grown out of" with development; in fact, the opposite might be true-adverse early life experiences may set developmental events into motion in the brain that last a lifetime.

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Prenatal stress is linked to enlarged lateral amygdala nucleus in offspring.
“For example significantly expanded dimensions of the lateral nucleus of the amygdala were observed in prenatally stressed offspring (Salm et al., 2004).”
From High pregnancy anxiety during mid-gestation is associated with decreased gray matter density in 6-9-year-old children. (2010) · cites this paper as Salm et al., 2004
The findings are consistent with animal evidence that medial temporal and prefrontal cortical regions are shaped by early experience.
“Our findings are consistent with accumulating evidence from animal studies that medial temporal and prefrontal cortical regions are shaped by early experience (e.g. Coe et al., 2003; Salm et al., 2004; Fujioka et al., 2006; Murmu et al., 2006).”
From High pregnancy anxiety during mid-gestation is associated with decreased gray matter density in 6-9-year-old children. (2010) · cites this paper as Salm et al., 2004

The rat brain in stereotaxic coordinates
Palkovits, M. (1983) · Neuropeptides · doi:10.1016/0143-4179(83)90049-5 · Cited by 28,959 · see citing works
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · see citing works
Emotion circuits in the brain
LeDoux, J. E. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.155 · Cited by 8,444 · see citing works
Functional neuroanatomy of emotion: A meta-analysis of emotion activation studies in PET and fMRI
Phan, K. L., Wager, T., Taylor, S. F., & Liberzon, I. (2002) · NeuroImage · doi:10.1006/nimg.2002.1087 · Cited by 3,502 · see citing works
Some new, simple and efficient stereological methods and their use in pathological research and diagnosis.
GUNDERSEN, H. J. G., BENDTSEN, T. F., KORBO, L., MARCUSSEN, N., MØLLER, A., NIELSEN, K., NYENGAARD, J. R., PAKKENBERG, B., SØRENSEN, F. B., VESTERBY, A., et al. (1988) · APMIS · doi:10.1111/j.1699-0463.1988.tb05320.x · Cited by 2,929 · see citing works
Subgenual prefrontal cortex abnormalities in mood disorders
Drevets, W. C., Price, J. L., Simpson, J. R., Todd, R. D., Reich, T., Vannier, M., & Raichle, M. E. (1997) · Nature · doi:10.1038/386824a0 · Cited by 2,693 · see citing works
The new stereological tools: Disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis
Gundersen, H. J. G., Bagger, P. V., Bendtsen, T. F., Evans, S. M., Korbo, L., Marcussen, N., Møller, A., Nielsen, K. N., Nyengaard, J. R., Pakkenberg, B., et al. (1988) · Apmis · doi:10.1111/j.1699-0463.1988.tb00954.x · Cited by 2,480 · see citing works
Pituitary-adrenal and autonomic responses to stress in women after sexual and physical abuse in childhood
Heim, C. (2000) · JAMA · doi:10.1001/jama.284.5.592 · Cited by 1,968 · see citing works
Response and Habituation of the Human Amygdala during Visual Processing of Facial Expression
Breiter, H. C., Etcoff, N. L., Whalen, P. J., Kennedy, W. A., Rauch, S. L., Buckner, R. L., Strauss, M. M., Hyman, S. E., & Rosen, B. R. (1996) · Neuron · doi:10.1016/s0896-6273(00)80219-6 · Cited by 1,711 · 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
The amygdala: Neurobiological aspects of emotion, memory, and mental dysfunction.
Aggleton, J. P. (1992) · Wiley-Liss eBooks · Cited by 1,536 · see citing works
Glial reduction in the subgenual prefrontal cortex in mood disorders
Öngür, D., Drevets, W. C., & Price, J. L. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.22.13290 · Cited by 1,525 · see citing works
What is the amygdala?
Swanson, L. W., & Petrovich, G. D. (1998) · Trends in Neurosciences · doi:10.1016/s0166-2236(98)01265-x · Cited by 1,351 · see citing works
Fear conditioning induces associative long-term potentiation in the amygdala
Rogan, M. T., Stäubli, U. V., & LeDoux, J. E. (1997) · Nature · doi:10.1038/37601 · Cited by 1,310 · see citing works
Cortical pathways to the mammalian amygdala
McDonald, A. J. (1998) · Progress in Neurobiology · doi:10.1016/s0301-0082(98)00003-3 · Cited by 1,303 · see citing works
The amygdala: Neurobiological aspects of emotion, memory and mental dysfunction
Scheel-Krüger, J. (1993) · Journal of Chemical Neuroanatomy · doi:10.1016/0891-0618(93)90037-5 · Cited by 1,277 · see citing works
Fear and the human amygdala
Adolphs, R., Tranel, D., Damasio, H., & Damasio, A. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-09-05879.1995 · Cited by 1,138 · see citing works
Exaggerated amygdala response to masked facial stimuli in posttraumatic stress disorder: A functional MRI study
Rauch, S. L., Whalen, P. J., Shin, L. M., McInerney, S. C., Macklin, M. L., Lasko, N. B., Orr, S. P., & Pitman, R. K. (2000) · Biological Psychiatry · doi:10.1016/s0006-3223(00)00828-3 · Cited by 1,111 · see citing works
A Symptom Provocation Study of Posttraumatic Stress Disorder Using Positron Emission Tomography and Script-Driven Imagery
Rauch, S. L. (1996) · Archives of General Psychiatry · doi:10.1001/archpsyc.1996.01830050014003 · Cited by 1,056 · see citing works
Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus
Lemaire, V., Koehl, M., Le Moal, M., & Abrous, D. N. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.20.11032 · Cited by 1,044 · see citing works
Organization of intra-amygdaloid circuitries in the rat: an emerging framework for understanding functions of the amygdala
Pitkänen, A., Savander, V., & LeDoux, J. E. (1997) · Trends in Neurosciences · doi:10.1016/s0166-2236(97)01125-9 · Cited by 980 · see citing works
Reciprocal Connections between the Amygdala and the Hippocampal Formation, Perirhinal Cortex, and Postrhinal Cortex in Rat: A Review
Pitkänen, A., Pikkarainen, M., Nurminen, N., & Ylinen, A. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb06738.x · Cited by 962 · see citing works
Alterations induced by gestational stress in brain morphology and behaviour of the offspring
Weinstock, M. (2001) · Progress in Neurobiology · doi:10.1016/s0301-0082(01)00018-1 · Cited by 791 · see citing works
Fear conditioning induces a lasting potentiation of synaptic currents in vitro
McKernan, M. G., & Shinnick-Gallagher, P. (1997) · Nature · doi:10.1038/37605 · Cited by 771 · see citing works
Chemical and Anatomical Plasticity of Brain
Bennett, E. L., Diamond, M. C., Krech, D., & Rosenzweig, M. R. (1964) · Science · doi:10.1126/science.146.3644.610 · Cited by 767 · see citing works
Regional cerebral blood flow during script-driven imagery in childhood sexual abuse-related PTSD: A PET investigation
Shin, L. M., McNally, R. J., Kosslyn, S. M., Thompson, W. L., Rauch, S. L., Alpert, N. M., Metzger, L. J., Lasko, N. B., Orr, S. P., & Pitman, R. K. (1999) · American Journal of Psychiatry · doi:10.1176/ajp.156.4.575 · Cited by 647 · see citing works
Untitled work
(1992) · Cited by 626 · see citing works
Control of Glutamate Clearance and Synaptic Efficacy by Glial Coverage of Neurons
Oliet, S. H. R., Piet, R., & Poulain, D. A. (2001) · Science · doi:10.1126/science.1059162 · Cited by 623 · see citing works
Synaptic plasticity in the basolateral amygdala induced by hippocampal formation stimulation in vivo
Maren, S., & Fanselow (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-11-07548.1995 · Cited by 499 · see citing works
Convergent neuroanatomical and behavioural evidence of an amygdala hypothesis of autism
Howard, M. A., Cowell, P. E., Boucher, J., Broks, P., Mayes, A. R., Farrant, A., & Roberts, N. P. (2000) · Neuroreport · doi:10.1097/00001756-200009110-00020 · Cited by 479 · see citing works
Newly generated neurons in the amygdala and adjoining cortex of adult primates
Bernier, P. J., Bédard, A., Vinet, J., Lévesque, M., & Parent, A. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.172403999 · Cited by 478 · see citing works
Amygdala core nuclei volumes are decreased in recurrent major depression
Sheline, Y. I., Gado, M. H., & Price, J. L. (1998) · NeuroReport · doi:10.1097/00001756-199806220-00021 · Cited by 472 · 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
Thalamoamygdaloid projections in the rat: A test of the amygdala's role in sensory processing
Turner, B. H., & Herkenham, M. (1991) · The Journal of comparative neurology · doi:10.1002/cne.903130208 · Cited by 437 · see citing works
Chronicity, relapse, and illness—course of panic disorder, social phobia, and generalized anxiety disorder: Findings in men and women from 8 years of follow‐up
Yonkers, K., Bruce, S., Dyck, I. R., & Keller, M. B. (2003) · Depression and Anxiety · doi:10.1002/da.10106 · Cited by 400 · see citing works
Prenatal Loss of Father and Psychiatric Disorders
HUTTUNEN, M. O. (1978) · Archives of General Psychiatry · doi:10.1001/archpsyc.1978.01770280039004 · Cited by 372 · see citing works
Neuroimaging findings in post-traumatic stress disorder
Hull, A. M. (2002) · The British Journal of Psychiatry · doi:10.1017/s000712500016180x · Cited by 343 · see citing works
A pilot study of amygdala volumes in pediatric generalized anxiety disorder
De Bellis, M. D., Casey, B. J., Dahl, R. E., Birmaher, B., Williamson, D. E., Thomas, K. M., Axelson, D. A., Frustaci, K., Boring, A. M., Hall, J., et al. (2000) · Biological Psychiatry · doi:10.1016/s0006-3223(00)00835-0 · Cited by 322 · cited 2× · see citing works
“In addition, structural MRI studies have also found increased amygdala volumes associated with anxiety disorders [ 17 ].”
Background
Cognitive-Behavior Therapy by Any Other Name Still Smells as Sweet
Menzies, R. G. (1998) · Archives of General Psychiatry · doi:10.1001/archpsyc.55.7.663 · Cited by 318 · see citing works
Enlargement of the Amygdala in Patients with a First Episode of Major Depression
Frodl, T., Meisenzahl, E., Zetzsche, T., Bottlender, R., Born, C., Groll, C., Jäger, M., Leinsinger, G., Hahn, K., & Möller, H.-J. (2002) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01359-2 · Cited by 316 · see citing works
Insulin-like growth factor-I and neurogenesis in the adult mammalian brain
Anderson, M. F., Åberg, M. A. I., Nilsson, M., & Eriksson, P. S. (2002) · Developmental Brain Research · doi:10.1016/s0165-3806(02)00277-8 · Cited by 314 · see citing works
Neuroimaging findings in post-traumatic stress disorder. Systematic review.
Hull, A. M. (2002) · PubMed · Cited by 307 · see citing works
Maternal Care, Gene Expression, and the Development of Individual Differences in Stress Reactivity
Francis, D. D., Champagne, F. A., Liu, D., & Meaney, M. J. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb08106.x · Cited by 291 · see citing works
Prenatal stress increase anxiety related behavior and alters cerebral lateralization of dopamine activity
Fride, E., & Weinstock, M. (1988) · Life Sciences · doi:10.1016/0024-3205(88)90561-9 · Cited by 255 · see citing works
Prenatal stress in rats: effects on plasma corticosterone, hippocampal glucocorticoid receptors, and maze performance
Szuran, T. F., Pliška, V., Pokorny, J., & Welzl, H. (2000) · Physiology & Behavior · doi:10.1016/s0031-9384(00)00351-6 · Cited by 253 · see citing works
Long‐term effects of prenatal stress on HPA axis activity in juvenile rhesus monkeys
Clarke, A. S., Wittwer, D. J., Abbott, D. H., & Schneider, M. L. (1994) · Developmental Psychobiology · doi:10.1002/dev.420270502 · Cited by 245 · see citing works
Investigating the pathogenesis of posttraumatic stress disorder with neuroimaging.
Pitman, R. K., Shin, L. M., & Rauch, S. L. (2001) · PubMed · Cited by 230 · see citing works
Follow‐up Study from Birth of the Effects of Prenatal Stresses
Stott, D. H. (1973) · Developmental Medicine & Child Neurology · doi:10.1111/j.1469-8749.1973.tb04912.x · Cited by 223 · see citing works
Voltage-dependent calcium and potassium channels in retinal glial cells
Newman, E. A. (1985) · Nature · doi:10.1038/317809a0 · Cited by 219 · see citing works
The effects of social environment on adult neurogenesis in the female prairie vole
Fowler, C. D., Liu, Y., Ouimet, C. C., & Wang, Z. (2002) · Journal of Neurobiology · doi:10.1002/neu.10042 · Cited by 207 · see citing works
Prenatal stress increases corticotropin-releasing factor (CRF) content and release in rat amygdala minces
Cratty, M. S., Ward, H. E., Johnson, E. A., Azzaro, A. J., & Birkle, D. L. (1995) · Brain Research · doi:10.1016/0006-8993(95)00087-7 · Cited by 201 · see citing works
Self-citation
Effects of prenatal stress on defensive withdrawal behavior and corticotropin releasing factor systems in rat brain
Ward, H. E. (2000) · Physiology & Behavior · doi:10.1016/s0031-9384(00)00270-5 · Cited by 196 · see citing works
Neuroimaging studies in post-traumatic stress disorder
Bremner, J. D. (2002) · Current Psychiatry Reports · doi:10.1007/s11920-996-0044-9 · Cited by 194 · see citing works
Right amygdala volume in adolescent and young adult offspring from families at high risk for developing alcoholism
Hill, S. Y., Bellis, M. D. D., Keshavan, M. S., Lowers, L., Shen, S., Hall, J., & Pitts, T. (2001) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01088-5 · Cited by 190 · see citing works
Prenatal stress has long‐term effects on behavioral responses to stress in juvenile rhesus monkeys
Clarke, A. S., & Schneider, M. L. (1993) · Developmental Psychobiology · doi:10.1002/dev.420260506 · Cited by 187 · see citing works
Prenatal stress effects on functional development of the offspring
Weinstock, M., Fride, E., & Hertzberg, R. (1988) · Progress in brain research · doi:10.1016/s0079-6123(08)60513-0 · Cited by 173 · see citing works
Child psychiatric sequelae of maternal war stress
Meijer, A. (1985) · Acta Psychiatrica Scandinavica · doi:10.1111/j.1600-0447.1985.tb02647.x · Cited by 168 · see citing works
Quantitative 3 H‐thymidine radiographic analyses of neurogenesis on the rat amygdala
Bayer, S. A. (1980) · The Journal of Comparative Neurology · doi:10.1002/cne.901940409 · Cited by 159 · see citing works
Plasticity of GFAP-immunoreactive astrocyte size and number in visual cortex of rats reared in complex environments
Sirevaag, A. M., & Greenough, W. T. (1991) · Brain Research · doi:10.1016/0006-8993(91)90517-y · Cited by 149 · see citing works
The basolateral amygdaloid complex as a cortical-like structure
Carlsen, J., & Heimer, L. (1988) · Brain Research · doi:10.1016/0006-8993(88)91418-7 · Cited by 149 · see citing works
Decreased left amygdala and hippocampal volumes in young offspring at risk for schizophrenia
Keshavan, M. S., DICK, E., Mankowski, I., Harenski, K. A., Montrose, D. M., Diwadkar, V. A., & DeBellis, M. D. (2002) · Schizophrenia Research · doi:10.1016/s0920-9964(01)00404-2 · Cited by 137 · see citing works
The prenatal stress syndrome: Current status
Ward, I. L. (1984) · Psychoneuroendocrinology · doi:10.1016/0306-4530(84)90016-7 · Cited by 136 · see citing works
Depression: reduced number of granule cells in the hippocampus of female, but not male, rats due to prenatal restraint stress
Schmitz, C., Rhodes, M. E., Bludau, M., Kaplan, S., Ong, P., Ueffing, I., Vehoff, J., Korr, H., & Frye, C. A. (2002) · Molecular Psychiatry · doi:10.1038/sj.mp.4001118 · Cited by 136 · see citing works
The effects of prenatal stress on the development of hypothalamic paraventricular neurons in fetal rats
Fujioka, T., Sakata, Y., Yamaguchi, K., Shibasaki, T., Kato, H., & Nakamura, S. (1999) · Neuroscience · doi:10.1016/s0306-4522(99)00073-1 · Cited by 134 · see citing works
Effects of prenatal stress on maternal behavior in the rat
Patin, V., Lordi, B., Vincent, A., Thoumas, J., Vaudry, H., & Caston, J. (2002) · Developmental Brain Research · doi:10.1016/s0165-3806(02)00491-1 · Cited by 133 · see citing works
Anxiety and increased 5-HT1A receptor response in NCAM null mutant mice
Stork, O., Welzl, H., Wotjak, C. T., Hoyer, D., Delling, M., Cremer, H., & Schachner, M. (1999) · Journal of Neurobiology · doi:10.1002/(sici)1097-4695(19990905)40:3 · Cited by 127 · see citing works
Forebrain and midbrain
Paxinos, G. (1985) · Academic Press eBooks · Cited by 110 · see citing works
Immunoreactive glial fibrillary acidic protein in pituicytes of the rat neurohypophysis
Salm, A. K., Hatton, G. I., & Nilaver, G. (1982) · Brain Research · doi:10.1016/0006-8993(82)90729-6 · Cited by 108 · see citing works
Self-citation
Estradiol (E2) enhances neurite outgrowth by repressing glial fibrillary acidic protein expression and reorganizing laminin.
Rozovsky, I., Wei, M., Stone, D., Zanjani, H., Anderson, C. P., Morgan, T. E., & Finch, C. E. (2002) · Endocrinology · doi:10.1210/endo.143.2.8615 · Cited by 98 · see citing works
Neighborly interactions of metabolically-activated astrocytes in vivo
Dienel, G. A., & Cruz, N. F. (2003) · Neurochemistry International · doi:10.1016/s0197-0186(03)00021-4 · Cited by 90 · see citing works
Anatomic heterogeneity of the rat amygdaloid complex.
Pitkänen, A., Jolkkonen, E., & Kemppainen, S. (2000) · PubMed · Cited by 85 · see citing works
Neuronal changes in the basolateral complex during development of the amygdala of the rat
Berdel, B., Moryś, J., & Maciejewska, B. (1997) · International Journal of Developmental Neuroscience · doi:10.1016/s0736-5748(97)00022-1 · Cited by 68 · see citing works
Prenatal stress and emotional response of adult offspring
Suchecki, D., & Neto, J. P. (1991) · Physiology & Behavior · doi:10.1016/0031-9384(91)90259-q · Cited by 59 · see citing works
Effects of pre‐ and postnatal corticosterone exposure on the rat hippocampal GABA system
Stone, D. J., Walsh, J. P., Sebro, R., Stevens, R. J. N., Pantazopolous, H., & Benes, F. M. (2001) · Hippocampus · doi:10.1002/hipo.1066 · Cited by 55 · see citing works
Prenatal Stress Alters Reproductive Responses of Rats in Behavioral Estrus and Paced Mating of Hormone-Primed Rats
Frye, C. A., & Orecki, Z. A. (2002) · Hormones and Behavior · doi:10.1006/hbeh.2002.1834 · Cited by 43 · see citing works
Sexually dimorphic areas in the rat medial amygdala: resistance to the demasculinizing effect of prenatal stress
Kerchner, M., Malsbury, C. W., Ward, O. B., & Ward, I. L. (1995) · Brain Research · doi:10.1016/0006-8993(94)01378-u · Cited by 36 · see citing works
Prenatal Stress Alters the Size of the Rostral Anterior Commissure in Rats
Jones, H. E., Ruscio, M., Keyser, L. A., Gonzalez, C., Billack, B., Rowe, R., Hancock, C., Lambert, K. G., & Kinsley, C. H. (1997) · Brain Research Bulletin · doi:10.1016/s0361-9230(96)00293-6 · Cited by 30 · see citing works
The increasingly plastic, hormone-responsive adult brain
Breedlove, S. M., & Jordan, C. L. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.071054098 · Cited by 24 · see citing works
Dehydration‐induced proliferation of identified pituicytes in fully adult rats
Murugaiyan, P., & Salm, A. K. (1995) · Glia · doi:10.1002/glia.440150108 · Cited by 21 · see citing works
Self-citation
Volume and topographical changes of the basolateral complex during the development of the rat's amygdaloid body.
Berdel, B., Moryś, J., Maciejewska, B., & Dziewíatkowski, J. (1997) · PubMed · Cited by 13 · see citing works
Structural plasticity of nonneuronal cells in the hypothalamo-neurohypophyseal system: in the right place at the right time
Salm, A. K., Ayoub, A. E., & Lally, B. E. (2003) · Advances in molecular and cell biology · doi:10.1016/s1569-2558(03)31008-2 · Cited by 4 · see citing works
Self-citation

Flagged first, then by citations

1 of the 83 references couldn’t be matched to a known paper.

Sorted by citations

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
The long-term behavioural consequences of prenatal stress
Weinstock, M. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.03.002 · Cited by 1,045 · see citing works
The potential influence of maternal stress hormones on development and mental health of the offspring
Weinstock, M. (2005) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2004.09.006 · Cited by 706 · see citing works
Maternal cortisol over the course of pregnancy and subsequent child amygdala and hippocampus volumes and affective problems
Buss, C., Davis, E. P., Shahbaba, B., Pruessner, J. C., Head, K., & Sandman, C. A. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1201295109 · Cited by 652 · see citing works
“Thus, excess levels of glucocorticoid exposure during this developmental period may have stable and permanent consequences by decreasing cell proliferation and neuronal differentiation and increasing gliogenesis (70), which, in turn, may account for the larger amygdala volumes observed in the context of excess prenata…”
Background
Modulation of the Hypothalamic-Pituitary-Adrenal Axis by Early Life Stress Exposure
van Bodegom, M., Homberg, J. R., & Henckens, M. J. A. G. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00087 · Cited by 562 · see citing works
Prenatal stress and brain development
Charil, A., Laplante, D. P., Vaillancourt, C., & King, S. (2010) · Brain Research Reviews · doi:10.1016/j.brainresrev.2010.06.002 · Cited by 554 · see citing works
High pregnancy anxiety during mid-gestation is associated with decreased gray matter density in 6-9-year-old children.
Buss, C., Davis, E. P., Muftuler, L. T., Head, K., & Sandman, C. A. (2010) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.07.010 · Cited by 435 · see citing works
“Our findings are consistent with accumulating evidence from animal studies that medial temporal and prefrontal cortical regions are shaped by early experience (e.g. Coe et al., 2003; Salm et al., 2004; Fujioka et al., 2006; Murmu et al., 2006).”
Fetal origins of mental health: Evidence and mechanisms
Schlotz, W., & Phillips, D. I. W. (2009) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2009.02.001 · Cited by 401 · see citing works
Timing of Prenatal Stressors and Autism
Beversdorf, D. Q., Manning, S. E., Hillier, A. J., Anderson, S. L., Nordgren, R. E., Walters, S., Nagaraja, H. N., Cooley, W. C., Gaelic, S. E., & Bauman, M. L. (2005) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-005-5037-8 · Cited by 359 · see citing works
“Maternal stress in animals also results in changes in the hypothalamic–pituitary–adrenal axis (HPA) and changes in the amygdala, including expansion of the lateral nucleus, that last into adulthood in the offspring (Ward, et al, 2000; Salm et al., 2004).”
Background
Gender Differences in the Effects of Prenatal Stress on Brain Development and Behaviour
Weinstock, M. (2007) · Neurochemical Research · doi:10.1007/s11064-007-9339-4 · Cited by 349 · see citing works
“The lateral nucleus of the amygdala was larger [98] in adult PS than in control male rats and had more neurons expressing neuronal nitric oxide synthase immunoreactivity [99].”
Background
Adult microbiota‐deficient mice have distinct dendritic morphological changes: differential effects in the amygdala and hippocampus
Luczynski, P., Whelan, S. O., O'SULLIVAN, C. T. D., Clarke, G. A., Shanahan, F., Dinan, T. G., & Cryan, J. F. (2016) · European Journal of Neuroscience · doi:10.1111/ejn.13291 · Cited by 345 · see citing works
“Prenatally stressed rats have increased LA volume (Salm et al., 2004) and both chronic stress and corticosterone treatment induce hippocampal atrophy (Isgor et al., 2004; Murray et al., 2008; Lee et al., 2009).”
Background
Prenatal maternal depression alters amygdala functional connectivity in 6-month-old infants
Qiu, A., Anh, T. T., Li, Y., Chen, H., Rifkin-Graboi, A., Broekman, B. F. P., Kwek, K., Saw, S.-M., Chong, Y.-S., Gluckman, P. D., et al. (2015) · Translational Psychiatry · doi:10.1038/tp.2015.3 · Cited by 282 · see citing works
Changes of spine density and dendritic complexity in the prefrontal cortex in offspring of mothers exposed to stress during pregnancy
Murmu, M. S., Salomon, S., Biala, Y., Weinstock, M., Braun, K., & Bock, J. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05024.x · Cited by 278 · see citing works
“Prenatal stress also reduced cortical N-acetylaspartic acid levels indicating neuronal damage or cell loss (Poland et al., 1999) and the density of hippocampal synapses (Hayashi et al., 1998), while causing expansion of the lateral nucleus of the amygdala (Salm et al., 2004).”
Background
Prenatal psychobiological predictors of anxiety risk in preadolescent children
Davis, E. P., & Sandman, C. A. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2011.12.016 · Cited by 254 · see citing works
“Further, exposure to stress during the prenatal period is associated with an increase in amygdala volume (Salm et al., 2004) suggesting a plausible mechanism by which prenatal cortisol may influence vulnerability to the development of anxiety.”
Reduced Amygdalar Gray Matter Volume in Familial Pediatric Bipolar Disorder
Chang, K., Karchemskiy, A., Barnea‐Goraly, N., Garrett, A. S., Simeonova, D. I., & Reiss, A. L. (2005) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/01.chi.0000159948.75136.0d · Cited by 253 · see citing works
“Rats exposed to prenatal stress showed increased volume of the lateral amygdaloid nucleus compared with controls (Salm et al., 2004).”
Method
Maternal Cortisol Concentrations During Pregnancy and Sex-Specific Associations With Neonatal Amygdala Connectivity and Emerging Internalizing Behaviors
Graham, A. M., Rasmussen, J. M., Entringer, S., Ben Ward, E., Rudolph, M. D., Gilmore, J. H., Styner, M., Wadhwa, P. D., Fair, D. A., & Buss, C. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.06.023 · Cited by 203 · see citing works
“Animal models provide experimental evidence for effects of heightened maternal GCs during pregnancy on amygdala development(32, 33), and associated elevations in stress reactivity and anxiety-like behaviors in offspring(32, 34–36).”
Background
Remodeling of axo-spinous synapses in the pathophysiology and treatment of depression
Licznerski, P., & Duman, R. S. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2012.09.057 · Cited by 157 · see citing works
“PNS exposure of rats leads to an enlarged amygdala volume in adulthood (Salm et al., 2004) and may also cause dysregulation in BDNF in adult rats that could contribute to alterations of dendrite and spine morphology (discussed above in a separate paragraph) (Fumagalli et al.”
Human milk cortisol is associated with infant temperament
Grey, K. R., Davis, E. P., Sandman, C. A., & Glynn, L. M. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.11.002 · Cited by 145 · see citing works
“The amygdala is the primary brain structure responsible for the experience of emotion (McDonald, 1998; LeDoux, 2000) and GC exposures early in life result in alterations in the developmental trajectory of the structure of the amygdala (Salm et al., 2004; Kraszpulski et al., 2006).”
Background
Learning by embryos and the ghost of predation future
Mathis, A., Ferrari, M. C. O., Windel, N. L., Messier, F., & Chivers, D. P. (2008) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2008.0754 · Cited by 136 · see citing works
Frontolimbic structural changes in borderline personality disorder
Minzenberg, M., Fan, J., New, A. S., Tang, C. Y., & Siever, L. J. (2007) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2007.07.015 · Cited by 127 · see citing works
“Increased neuronal density in the lateral nucleus of the amygdala is found in adult rats subject to prenatal stress (Salm et al., 2004), and enhanced amygdala neurogenesis may be found in adult rats subject to either social stressors (Fowler et al., 2002) or bilateral olfactory bulbectomy (an…”
BackgroundResultInfluential
Enhanced De Novo Neurogenesis and Dopaminergic Neurogenesis in the Substantia Nigra of 1‐Methyl‐4‐phyenyl‐1,2,3,6‐Tetrahydropyridine‐Induced Parkinson's Disease‐Like Mice
Shan, X., Chi, L., Bishop, M., Luo, C., Lien, L., Zhang, Z., & Liu, R. (2006) · Stem Cells · doi:10.1634/stemcells.2005-0487 · Cited by 132 · see citing works
Prenatal stress produces more behavioral alterations than maternal separation in the elevated plus-maze and in the elevated T-maze
Estanislau, C. R., & Morato, S. (2005) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.04.003 · Cited by 132 · see citing works
Prespawning stress in farmed Atlantic salmon Salmo salar : maternal cortisol exposure and hyperthermia during embryonic development affect offspring survival, growth and incidence of malformations
Eriksen, M. S., Bakken, M., Espmark, Å. M. O., Braastad, B. O., & Salte, R. (2006) · Journal of Fish Biology · doi:10.1111/j.1095-8649.2006.01071.x · Cited by 128 · see citing works
Prenatal Immune and Endocrine Modulators of Offspring's Brain Development and Cognitive Functions Later in Life
Schepanski, S. N., Buß, C., Hanganu‐Opatz, I. L., & Arck, P. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02186 · Cited by 129 · see citing works
“an increased microglia density after prenatal cytokine and glucocorticoid exposure has been detected in the lateral nucleus (LN) (120, 121).”
Background
Effect of varied gestational stress on acquisition of spatial memory, hippocampal LTP and synaptic proteins in juvenile male rats
Yaka, R., Salomon, S., Matzner, H., & Weinstock, M. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.01.018 · Cited by 120 · see citing works
Chronic traffic noise stress accelerates brain impairment and cognitive decline in mice
Jafari, Z., Kolb, B. E., & Mohajerani, M. H. (2018) · Experimental Neurology · doi:10.1016/j.expneurol.2018.06.011 · Cited by 113 · see citing works
“A study on rats with a mild prenatal stress revealed significantly expanded dimensions of the lateral nucleus compared with the controls resulting from more neurons and glia (Salm et al., 2004).”
The development of antisocial behavior: What can we learn from functional neuroimaging studies?
Crowe, S. L., & Blair, J. (2008) · Development and Psychopathology · doi:10.1017/s0954579408000540 · Cited by 109 · see citing works
“Furthermore, this system is regulated by higher order structures such as the orbital, medial, and inferior frontal cortices (Blair, 2004a).”
Background
Astrocyte–neuron vulnerability to prenatal stress in the adult rat brain
Barros, V. G., Vega, M. D., Caltana, L. R., Brusco, A., & Antonelli, M. C. (2006) · Journal of Neuroscience Research · doi:10.1002/jnr.20758 · Cited by 103 · see citing works
“Gross morphological changes were reported as a 30% expansion of the lateral amygdaloid nucleus following exposure to prenatal stress (Salm et al., 2004).”
Background
Larger Amygdala Volume Mediates the Association Between Prenatal Maternal Stress and Higher Levels of Externalizing Behaviors: Sex Specific Effects in Project Ice Storm
Jones, S. L., Dufoix, R., Laplante, D. P., Elgbeili, G., Patel, R., Chakravarty, M. M., King, S., & Pruessner, J. C. (2019) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2019.00144 · Cited by 92 · see citing works
Air pollution exposure during pregnancy and childhood and brain morphology in preadolescents
Lubczynska, M. J., Muetzel, R. L., Marroun, H. E., Hoek, G., Kooter, I. M., Thomson, E. M., Hillegers, M. H. J., Vernooij, M. W., White, T. J. H., Tiemeier, H. W., et al. (2020) · Environmental Research · doi:10.1016/j.envres.2020.110446 · Cited by 100 · see citing works
Amygdala volume and depressive symptoms in patients with borderline personality disorder.
Zetzsche, T., Frodl, T., Preuss, U., Schmitt, G., Seifert, D., Leinsinger, G., Born, C., Reiser, M., Möller, H., & Meisenzahl, E. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.11.020 · Cited by 104 · see citing works
Neurobehavioral risk is associated with gestational exposure to stress hormones
Sandman, C. A., & Davis, E. P. (2012) · Expert Review of Endocrinology & Metabolism · doi:10.1586/eem.12.33 · Cited by 90 · see citing works
Impact of Prenatal Stress on Neuroendocrine Programming
Viltart, O., & Vanbesien-Mailliot, C. (2007) · The Scientific World JOURNAL · doi:10.1100/tsw.2007.204 · Cited by 86 · see citing works
“In particular, PS increases the number of neurons and glia in the lateral amygdaloid nucleus[283].”
Background
Prenatal stress affects the developmental trajectory of the rat amygdala
Kraszpulski, M., Dickerson, P. A., & Salm, A. K. (2006) · Stress · doi:10.1080/10253890600798109 · Cited by 85 · see citing works
“Previously we showed a significant expansion in the girth of the La and no changes in the cell numbers or dimensions of the Ce and BL for P80–P120 PS rats (Salm et al. 2004).”
BackgroundMethodResultInfluentialSelf-citation
Maternal Pregnancy-Related Anxiety Is Associated With Sexually Dimorphic Alterations in Amygdala Volume in 4-Year-Old Children
Acosta, H., Tuulari, J. J., Scheinin, N. M., Hashempour, N., Rajasilta, O., Lavonius, T. I., Pelto, J., Saunavaara, V., Parkkola, R., Lähdesmäki, T., et al. (2019) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2019.00175 · Cited by 80 · see citing works
Anxiety induced by prenatal stress is associated with suppression of hippocampal genes involved in synaptic function
Bogoch, Y., Biala, Y. N., Linial, M., & Weinstock, M. (2007) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2006.04402.x · Cited by 74 · see citing works
“A chronic anxiety state in association with excessive fear of novelty has been linked to alterations in the size of the lateral amygdaloid nucleus in humans (De Bellis et al. 2000) and prenatally stressed (PS) rats ( Salm et al. 2004 ) and also in the size of the synaptic area of the mossy fibres in the dentate gyrus…”
Background
Maternal Prenatal Stress Is Associated With Altered Uncinate Fasciculus Microstructure in Premature Neonates
Lautarescu, A., Pecheva, D., Nosarti, C., Sigurðardottir, J. N., Zhang, H. G., Victor, S., Craig, M., Edwards, A. D., & Counsell, S. J. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2019.08.010 · Cited by 72 · see citing works
“Prenatal stress exposure has been linked to abnormal neurodevelopment of a number of brain regions including the limbic system and prefrontal cortex, in both animal (Uno et al. 1994; Salm et al. 2004; Kraszpulski et al. 2006; Tamura et al. 2011) and human studies (e.”
Background
Behavior ontogeny in the elevated plus‐maze: prenatal stress effects
Estanislau, C. R., & Morato, S. (2006) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2006.03.001 · Cited by 72 · see citing works
“Indeed, it has been associated with some characteristics of generalized anxiety (De Bellis et al., 2000; Salm et al., 2004; Estanislau and Morato, 2005), depression (Morley-Fletcher et al., 2003; Smith et al., 2004) and schizophrenia (Weinstock, 2001; McClure et al., 2004).”
Background
SK2 potassium channel overexpression in basolateral amygdala reduces anxiety, stress-induced corticosterone secretion and dendritic arborization
Mitra, R., Ferguson, D., & Sapolsky, R. M. (2009) · Molecular Psychiatry · doi:10.1038/mp.2009.9 · Cited by 70 · see citing works
“Stress and stress hormones also change structure and function of the BLA, resulting in hypertrophy and increased excitability (11-15).”
Prenatal stress and limbic-prefrontal white matter microstructure in children aged 6–9 years: a preliminary diffusion tensor imaging study
Sarkar, S., Craig, M. C., Dell’Acqua, F., O’Connor, T. G., Catani, M., Deeley, Q., Glover, V., & Murphy, D. G. M. (2014) · The World Journal of Biological Psychiatry · doi:10.3109/15622975.2014.903336 · Cited by 70 · see citing works
“In particular, compared to controls, animals exposed to prenatal stress exhibited initially reduced, and subsequently increased, amygdala volume (Salm et al. 2004; Kraszpulski et al. 2006).”
Background
Neurodevelopmental consequences of maternal distress: what do we really know?
Schuurmans, C., & Kurrasch, D. M. (2012) · Clinical Genetics · doi:10.1111/cge.12049 · Cited by 68 · see citing works
“Interestingly, by P80 this decrease in cell numbers has reversed, suggesting that the effects of prenatal stress may be overcome later in life (103).”
Background
Effect of early maternal separation stress on attention, spatial learning and social interaction behaviour
Kambali, M., Anshu, K., Kutty, B. M., Muddashetty, R. S., & Laxmi, T. R. (2019) · Experimental Brain Research · doi:10.1007/s00221-019-05567-2 · Cited by 65 · see citing works
Prospective association of maternal psychosocial stress in pregnancy with newborn hippocampal volume and implications for infant social-emotional development
Moog, N. K., Nolvi, S., Kleih, T. S., Styner, M. A., Gilmore, J. H., Rasmussen, J. M., Heim, C. C., Entringer, S., Wadhwa, P. D., & Buß, C. (2021) · Neurobiology of Stress · doi:10.1016/j.ynstr.2021.100368 · Cited by 63 · see citing works
The transgenerational transmission of childhood adversity: behavioral, cellular, and epigenetic correlates
Gröger, N., Matas, E., Gos, T., Lesse, A., Poeggel, G., Braun, K., & Bock, J. (2016) · Journal of Neural Transmission · doi:10.1007/s00702-016-1570-1 · Cited by 61 · see citing works
“Disturbances of cell proliferation resulting in altered area volumes have also been reported for the amygdala in PS offspring (Kawamura et al. 2006; Kraszpulski et al. 2006; Salm et al. 2004).”
Background
Prenatal Stress Down-Regulates Reelin Expression by Methylation of Its Promoter and Induces Adult Behavioral Impairments in Rats
Palacios-García, I., Lara-Vásquez, A., Montiel, J. F., Díaz‐Véliz, G., Sepúlveda, H., Utreras, E., Montecino, M. A., González-Billault, C. E., & Aboitiz, F. (2015) · PLoS ONE · doi:10.1371/journal.pone.0117680 · Cited by 60 · see citing works
“This deficit is likely due to plasticity changes in the amygdala-prefrontal cortex circuit, which have been previously documented in stressed animals [92, 93].”
Background
The Effects of Early Life Stress on the Brain and Behaviour: Insights From Zebrafish Models
Eachus, H., Choi, M., & Ryu, S. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.657591 · Cited by 52 · see citing works
Effects of prenatal maternal stress by repeated cold environment on behavioral and emotional development in the rat offspring
Tazumi, T., Hori, E., Uwano, T., Umeno, K., Tanebe, K., Tabuchi, E., Ono, T., & Nishijo, H. (2005) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.03.006 · Cited by 55 · see citing works
Prenatal stress may increase vulnerability to life events: Comparison with the effects of prenatal dexamethasone
Hougaard, K. S., Andersen, M. B., Kjær, S. L., Hansen, Å. M., Werge, T. M., & Lund, S. P. (2005) · Developmental Brain Research · doi:10.1016/j.devbrainres.2005.06.014 · Cited by 55 · see citing works
Inflammation-Related Disorders in the Tryptophan Catabolite Pathway in Depression and Somatization
Anderson, G., Maes, M. H. J., & Berk, M. (2012) · Advances in protein chemistry and structural biology · doi:10.1016/b978-0-12-398314-5.00002-7 · Cited by 54 · see citing works
“The amygdala may be a key site as it matures earlier than other brain regions and has a powerful developmental influence on the cortex and on motivational out- puts via the nucleus accumbens/ventral tegmental area (NA/VTA) junction (Anderson, 2011; McGinty & Grace, 2009a; Salm et al., 2004).”
Background
Schizophrenia: A unique translational opportunity in behavioral neuroendocrinology
Koenig, J. I. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.06.027 · Cited by 51 · see citing works
Nutritional and immunological factors in breast milk: A role in the intergenerational transmission from maternal psychopathology to child development
Benedetto, M. G. D., Bottanelli, C., Cattaneo, A., Pariante, C. M., & Borsini, A. (2019) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2019.05.032 · Cited by 49 · see citing works
“As suggested by preclinical studies, this adverse effect of cortisol on the infant emotional attitude might be due to developmental alterations, caused by glucocorticoids exposure in early life, of distinct brain structures, including the amygdala, which is highly involved in the emotional regulation (Kraszpulski et a…”
Background
Early emergence of increased fearful behavior in prenatally stressed rats
Dickerson, P. A., LALLY, B., GUNNEL, E., Birkle, D. L., & Salm, A. K. (2005) · Physiology & Behavior · doi:10.1016/j.physbeh.2005.08.025 · Cited by 49 · see citing works
“We demonstrated that PS animals at P90 show significantly expanded dimensions of the lateral amygdala nucleus due to increased numbers of neurons and glia [ 19 ] .W e have recently completed stereological studies on the developmental trajectory of the amygdala of the PS rat [20] and have found significant differences…”
BackgroundSelf-citation
Cortico-amygdala circuits: Role in the conditioned stress response
Berretta, S. (2005) · Stress · doi:10.1080/10253890500489395 · Cited by 47 · see citing works
“It should not be forgotten, however, that chronic stress induces profound morphological and neurochemical changes in brain regions such as the medial prefrontal cortex (mPFC), amygdala and hippocampus (Cook and Wellman 2004; Czeh et al. 2005; Joels et al. 2004; McEwen 2005; McEwen et al. 2002; Radley et al. 2004; Salm…”
Background
Basal anxiety-like behavior predicts differences in dendritic morphology in the medial prefrontal cortex in two strains of rats
Miller, M. M., Morrison, J. H., & McEwen, B. S. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.01.029 · Cited by 46 · see citing works
The effects of prenatal stress on the Purkinje cell neurogenesis
Ulupınar, E., Yücel, F., & Ortuğ, G. (2005) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2005.10.003 · Cited by 46 · see citing works
Enriched environment treatment counteracts enhanced addictive and depressive-like behavior induced by prenatal chronic stress
Yang, J., Li, W., Liu, X., Li, Z., Li, H., Yang, G., Xu, L., & Li, L. (2006) · Brain Research · doi:10.1016/j.brainres.2006.10.028 · Cited by 44 · see citing works
Exposure to Prenatal Stress Is Associated With an Excitatory/Inhibitory Imbalance in Rat Prefrontal Cortex and Amygdala and an Increased Risk for Emotional Dysregulation
Marchisella, F., Creutzberg, K. C., Begni, V., Sanson, A., Wearick‐Silva, L. E., Tractenberg, S. G., Orso, R., Kestering-Ferreira, É., Grassi‐Oliveira, R., & Riva, M. A. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.653384 · Cited by 45 · see citing works
Gamma Oscillations in the Basolateral Amygdala: Biophysical Mechanisms and Computational Consequences
Feng, F., Headley, D. B., Amir, A., Kanta, V., Chen, Z., Paré, D., & Nair, S. S. (2019) · eNeuro · doi:10.1523/eneuro.0388-18.2018 · Cited by 43 · see citing works
“5 10(4) to 2 10(5)/mm(3) (Tuunanen and Pitkänen, 2000; Salm et al., 2004; Pêgo et al., 2008; Rubinow and Juraska, 2009; Chareyron et al., 2011), while the model density is 9840 neurons/mm(3) (27,000 neurons, 1.”
BackgroundInfluential
Neuronal–immune interactions in mediating stress effects in the etiology and course of schizophrenia: Role of the amygdala in developmental co-ordination
Anderson, G. (2010) · Medical Hypotheses · doi:10.1016/j.mehy.2010.08.029 · Cited by 40 · see citing works
“dent amygdala [48], which can be prevented by lithium and modulated by nicotine [49].”
Background
Prenatal Stress, Poverty, and Child Outcomes
Lefmann, T., & Combs-Orme, T. D. (2014) · Child and Adolescent Social Work Journal · doi:10.1007/s10560-014-0340-x · Cited by 41 · see citing works
“Prenatal stress also caused expansion of the lateral nucleus of the amygdala, an area in which learned fear is encoded (Salm et al. 2004).”
Background
Changes Induced by Prenatal Stress in Behavior and Brain Morphology: Can They Be Prevented or Reversed?
Weinstock, M. (2014) · Advances in neurobiology · doi:10.1007/978-1-4939-1372-5_1 · Cited by 37 · see citing works
“In a study performed only in male offspring, prenatal stress caused an increase in the volume of the lateral amygdaloid nucleus which contained more neurons than that of controls (Salm et al. 2004).”
Background
Association Between Prenatal Stress and Infantile Spasms: A Case-Control Study in China
Shang, N.-X., Zou, L., Zhao, J., Zhang, F., & Li, H. (2010) · Pediatric Neurology · doi:10.1016/j.pediatrneurol.2009.09.003 · Cited by 37 · see citing works
“[11] Salm AK, Pavelko M, Krouse EM, Webster W, Kraszpulski M, Birkle DL.”
Background
Neurobehavioral Consequences of Fetal Exposure to Gestational Stress
Sandman, C. A., Glynn, L. M., & Davis, E. P. (2016) · Springer eBooks · doi:10.1007/978-3-319-22023-9_13 · Cited by 37 · see citing works
Maternal exercise during pregnancy ameliorates the postnatal neuronal impairments induced by prenatal restraint stress in mice
Bustamante, C., Henríquez, R., Medina, F., Reinoso, C., Vargas-Foitzick, R., & Pascual, R. (2013) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2013.02.007 · Cited by 35 · see citing works
“These abnormalities are likely due to morphological and functional changes in key areas of the brain that control motor and emotional behaviors, such as the prefrontal cortex (Muhammad et al., 2012) and amygdala (Salm et al., 2004; Kraszpulski et al., 2006).”
Background
Prenatal irradiation–induced brain neuropathology and cognitive impairment
Yang, B., Ren, B. X., & Tang, F. R. (2016) · Brain and Development · doi:10.1016/j.braindev.2016.07.008 · Cited by 34 · see citing works
Neonatal handling enduringly decreases anxiety and stress responses and reduces hippocampus and amygdala volume in a genetic model of differential anxiety: Behavioral-volumetric associations in the Roman rat strains
Río-Álamos, C., Oliveras, I., Piludu, M. A., Gerbolés, C., Cañete, T., Blázquez, G., Lope‐Piedrafita, S., Martínez-Membrives, E., Torrúbia, R., Tobeña, A., et al. (2017) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2016.12.003 · Cited by 34 · see citing works
Gamma Oscillations in the Basolateral Amygdala: Localization, Microcircuitry, and Behavioral Correlates
Headley, D. B., Kyriazi, P., Feng, F., Nair, S. S., & Paré, D. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.3159-20.2021 · Cited by 33 · see citing works
“This resulted in a cell density of 1.25 105 neurons/mm3, in the middle of the range from 2.5 104 to 2 105 neurons/mm3 reported in rats (Tuunanen and Pitkänen, 2000; Salm et al., 2004; Pêgo et al., 2008; Rubinow and Juraska, 2009; Chareyron et al., 2011).”
BackgroundInfluential
Effects of psychologic stress on fetal development and pregnancy outcome
Koubovec, D., Geerts, L., Odendaal, H. J., Stein, D. J., & Vythilingum, B. (2005) · Current Psychiatry Reports · doi:10.1007/s11920-005-0081-9 · Cited by 33 · see citing works
Hub distribution of the brain functional networks of newborns prenatally exposed to maternal depression and SSRI antidepressants
Rotem‐Kohavi, N., Williams, L. J., Muller, A. M., Abdi, H., Virji‐Babul, N., Björnson, B., Brain, U. M., Werker, J. F., GRUNAU, R. E., Miller, S. P., et al. (2019) · Depression and Anxiety · doi:10.1002/da.22906 · Cited by 31 · see citing works
Associations of Air Pollution on the Brain in Children: A Brain Imaging Study.
Guxens, M., Lubczynska, M. J., Pérez‐Crespo, L., Muetzel, R. L., Marroun, H. E., Basagaña, X., Hoek, G., & Tiemeier, H. W. (2022) · PubMed Central · Cited by 27 · see citing works
Antenatal maternal stress alters functional brain responses in adult offspring during conditioned fear
Sadler, T. R., Nguyen, P. T., Yang, J., Givrad, T. K., Mayer, E. A., Maarek, J. I., Hinton, D. R., & Holschneider, D. P. (2011) · Brain Research · doi:10.1016/j.brainres.2011.01.104 · Cited by 26 · see citing works
“These findings are consistent with prior neuroanatomic work reporting enlargement of the amygdala of adult rats previously exposed in-utero to MS (Salm et al., 2004).”
BackgroundResult
Prenatal stress and its association with amygdala-related structural covariance patterns in youth
Marečková, K., Miles, A. E., Liao, Z., Andrýsková, L., Brázdil, M., Paus, T., & Nikolova, Y. S. (2022) · NeuroImage Clinical · doi:10.1016/j.nicl.2022.102976 · Cited by 26 · see citing works
“In humans, all the major amygdala nuclei are fully formed by the 15th week of gestational development (Nikolić and Kostović, 1986) and prior work, including our own, has observed associations between prenatal stress and amygdala volume (Buss et al., 2012; Lupien et al., 2011; Mareckova et al.,…”
Background
Repeated antenatal corticosteroid treatments adversely affect neural transmission time and auditory thresholds in laboratory rats
Church, M. W., Adams, B. R., Anumba, J. I., Jackson, D. A., Kruger, M. L., & Jen, K. ‐. C. (2011) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2011.09.004 · Cited by 23 · see citing works
“Even though rat pregnancy studies found adverse neurodevelopmental [27,39,40,53,79] and ABR effects [50] on offspring following maternal handling stress and saline injections, we did not specifically hypothesize that our SAL offspring would have abnormalities.”
Background
Choline chloride modulates learning, memory, and synaptic plasticity impairments in maternally separated adolescent male rats
Shahraki, S., Esmaeilpour, K., Shabani, M., Sepehri, G., Rajizadeh, M. A., Maneshian, M., Joushi, S., & Sheibani, V. (2021) · International Journal of Developmental Neuroscience · doi:10.1002/jdn.10155 · Cited by 22 · see citing works
“Some studies have shown impairments in emotional capacities as a result of MS leading to the development of anxiety-like behaviours (Huot et al., 2001; Salm et al., 2004), as well as depressive-like (Meaney & Plotsky, 2000) and anhedonia behaviours (Salm et al., 2004).”
Background
The effects of prenatal stress on motivation in the rat pup
Harmon, K. M., Greenwald, M. L., McFarland, A. M., Beckwith, T. J., & Cromwell, H. C. (2008) · Stress · doi:10.1080/10253890802367265 · Cited by 22 · see citing works
“This mild stress regimen has been demonstrated in rats to produce disruption of the HPA axis, increased fearfulness, and changes in amygdala morphology (Ward et al. 2000; Salm et al. 2004; Kraszpulski et al. 2006).”
BackgroundInfluential
Maternal Separation Modifies the Activity of Social Processing Brain Nuclei Upon Social Novelty Exposure
Mejía-Chávez, S., Venebra-Muñoz, A., García‐García, F., Corona-Morales, A. A., & Vargas, A. E. O. (2021) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.651263 · Cited by 21 · see citing works
“, 2007) and anxiety-like behaviors (Wigger and Neumann, 1999; Huot et al., 2001; Salm et al., 2004; Aisa et al., 2007), anhedonia (Huot et al.”
Background
Cocaine-conditioned place preference is predicted by previous anxiety-like behavior and is related to an increased number of neurons in the basolateral amygdala
de Guevara‐Miranda, D. L., Pavón, F. J., Serrano, A., Rivera, P., Estivill‐Torrús, G., Suárez, J., de Fonseca, F. R., Santín, L. J., & Castilla‐Ortega, E. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.10.048 · Cited by 20 · see citing works
Hyper-responsivity to stress in rats is associated with a large increase in amygdala volume. A 7 T MRI study
Bourgin, J., Cachia, A., Boumezbeur, F., Djemaï, B., Bottlaender, M., Duchesnay, É., Mériaux, S., & Jay, T. M. (2015) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2015.02.010 · Cited by 20 · see citing works
“Indeed, the effects of stress on the amygdala may be very longlasting indeed: in rats, prenatal stress can lead to increased amygdala size in adulthood (Salm et al., 2004).”
Prenatal Exposure to Stress and Stress Hormones Influences Child Development
Davis, E. P., & Sandman, C. A. (2006) · Infants & Young Children · doi:10.1097/00001163-200607000-00008 · Cited by 20 · see citing works
“In addition, manipulations during the prenatal and perinatal periods that are likely to lead to elevations of GCs are associated with an increase in amygdalar volume (Salm et al., 2004) and a decrease in PFC GC receptors (Shanks, Larocque, & Meaney, 1995).”
Background
Cognitive and affective alterations by prenatal and postnatal stress interaction
Lee, Y., Kim, Y., & Goto, Y. (2016) · Physiology & Behavior · doi:10.1016/j.physbeh.2016.07.014 · Cited by 19 · see citing works
Functional connectivity in prenatally stressed rats with and without maternal treatment with ladostigil, a brain‐selective monoamine oxidase inhibitor
Goelman, G., Ilinca, R., Zohar, I., & Weinstock, M. (2014) · European Journal of Neuroscience · doi:10.1111/ejn.12621 · Cited by 18 · see citing works
“, 2003; Weinstock, 2008), and an increase in the number of neurons in the lateral amygdaloid nucleus (Salm et al., 2004).”
Background
Prenatal Stress Alters Progestogens to Mediate Susceptibility to Sex-Typical, Stress-Sensitive Disorders, such as Drug Abuse: A Review
Frye, C. A., Paris, J. J., Osborne, D. M., Campbell, J. C., & Kippin, T. E. (2011) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2011.00052 · Cited by 18 · see citing works
“, 2006), and may even surpass controls in the region of the lateral nucleus later in adulthood (Salm et al., 2004).”
Background
Antenatal betamethasone produces protracted changes in anxiety‐like behaviors and in the expression of microtubule‐associated protein 2, brain‐derived neurotrophic factor and the tyrosine kinase B receptor in the rat cerebellar cortex
Pascual, R., Valencia, M., & Bustamante, C. (2015) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2015.04.005 · Cited by 17 · see citing works
“, 2012) in association with morphological limbic changes, including hypertrophy of the lateral amygdaloid nucleus (Salm et al., 2004), decreased dendritic tree complexity in the hippocampus (Bustamante et al.”
Background
Prenatal Stress and Adult Drug-Seeking Behavior: Interactions with Genes and Relation to Nondrug-Related Behavior
Kippin, T. E., Campbell, J. C., Ploense, K. L., Knight, C. P., & Bagley, J. R. (2014) · Advances in neurobiology · doi:10.1007/978-1-4939-1372-5_5 · Cited by 16 · see citing works
Prenatal Stress and Neurodevelopmental Plasticity: Relevance to Psychopathology
Pallarés, M. E., & Antonelli, M. C. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-62817-2_7 · Cited by 17 · see citing works
An epigenetic pathway approach to investigating associations between prenatal exposure to maternal mood disorder and newborn neurobehavior
Conradt, E. D., Adkins, D. E., Crowell, S. E., Monk, C. E., & Kobor, M. S. (2018) · Development and Psychopathology · doi:10.1017/s0954579418000688 · Cited by 16 · see citing works
“These elevations could alter fetal brain structures such as the amygdala, as is the case in animal models (Salm et al., 2004) and human studies (Buss et al., 2012).”
Result
Impact of Prenatal Stress on Amygdala Anatomy in Young Adulthood: Timing and Location Matter
Marečková, K., Mareček, R., Andrýsková, L., Brázdil, M., & Nikolova, Y. S. (2021) · Biological Psychiatry Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2021.07.009 · Cited by 15 · see citing works
An Overview of Psychological and Neurobiological Mechanisms by which Early Negative Experiences Increase Risk of Mood Disorders.
Hassel, S., McKinnon, M. C., Cusi, A. M., & MacQUEEN, G. M. (2011) · Europe PMC (PubMed Central) · Cited by 16 · see citing works
“Down Will Come Baby”: Prenatal Stress, Primitive Defenses and Gestational Dysregulation
Thomson, P. (2007) · Journal of Trauma & Dissociation · doi:10.1300/j229v08n03_05 · Cited by 15 · see citing works
Cognitive behavior therapy and worry reduction in an outpatient with generalized anxiety disorder
Khodarahimi, S., & Pole, N. (2010) · Clinical Case Studies · doi:10.1177/1534650109351306 · Cited by 14 · see citing works
“Anxiety includes pervasive feelings of tension, dread, apprehension, and impending disaster, as well as unpleasant feelings of stress, uneasiness, tension, and worry (Salm et al., 2004).”
Influence of prenatal transportation stress-induced differential DNA methylation on the physiological control of behavior and stress response in suckling Brahman bull calves
Littlejohn, B. P., Price, D. M., Neuendorff, D. A., Carroll, J. A., VANN, R. C., Riggs, P. K., Riley, D. G., Long, C. R., Randel, R. D., & Welsh, T. H. (2019) · Journal of Animal Science · doi:10.1093/jas/skz368 · Cited by 14 · see citing works
A Neuroscience Perspective on Emotional Development
Morales, S., & Fox, N. A. (2019) · Springer eBooks · doi:10.1007/978-3-030-17332-6_4 · Cited by 13 · see citing works
Brain Magnetic Resonance Imaging Findings in Children after Antenatal Maternal Depression Treatment, a Longitudinal Study Built on a Pilot Randomized Controlled Trial
Bleker, L., Milgrom, J., Parker, D., Gemmill, A. W., Holt, C. J., Connelly, A., Burger, H., Roseboom, T., & de Rooij, S. (2019) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph16101816 · Cited by 13 · see citing works
“In animal models, changes in brain morphology have been observed in offspring of mothers exposed to prenatal stress, such as expanded dimensions of the lateral nucleus of the amygdala [34], and reduced spine density and dendritic complexity in the prefrontal cortex [35] in prenatally stressed animals.”
Background
Mismatch between anxiety status and morphometric parameters in the amygdala and bed nucleus of the stria terminalis
Pêgo, J. M., Morgado, P. F., Cerqueira, J., Almeida, O. F. X., & Sousa, N. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.06.035 · Cited by 12 · see citing works
Neurobehavioral Disorders and Developmental Origins of Health and Disease
Sandman, C. A., Class, Q. A., Glynn, L. M., & Davis, E. P. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-801383-0.00013-x · Cited by 11 · see citing works
Os efeitos do estresse na função do eixo hipotalâmico-pituitário-adrenal em indivíduos com esquizofrenia
Guest, F. L., Martins‐de‐Souza, D., Rahmoune, H., Bahn, S., & Guest, P. C. (2012) · Archives of Clinical Psychiatry (São Paulo) · doi:10.1590/s0101-60832012005000002 · Cited by 14 · see citing works
Developmental Origins of Stress and Psychiatric Disorders
Guest, F. L., & Guest, P. C. (2018) · Methods in molecular biology · doi:10.1007/978-1-4939-7614-0_3 · Cited by 10 · see citing works
Prenatal stress influences 8-OH-DPAT modulated startle responding and [H]-8-OH-DPAT binding in rats
GRIFFINIII, W., Skinner, H. D., & Birkle, D. L. (2005) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2005.04.013 · Cited by 9 · see citing works
Self-citation
Dendritic Architecture of Principal Basolateral Amygdala Neurons Changes Congruently with Endocrine Response to Stress
Hegde, A., Yee, P. S., & Mitra, R. (2017) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph14070779 · Cited by 7 · see citing works
“This is also supported by the observation that prenatal stress significantly increases the volume of the lateral amygdala [39] in parallel to increasing glucocorticoid levels and causing adrenal hypertrophy [40].”
Background
Maternal stress suppresses cell proliferation in the forebrain of zebrafish larvae
Higuchi, M. (2020) · Genes to Cells · doi:10.1111/gtc.12761 · Cited by 6 · see citing works
“Of interest, the volume of amygdala, the numbers of neurons and glial cells were found to increase in later postnatal stages (Kerchner, Malsbury, Ward, & Ward, 1995; Salm et al., 2004).”
Background

Prenatal stress affects the developmental trajectory of the rat amygdala
Kraszpulski, M., Dickerson, P. A., & Salm, A. K. (2006) · Stress · doi:10.1080/10253890600798109 · Cited by 85 · see citing works
Self-citation
Prenatal Stress Alters the Development of Socioemotional Behavior and Amygdala Neuron Excitability in Rats
Ehrlich, D., & Rainnie, D. G. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.55 · Cited by 48 · see citing works
Early emergence of increased fearful behavior in prenatally stressed rats
Dickerson, P. A., LALLY, B., GUNNEL, E., Birkle, D. L., & Salm, A. K. (2005) · Physiology & Behavior · doi:10.1016/j.physbeh.2005.08.025 · Cited by 49 · see citing works
Self-citation
Prenatal stress increases corticotropin-releasing factor (CRF) content and release in rat amygdala minces
Cratty, M. S., Ward, H. E., Johnson, E. A., Azzaro, A. J., & Birkle, D. L. (1995) · Brain Research · doi:10.1016/0006-8993(95)00087-7 · Cited by 201 · see citing works
Self-citation
Prenatal Restraint Stress and Long-Term Affective Consequences
van den Hove, D., Blanco, C. E., Aendekerk, B., Desbonnet, L., Bruschettini, M., Steinbusch, H. P., Prickaerts, J., & Steinbusch, H. W. M. (2005) · Developmental Neuroscience · doi:10.1159/000086711 · Cited by 129 · see citing works

Authors: Salm, A. K., Pavelko, M., Krouse, E. M., Webster, W., Kraszpulski, M., & Birkle, D. L.
Affiliations: West Virginia University (US)
Corresponding author: Salm, A.K.
ORCID: Salm, A.K.
Venue: Developmental Brain Research
Publisher: Elsevier BV
Published: 2004-02
Volume: 148
Issue: 2
Pages: 159-167
ISSN: 0165-3806 (ISSN-L)
DOI: 10.1016/j.devbrainres.2003.11.005
OpenAlex: W2110558389
Cited by: 125
References: 83
Citations by year: 2025: 1 · 2024: 1 · 2023: 1 · 2022: 3 · 2021: 9 · 2020: 3 · 2019: 10 · 2018: 7 · 2017: 5 · 2016: 5 · 2015: 7 · 2014: 7 · 2013: 2 · 2012: 11
FWCI: 4.22
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Developmental Brain Research (publishedVersion)
PubMed (publishedVersion)
Funders: British Sedimentological Research Group
National Institutes of Health (5r01mh060945-03)
National Institute of Mental Health (MH60945)
Topics: Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Maternal Mental Health During Pregnancy and Postpartum
Keywords: prenatal stress, lateral amygdala, amygdala development, anxiety disorders, fear, corticotropin-releasing factor, hypothalamic-pituitary-adrenal axis, glial cells, rat offspring
MeSH terms: Aging, Amygdala, Animals, Animals, Newborn, Cell Count, Female, Male, Neuroglia, Neurons, Pregnancy, Prenatal Exposure Delayed Effects, Stress, Psychological, Rats, Sprague-Dawley, Rats

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Lateral amygdaloid nucleus expansion in adult rats is associated with exposure to prenatal stress

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