Neuron number decreases in the rat ventral, but not dorsal, medial prefrontal cortex between adolescence and adulthood
Abstract
Neuroimaging studies have established that there are losses in the volume of gray matter in certain cortical regions between adolescence and adulthood, with changes in the prefrontal cortex being particularly dramatic. Previous work from our laboratory has demonstrated that cell death can occur as late as the fourth postnatal week in the rat cerebral cortex. The present study examined the possibility that neuronal loss may occur between adolescence and adulthood in the rat prefrontal cortex. Rats of both sexes were examined during adolescence (at day 35) and young adulthood (at day 90). The volume, neuronal number, and glial number of the medial prefrontal cortex (mPFC) were quantified using unbiased stereological techniques. Neurons were lost from the ventral, but not dorsal, mPFC between adolescence and adulthood, suggesting a late wave of apoptosis that was region-specific. This was accompanied by a decrease in the volume of the female ventral mPFC. In contrast to neuron number, the number of glial cells was stable in the ventral mPFC and increased between adolescence and adulthood in the dorsal mPFC. Sex-specific developmental changes in neuron number, glial number, and volume resulted in sex differences in adults that were not seen during adolescence. The loss of neurons at this time may make the peri-adolescent prefrontal cortex particularly susceptible to the influence of environmental factors.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In rats, neuron number declines in ventral but not dorsal medial prefrontal cortex between adolescence and adulthood.
“Stereological analyses have revealed declines in the number of neurons within both of these regions between adolescence and adulthood in rats, effects studied in the basolateral nucleus of the amygdala (Rubinow & Juraska, 2009) and seen in ventral (but not dorsal) mPFC (Markham et al, 2007)”
From Rewards, aversions and affect in adolescence: emerging convergences across laboratory animal and human data (2011) · cites this paper as Markham et al, 2007
In humans and laboratory animals, frontal cortex volume decreases during adolescence.
“In both humans and laboratory animals, the volume of frontal cortex decreases in adolescence whereas the volume of the amygdala increases (e.g., Giedd et al, 1996; Giedd, 2004; Markham et al, 2007).”
From Rewards, aversions and affect in adolescence: emerging convergences across laboratory animal and human data (2011) · cites this paper as Markham et al, 2007
In humans and laboratory animals, amygdala volume increases during adolescence.
“In both humans and laboratory animals, the volume of frontal cortex decreases in adolescence whereas the volume of the amygdala increases (e.g., Giedd et al, 1996; Giedd, 2004; Markham et al, 2007).”
From Rewards, aversions and affect in adolescence: emerging convergences across laboratory animal and human data (2011) · cites this paper as Markham et al, 2007
In humans and laboratory animals, frontal cortex volume declines during adolescence while amygdala volume increases.
“In both humans and laboratory animals, the volume of frontal cortex decreases in adolescence whereas the volume of the amygdala increases (e.g., Giedd et al, 1996; Giedd, 2004; Markham et al, 2007).”
From Rewards, aversions and affect in adolescence: emerging convergences across laboratory animal and human data (2011) · cites this paper as Markham et al, 2007
In rats, stereological analyses show declines in neuron number in the basolateral amygdala and ventral mPFC between adolescence and adulthood.
“Stereological analyses have revealed declines in the number of neurons within both of these regions between adolescence and adulthood in rats, effects studied in the basolateral nucleus of the amygdala (Rubinow & Juraska, 2009) and seen in ventral (but not dorsal) mPFC (Markham et al, 2007)”
From Rewards, aversions and affect in adolescence: emerging convergences across laboratory animal and human data (2011) · cites this paper as Markham et al, 2007
In rodents, frontal white matter is affected by age and hormones in both sexes.
“In rodents, frontal white matter is also affected by age and hormones in both sexes (Markham et al., 2007).”
From Does puberty mark a transition in sensitive periods for plasticity in the associative neocortex? (2017) · cites this paper as Markham et al., 2007
Cites
Brain development during childhood and adolescence: a longitudinal MRI study
Giedd, J. N., Blumenthal, J., Jeffries, N. O., Castellanos, F. X., Liu, H., Zijdenbos, A., Paus, T., Evans, A. C., & Rapoport, J. L. (1999) · Nature Neuroscience · doi:10.1038/13158 · Cited by 5,552 · see citing works
The adolescent brain and age-related behavioral manifestations
Spear, L. P. (2000) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(00)00014-2 · Cited by 5,433 · see citing works
Cognitive and affective development in adolescence
Steinberg, L. (2005) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2004.12.005 · Cited by 2,978 · see citing works
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
Synaptic density in human frontal cortex —Developmental changes and effects of aging
Peter R., H. (1979) · Brain Research · doi:10.1016/0006-8993(79)90349-4 · Cited by 2,645 · see citing works
Regional Development of the Brain in Early Life
(1968) · Archives of Disease in Childhood · doi:10.1136/adc.43.229.388 · Cited by 2,107 · see citing works
Positron emission tomography study of human brain functional development
Chugani, H. T., Phelps, M. E., & Mazziotta, J. C. (1987) · Annals of Neurology · doi:10.1002/ana.410220408 · Cited by 1,548 · see citing works
Intellectual ability and cortical development in children and adolescents
Shaw, P., Greenstein, D., Lerch, J., Clasen, L., Lenroot, R., Gogtay, N., Evans, A., Rapoport, J., & Giedd, J. (2006) · Nature · doi:10.1038/nature04513 · Cited by 1,543 · see citing works
Structural and functional brain development and its relation to cognitive development
Casey, B. J., Giedd, J. N., & Thomas, K. M. (2000) · Biological Psychology · doi:10.1016/s0301-0511(00)00058-2 · Cited by 1,506 · see citing works
Longitudinal Mapping of Cortical Thickness and Brain Growth in Normal Children
Sowell, E. R., Thompson, P. M., Leonard, C. M., Welcome, S. E., Kan, E., & Toga, A. W. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.1798-04.2004 · Cited by 1,481 · see citing works
In vivo evidence for post-adolescent brain maturation in frontal and striatal regions
Sowell, E. R., Thompson, P. M., Holmes, C. J., Jernigan, T. L., & Toga, A. W. (1999) · Nature Neuroscience · doi:10.1038/13154 · Cited by 1,439 · see citing works
Pfefferbaum, A., Mathalon, D. H., Sullivan, E. V., Rawles, J. M., Zipursky, R. B., & Lim, K. O. (1994) · Archives of Neurology · doi:10.1001/archneur.1994.00540210046012 · Cited by 1,363 · see citing works
Structural maturation of neural pathways in children and adolescents: in vivo study
Paus, T., Zijdenbos, A., Worsley, K., Collins, D. L., Blumenthal, J., Giedd, J. N., Rapoport, J. L., & Evans, A. C. (1999) · Science · doi:10.1126/science.283.5409.1908 · Cited by 1,322 · see citing works
The cortical projections of the mediodorsal nucleus and adjacent thalamic nuclei in the rat
Krettek, J. E., & Price, J. L. (1977) · The Journal of Comparative Neurology · doi:10.1002/cne.901710204 · Cited by 1,277 · see citing works
Unbiased Stereology: Three-Dimensional Measurement in Microscopy
Howard, C. V., & Reed, M. (1998) · Cited by 1,143 · see citing works
Quantitative magnetic resonance imaging of human brain development: ages 4–18
Giedd, J. N., Snell, J. W., Lange, N., Rajapakse, J. C., Casey, B. J., Kozuch, P. L., Vaituzis, A. C., Vauss, Y. C., Hamburger, S. D., Kaysen, D., et al. (1996) · Cerebral Cortex · doi:10.1093/cercor/6.4.551 · Cited by 1,024 · see citing works
Do rats have a prefrontal cortex?
Uylings, H. B. M., Groenewegen, H. J., & Kolb, B. (2003) · Behavioural Brain Research · doi:10.1016/j.bbr.2003.09.028 · Cited by 1,013 · see citing works
Sowell, E. R., Thompson, P. M., Tessner, K. D., & Toga, A. W. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-22-08819.2001 · Cited by 983 · see citing works
Unbiased Stereology. Three‐Dimensional Measurement in Microscopy.
Sandau, K. (1999) · Journal of Microscopy · doi:10.1046/j.1365-2818.1999.0429a.x · Cited by 890 · see citing works
Maturation of white matter in the human brain: A review of magnetic resonance studies.
Paus, T., Collins, D. L., Evans, A. C., Leonard, G., Pike, B., & Zijdenbos, A. (2001) · Brain Research Bulletin · doi:10.1016/s0361-9230(00)00434-2 · Cited by 863 · see citing works
Neurobiology of Cingulate Cortex and Limbic Thalamus
Vogt, B. A., & Gabriel, M. (1993) · Birkhäuser Boston eBooks · doi:10.1007/978-1-4899-6704-6 · Cited by 772 · see citing works
Benes, F. M. (1994) · Archives of General Psychiatry · doi:10.1001/archpsyc.1994.03950060041004 · Cited by 744 · see citing works
Sex Differences in Brain Maturation during Childhood and Adolescence
De Bellis, M. D. (2001) · Cerebral Cortex · doi:10.1093/cercor/11.6.552 · Cited by 728 · see citing works
Synaptogenesis in the Prefrontal Cortex of Rhesus Monkeys
Bourgeois, J.-P., Goldman-Rakic, P. S., & Rakic, P. (1994) · Cerebral Cortex · doi:10.1093/cercor/4.1.78 · Cited by 687 · see citing works
Developmental changes in performance on tests of purported frontal lobe functioning
Levin, H. S., Culhane, K. A., Hartmann, J., Evankovich, K. D., Mattson, A. J., Harward, H. N., Ringholz, G. M., Ewing‐Cobbs, L., & Fletcher, J. M. (1991) · Developmental Neuropsychology · doi:10.1080/87565649109540499 · Cited by 581 · see citing works
Sexual dimorphism of the developing human brain
Giedd, J. N., Castellanos, F. X., Rajapakse, J. C., Vaituzis, A. C., & Rapoport, J. L. (1997) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/s0278-5846(97)00158-9 · Cited by 500 · see citing works
MATURATION OF HUMAN CEREBRUM OBSERVED <i>IN VIVO</i> DURING ADOLESCENCE
JERNIGAN, T. L., TRAUNER, D. A., HESSELINK, J. R., & TALLAL, P. A. (1991) · Brain · doi:10.1093/brain/114.5.2037 · Cited by 444 · see citing works
Changes in regional cerebral blood flow during brain maturation in children and adolescents.
Chiron, C., Raynaud, C., Maziere, B., Zilbovicius, M., Laflamme, L., Masure, M. C., Dulac, O., Bourguignon, M., & Syrota, A. (1992) · PubMed · Cited by 405 · see citing works
Lewis, D. (1997) · Neuropsychopharmacology · doi:10.1016/s0893-133x(96)00277-1 · Cited by 388 · see citing works
SOWELL, E. R., DELIS, D., STILES, J., & JERNIGAN, T. L. (2001) · Journal of the International Neuropsychological Society · doi:10.1017/s135561770173305x · Cited by 388 · see citing works
Cytoarchitectonic development of the prefrontal cortex in the rat
van Eden, C. G., & Uylings, H. B. M. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902410302 · Cited by 306 · see citing works
Functional development of the prefrontal cortex in early life and the problem of neuronal plasticity
Goldman, P. S. (1971) · Experimental Neurology · doi:10.1016/0014-4886(71)90005-7 · Cited by 271 · see citing works
Anderson, S. A., Classey, J. D., Condé, F., Lund, J. S., & Lewis, D. A. (1995) · Neuroscience · doi:10.1016/0306-4522(95)00051-j · Cited by 245 · see citing works
Psychophysiological indices of cerebral maturation
Hudspeth, W. J., & Pribram, K. H. (1992) · International Journal of Psychophysiology · doi:10.1016/0167-8760(92)90039-e · Cited by 167 · see citing works
Neafsey, E. J., Terreberry, R. R., Hurley, K. M., Ruit, K. G., & Frysztak, R. J. (1993) · Birkhäuser Boston eBooks · doi:10.1007/978-1-4899-6704-6_7 · Cited by 159 · see citing works
Peripubertal refinement of the intrinsic and associational circuitry in monkey prefrontal cortex
Woo, T.-U., Pucak, M. L., Kye, C. H., Matus, C. V., & Lewis, D. A. (1997) · Neuroscience · doi:10.1016/s0306-4522(97)00059-6 · Cited by 157 · see citing works
Development of place navigation in rats from weaning to puberty
Schenk, F. (1985) · Behavioral and Neural Biology · doi:10.1016/s0163-1047(85)91510-9 · Cited by 143 · see citing works
Postnatal volumetric development of the prefrontal cortex in the rat
van Eden, C. G., & Uylings, H. B. M. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902410303 · Cited by 135 · see citing works
Alexander, G. E., & Goldman, P. S. (1978) · Brain Research · doi:10.1016/0006-8993(78)90566-8 · Cited by 134 · see citing works
Ovarian hormones after postnatal day 20 reduce neuron number in the rat primary visual cortex
Nuñez, J. L., Sodhi, J., & Juraska, J. M. (2002) · Journal of Neurobiology · doi:10.1002/neu.10092 · Cited by 102 · see citing works
Self-citationThe Effects of Prelimbic and Infralimbic Lesions on Working Memory for Visual Objects in Rats
Ragozzino, M. E., Detrick, S., & Kesner, R. P. (2002) · Neurobiology of Learning and Memory · doi:10.1006/nlme.2001.4003 · Cited by 97 · see citing works
Cell death in the development of the posterior cortex in male and female rats
Nuñez, J. L., Lauschke, D. M., & Juraska, J. M. (2001) · The Journal of Comparative Neurology · doi:10.1002/cne.1051 · Cited by 96 · see citing works
Self-citationGabbott, P. L. A., & Stewart, M. G. (1987) · Neuroscience · doi:10.1016/0306-4522(87)90040-6 · Cited by 93 · see citing works
Sexually dimorphic cognitive style in rats emerges after puberty
Kanıt, L., Taşkıran, D., Yılmaz, O., Balkan, B., Demirgören, S., Furedy, J. J., & Pöğün, Ş. (2000) · Brain Research Bulletin · doi:10.1016/s0361-9230(00)00232-x · Cited by 83 · see citing works
Sex differences in neuron number in the binocular area of the rat visual cortex
Reid, S. N. M., & Juraska, J. M. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903210311 · Cited by 68 · see citing works
Self-citationMyelination in the splenium of the corpus callosum in adult male and female rats
Nuñez, J. L., Nelson, J., Pych, J. C., Kim, J. H. Y., & Juraska, J. M. (2000) · Developmental Brain Research · doi:10.1016/s0165-3806(99)00193-5 · Cited by 65 · see citing works
Self-citationKesner, R. P., & Ragozzino, M. E. (2003) · Behavioural Brain Research · doi:10.1016/j.bbr.2003.09.024 · Cited by 64 · see citing works
Age-Related Changes in Frontal and Temporal Lobe Volumes in Men: A Magnetic Resonance Imaging Study
Bartzokis, G., Beckson, M., Lu, P. H., Nuechterlein, K. H., Edwards, N., & Mintz, J. (2001) · Archives of General Psychiatry · doi:10.1001/archpsyc.58.5.461 · Cited by 14 · see citing works
Flagged first, then by citations
1 of the 51 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Stress, sensitive periods and maturational events in adolescent depression
Andersen, S. L., & Teicher, M. H. (2008) · Trends in Neurosciences · doi:10.1016/j.tins.2008.01.004 · Cited by 1,005 · see citing works
Air pollution, cognitive deficits and brain abnormalities: A pilot study with children and dogs
Calderón‐Garcidueñas, L., Mora-Tiscareño, A., Ontiveros, E., Gómez-Garza, G., Mejía, G. B., Broadway, J. M., Chapman, S., Valencia‐Salazar, G., Jewells, V. L., Maronpot, R. R., et al. (2008) · Brain and Cognition · doi:10.1016/j.bandc.2008.04.008 · Cited by 580 · see citing works
Stress and the developing adolescent brain
Eiland, L. R., & Romeo, R. D. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.10.048 · Cited by 491 · see citing works
Sex Differences and the Impact of Steroid Hormones on the Developing Human Brain
Neufang, S., Specht, K., Hausmann, M., Güntürkün, O., Herpertz‐Dahlmann, B., Fink, G. R., & Konrad, K. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhn100 · Cited by 421 · see citing works
Sex differences in anxiety and emotional behavior
Donner, N. C., & Lowry, C. A. (2013) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-013-1271-7 · Cited by 379 · see citing works
Brenhouse, H. C., & Andersen, S. L. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.04.013 · Cited by 340 · see citing works
Adolescent Alcohol Exposure Persistently Impacts Adult Neurobiology and Behavior
Crews, F. T., Vetreno, R. P., Broadwater, M., & Robinson, D. L. (2016) · Pharmacological Reviews · doi:10.1124/pr.115.012138 · Cited by 332 · see citing works
The organizing actions of adolescent gonadal steroid hormones on brain and behavioral development
Schulz, K. M., & Sisk, C. L. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.07.036 · Cited by 316 · see citing works
Spear, L. P. (2011) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2011.08.001 · Cited by 292 · see citing works
Pubertal onset as a critical transition for neural development and cognition
Juraska, J. M., & Willing, J. (2016) · Brain Research · doi:10.1016/j.brainres.2016.04.012 · Cited by 249 · see citing works
Self-citationMcCormick, C. M., & Mathews, I. Z. (2010) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2009.09.019 · Cited by 230 · see citing works
Koss, W. A., Belden, C. E., Hristov, A. D., & Juraska, J. M. (2014) · Synapse · doi:10.1002/syn.21716 · Cited by 228 · see citing works
Self-citationRomeo, R. D. (2016) · Brain Research · doi:10.1016/j.brainres.2016.03.021 · Cited by 226 · see citing works
Understanding the role of puberty in structural and functional development of the adolescent brain
Goddings, A., Beltz, A., Peper, J. S., Crone, E. A., & Braams, B. R. (2019) · Journal of Research on Adolescence · doi:10.1111/jora.12408 · Cited by 219 · see citing works
Page, C. E., & Coutellier, L. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.07.024 · Cited by 213 · see citing works
Shanmugan, S., & Epperson, C. N. (2012) · Human Brain Mapping · doi:10.1002/hbm.22218 · Cited by 210 · see citing works
Juraska, J. M., Sisk, C. L., & DonCarlos, L. L. (2013) · Hormones and Behavior · doi:10.1016/j.yhbeh.2013.05.010 · Cited by 192 · see citing works
Self-citationAdolescence and Reward: Making Sense of Neural and Behavioral Changes Amid the Chaos
Walker, D. M., Bell, M. R., Flores, C., Gulley, J. M., Willing, J., & Paul, M. J. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.1834-17.2017 · Cited by 183 · see citing works
Perry, J. L., Joseph, J. E., Jiang, Y., Zimmerman, R. S., Kelly, T. H., Darna, M., Huettl, P., Dwoskin, L. P., & Bardo, M. T. (2011) · Brain Research Reviews · doi:10.1016/j.brainresrev.2010.09.001 · Cited by 180 · see citing works
(2010) · American journal of play · Cited by 179 · see citing works
Does puberty mark a transition in sensitive periods for plasticity in the associative neocortex?
Piekarski, D. J., Johnson, C. M., Boivin, J. R., Thomas, A. W., Lin, W. C., Delevich, K., M. Galarce, E., & Wilbrecht, L. (2017) · Brain Research · doi:10.1016/j.brainres.2016.08.042 · Cited by 175 · see citing works
Drzewiecki, C. M., Willing, J., & Juraska, J. M. (2016) · Synapse · doi:10.1002/syn.21909 · Cited by 168 · see citing works
Self-citationAssociation weight matrix for the genetic dissection of puberty in beef cattle
Fortes, M. R. S., Reverter, A., Zhang, Y., Collis, E., Nagaraj, S. H., Jonsson, N. N., Prayaga, K. C., Barris, W., & Hawken, R. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1002044107 · Cited by 166 · see citing works
Long-Lasting Cognitive Deficits Resulting from Adolescent Nicotine Exposure in Rats
Counotte, D. S., Spijker, S., Van de Burgwal, L. H., Hogenboom, F., Schoffelmeer, A. N. M., De Vries, T. J., Smit, A. B., & Pattij, T. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2008.96 · Cited by 163 · see citing works
Prefrontal cortical inputs to the basal amygdala undergo pruning during late adolescence in the rat
Cressman, V. L., Balaban, J., Steinfeld, S., Shemyakin, A., Graham, P., Parisot, N., & Moore, H. (2010) · Journal of Comparative Neurology · doi:10.1002/cne.22359 · Cited by 161 · see citing works
Sex Differences in Adolescent Depression: Do Sex Hormones Determine Vulnerability?
Naninck, E. F. G., Lucassen, P. J., & Bakker, J. (2011) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2011.02125.x · Cited by 160 · see citing works
Sex differences in hippocampal function
Koss, W. A., & Frick, K. M. (2017) · Journal of Neuroscience Research · doi:10.1002/jnr.23864 · Cited by 156 · see citing works
Willing, J., & Juraska, J. M. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.05.073 · Cited by 153 · see citing works
Self-citationImmunohistochemical Analyses of Long-Term Extinction of Conditioned Fear in Adolescent Rats
Kim, J. H., Li, S., & Richardson, R. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhq116 · Cited by 149 · see citing works
Sex steroids and schizophrenia
Markham, J. A. (2011) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-011-9184-2 · Cited by 148 · see citing works
Self-citationHiramoto, T., Kang, G., Suzuki, G., Satoh, Y., Kucherlapati, R., Watanabe, Y., & Hiroi, N. (2011) · Human Molecular Genetics · doi:10.1093/hmg/ddr404 · Cited by 126 · see citing works
Research on alcohol and adolescent brain development: opportunities and future directions
Witt, E. D. (2010) · Alcohol · doi:10.1016/j.alcohol.2009.08.011 · Cited by 125 · see citing works
SPEAR, L. P., & Varlinskaya, E. I. (2010) · Developmental Psychobiology · doi:10.1002/dev.20457 · Cited by 120 · see citing works
Rubinow, M. J., & Juraska, J. M. (2008) · The Journal of Comparative Neurology · doi:10.1002/cne.21924 · Cited by 118 · see citing works
Self-citationCharacterization of the Cognitive Impairments Induced by Prenatal Exposure to Stress in the Rat
Markham, J. A., Taylor, A. R., Taylor, S. B., Bell, D. B., & Koenig, J. I. (2010) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2010.00173 · Cited by 116 · see citing works
Self-citationHammerslag, L. R., & Gulley, J. M. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.04.008 · Cited by 110 · see citing works
Zehr, J. L., Culbert, K. M., Sisk, C. L., & Klump, K. L. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.06.005 · Cited by 106 · see citing works
Silvers, J. A., Insel, C., Powers, A., Franz, P., Helion, C., Martin, R., Weber, J., Mischel, W., Casey, B. J., & Ochsner, K. N. (2017) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2016.06.005 · Cited by 99 · see citing works
Koss, W. A., Lloyd, M. M., Sadowski, R. N., Wise, L. M., & Juraska, J. M. (2015) · Developmental Psychobiology · doi:10.1002/dev.21290 · Cited by 96 · see citing works
Self-citationEpigenetic impacts of endocrine disruptors in the brain
Walker, D. M., & Gore, A. C. (2017) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2016.09.002 · Cited by 94 · see citing works
Guadagno, A., Belliveau, C., Mechawar, N., & Walker, C. (2021) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2021.669120 · Cited by 92 · see citing works
Stress, sensitive periods, and substance abuse
Andersen, S. L. (2019) · Neurobiology of Stress · doi:10.1016/j.ynstr.2018.100140 · Cited by 92 · see citing works
Prefrontal Plasticity and Stress Inoculation-Induced Resilience
Katz, M., Liu, C., Schaer, M., Parker, K. J., Ottet, M.-C., Epps, A., Buckmaster, C. L., Bammer, R., Moseley, M. E., Schatzberg, A. F., et al. (2009) · Developmental Neuroscience · doi:10.1159/000216540 · Cited by 91 · see citing works
Sex Differences in the Development of the Rodent Corticolimbic System
Premachandran, H., Zhao, M., & Arruda-Carvalho, M. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.583477 · Cited by 89 · see citing works
Xu, X., Dong, T., Hong, X., Chen, L., & Xie, L. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.04.027 · Cited by 88 · see citing works
Coming of age in the frontal cortex: The role of puberty in cortical maturation
Delevich, K. M., Klinger, M., Okada, N. J., & Wilbrecht, L. (2021) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2021.04.021 · Cited by 86 · see citing works
Markham, J. A., Mullins, S. E., & Koenig, J. I. (2012) · The Journal of Comparative Neurology · doi:10.1002/cne.23262 · Cited by 85 · see citing works
Self-citationEffects of stressors in adolescence on learning and memory in rodent models
Green, M. R., & McCormick, C. M. (2013) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.09.012 · Cited by 81 · see citing works
Counotte, D. S., Smit, A. B., Pattij, T., & Spijker, S. (2011) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2011.05.010 · Cited by 77 · see citing works
Play fighting and the development of the social brain: The rat’s tale
Pellis, S. M., Pellis, V. C., Ham, J. R., & Stark, R. A. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105037 · Cited by 76 · see citing works
Broadwater, M., & SPEAR, L. P. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.08.013 · Cited by 76 · see citing works
Bell, M. R., Thompson, L. M., Rodriguez, K. M., & Gore, A. C. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.11.007 · Cited by 74 · see citing works
Werd, H. J. J. M. V. D., & Uylings, H. B. M. (2008) · Brain Structure and Function · doi:10.1007/s00429-007-0164-y · Cited by 73 · see citing works
The effects of abused drugs on adolescent development of corticolimbic circuitry and behavior
Gulley, J. M., & Juraska, J. M. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.05.026 · Cited by 73 · see citing works
Self-citationKougias, D. G., Sellinger, E. P., Willing, J., & Juraska, J. M. (2018) · The Journal of Neuroscience · doi:10.1523/jneurosci.0607-18.2018 · Cited by 72 · see citing works
Self-citationUnemura, K., Kume, T., Kondo, M., Maeda, Y., Izumi, Y., & Akaike, A. (2012) · Journal of Pharmacological Sciences · doi:10.1254/jphs.12047fp · Cited by 69 · see citing works
Reducing substance use during adolescence: a translational framework for prevention
Stanis, J. J., & Andersen, S. L. (2014) · Psychopharmacology · doi:10.1007/s00213-013-3393-1 · Cited by 69 · see citing works
Shapiro, L. P., Parsons, R. G., Koleske, A. J., & Gourley, S. L. (2016) · Journal of Neuroscience Research · doi:10.1002/jnr.23960 · Cited by 68 · see citing works
Broadwater, M., Lee, S., Yu, Y., Hongtu Zhu, B., Crews, F. T., Robinson, D. L., & Shih, Y. I. (2017) · Addiction Biology · doi:10.1111/adb.12530 · Cited by 68 · see citing works
Drzewiecki, C. M., Willing, J., & Juraska, J. M. (2020) · Brain Structure and Function · doi:10.1007/s00429-020-02137-z · Cited by 67 · see citing works
Self-citationDrzewiecki, C. M., & Juraska, J. M. (2020) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2020.173044 · Cited by 67 · see citing works
Self-citationAndersen, S. L. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.07.012 · Cited by 67 · see citing works
Willing, J., Cortes, L. R., Brodsky, J. M., Kim, T., & Juraska, J. M. (2017) · Developmental Psychobiology · doi:10.1002/dev.21525 · Cited by 66 · see citing works
Self-citationZovkic, I. B., & McCormick, C. M. (2007) · Behavioural Pharmacology · doi:10.1097/fbp.0b013e3282effbf5 · Cited by 64 · see citing works
A longitudinal analysis of puberty‐related cortical development
Vijayakumar, N., Youssef, G. J., Allen, N. B., Anderson, V. A., Efron, D., Hazell, P., Mundy, L. K., Nicholson, J. M., Patton, G. C., Seal, M. L., et al. (2020) · NeuroImage · doi:10.1016/j.neuroimage.2020.117684 · Cited by 62 · see citing works
Sex differences in animal models of schizophrenia shed light on the underlying pathophysiology
Hill, R. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.10.014 · Cited by 61 · see citing works
Westbrook, S. R., Hankosky, E. R., Dwyer, M. R., & Gulley, J. M. (2018) · Behavioral Neuroscience · doi:10.1037/bne0000235 · Cited by 61 · see citing works
Bergstrom, H. C., McDonald, C. G., French, H. T., & Smith, R. F. (2008) · Synapse · doi:10.1002/syn.20467 · Cited by 60 · see citing works
Küppers, E., Gleiser, C., Brito, V., Wachter, B., Pauly, T., Hirt, B., & Grissmer, S. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06531.x · Cited by 60 · see citing works
The impact of adolescent stress experiences on neurobiological development
Iacono, L. L., & Carola, V. (2017) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2017.09.040 · Cited by 59 · see citing works
Markham, J. A., Herting, M. M., Luszpak, A. E., Juraska, J. M., & Greenough, W. T. (2009) · Brain Research · doi:10.1016/j.brainres.2009.06.087 · Cited by 58 · see citing works
Self-citationFramework for sex differences in adolescent neurobiology: A focus on cannabinoids
Viveros, M., Marco, E. M., López‐Gallardo, M., García‐Segura, L. M., & Wagner, E. J. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.09.005 · Cited by 58 · see citing works
Prefrontal-Amygdala Connectivity and State Anxiety during Fear Extinction Recall in Adolescents
Ganella, D. E., Barendse, M. E. A., Kim, J. H., & Whittle, S. (2017) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2017.00587 · Cited by 56 · see citing works
Cortical reorganization during adolescence: What the rat can tell us about the cellular basis
Juraska, J. M., & Drzewiecki, C. M. (2020) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2020.100857 · Cited by 56 · see citing works
Self-citationRole of gonadal hormones in anxiety and fear memory formation and inhibition in male mice
McDermott, C. M., Liu, D., & Schrader, L. A. (2011) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.12.016 · Cited by 55 · see citing works
Zhang, W., & Rosenkranz, J. A. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.03.028 · Cited by 55 · see citing works
An Adolescent Sensitive Period for Threat Responding: Impacts of Stress and Sex
Gerhard, D. M., Meyer, H. C., & Lee, F. S. (2021) · Biological Psychiatry · doi:10.1016/j.biopsych.2020.10.003 · Cited by 54 · see citing works
Meitzen, J., Pflepsen, K. R., Stern, C. M., Meisel, R. L., & Mermelstein, P. G. (2010) · Neuroscience Letters · doi:10.1016/j.neulet.2010.10.017 · Cited by 54 · see citing works
Sadowski, R. N., Wise, L. M., Park, P. Y., Schantz, S. L., & Juraska, J. M. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.08.038 · Cited by 54 · see citing works
Self-citationMcDougall, S., Riad, W. V., Silva-Gotay, A., Tavares, E. R., Harpalani, D., Li, G., & Richardson, H. N. (2018) · eNeuro · doi:10.1523/eneuro.0203-18.2018 · Cited by 54 · see citing works
Social touch during development: Long-term effects on brain and behavior
Bales, K. L., Witczak, L. R., Simmons, T. C., Savidge, L. E., Rothwell, E. S., Rogers, F. D., Manning, R., Heise, M. J., Englund, M., & Razo, R. A. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.09.019 · Cited by 54 · see citing works
Yates, M. A., Markham, J. A., Anderson, S. E., Morris, J. R., & Juraska, J. M. (2008) · Brain Research · doi:10.1016/j.brainres.2008.04.055 · Cited by 53 · see citing works
Self-citationBarfield, E. T., & Gourley, S. L. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.10.015 · Cited by 53 · see citing works
Koss, W. A., Sadowski, R. N., Sherrill, L. K., Gulley, J. M., & Juraska, J. M. (2012) · Brain Research · doi:10.1016/j.brainres.2012.05.023 · Cited by 50 · see citing works
Self-citationvan den Bos, R., Davies, W., Dellu-Hagedorn, F., Goudriaan, A. E., Granon, S., Homberg, J. R., Rivalan, M., Swendsen, J. D., & Adriani, W. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.07.005 · Cited by 49 · see citing works
Age-dependent effects of repeated amphetamine exposure on working memory in rats
Sherrill, L. K., Stanis, J. J., & Gulley, J. M. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.12.044 · Cited by 49 · see citing works
Counotte, D. S., Li, K. W., Wortel, J., Gouwenberg, Y., Van Der Schors, R. C., Smit, A. B., & Spijker, S. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07404.x · Cited by 47 · see citing works
Brain structural and functional changes in adolescents with psychiatric disorders
Miguel-Hidalgo, J. J. (2013) · International Journal of Adolescent Medicine and Health · doi:10.1515/ijamh-2013-0058 · Cited by 45 · see citing works
Majcher‐Maślanka, I., Solarz, A., & Chocyk, A. (2019) · Neuroscience · doi:10.1016/j.neuroscience.2019.10.033 · Cited by 42 · see citing works
Sherrill, L. K., Koss, W. A., Foreman, E. S., & Gulley, J. M. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.08.048 · Cited by 40 · see citing works
Noorafshan, A., Hashemi, M., Karbalay‐Doust, S., & Karimi, F. (2018) · Acta Histochemica · doi:10.1016/j.acthis.2018.07.004 · Cited by 39 · see citing works
Delayed alternation in adolescent and adult male and female rats
Koss, W. A., Franklin, A. D., & Juraska, J. M. (2011) · Developmental Psychobiology · doi:10.1002/dev.20543 · Cited by 38 · see citing works
Self-citationTaylor, S. B., Taylor, A. R., & Koenig, J. I. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.09.045 · Cited by 38 · see citing works
Melbourne, J. K., Chandler, C. M., Van Doorn, C. E., Bardo, M. T., Pauly, J. R., Peng, H., & Nixon, K. (2021) · Alcoholism: Clinical and Experimental Research · doi:10.1111/acer.14694 · Cited by 37 · see citing works
Doherty, J. M., Cooke, B. M., & Frantz, K. J. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2012.200 · Cited by 37 · see citing works
Green, M. R., & McCormick, C. M. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.08.011 · Cited by 36 · see citing works
Kang, S., Cho, S., Na, K., Lee, J. S., Joo, S. W., Cho, S., Son, Y., & Lee, Y. J. (2020) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2020.111032 · Cited by 35 · see citing works
Wise, L., Sadowski, R. N., Kim, T., Willing, J., & Juraska, J. M. (2016) · NeuroToxicology · doi:10.1016/j.neuro.2016.01.011 · Cited by 33 · see citing works
Self-citationSexually dimorphic c-Fos expression following spatial working memory in young and adult rats
Méndez-López, M., Méndez, M., López, L., & Arias, J. L. (2009) · Physiology & Behavior · doi:10.1016/j.physbeh.2009.06.006 · Cited by 33 · see citing works
Hamilton, G. F., Hernandez, I. J., Krebs, C. P., Bucko, P. J., & Rhodes, J. S. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.03.058 · Cited by 33 · see citing works
- Authors
- Markham, J. A., Morris, J. R., & Juraska, J. M.
- Affiliations
- University of Illinois Urbana-Champaign (US)
- ORCID
- Juraska, J.M.
- Venue
- Neuroscience
- Publisher
- Elsevier BV
- Published
- 2007-02
- Volume
- 144
- Issue
- 3
- Pages
- 961-968
- ISSN
- 0306-4522 (ISSN-L)
- OpenAlex
- W2058932154
- Cited by
- 230
- References
- 51
- Citations by year
- 2026: 5 · 2025: 7 · 2024: 12 · 2023: 11 · 2022: 9 · 2021: 12 · 2020: 12 · 2019: 9 · 2018: 19 · 2017: 14 · 2016: 20 · 2015: 9 · 2014: 5 · 2013: 25 · 2012: 13
- FWCI
- 1.79
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD07333, T32HD007333)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- neuronal loss, ventromedial prefrontal cortex, dorsomedial prefrontal cortex, adolescence, adulthood, apoptosis, gray matter volume, glial cells, sex differences, postnatal development, rat brain
- MeSH terms
- Aging, Animals, Cell Count, Environment, Female, Male, Nerve Fibers, Myelinated, Neuroglia, Neuronal Plasticity, Neurons, Sex Characteristics, Cell Death, Prefrontal Cortex, Rats, Long-Evans, Cell Proliferation, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
