Abstract
Much evidence indicates that experiences in adolescence can alter the development of social behaviour. We previously demonstrated that male rats exposed to social instability stress in adolescence (SS; 1 h isolation and return to an unfamiliar cagemate daily from postnatal day [PND] 30–45) had reduced social interaction, impaired social recognition, reduced sexual performance, and increased aggression in competition for food reward compared with non-stressed control (CTL) rats. Here, we investigated whether SS affects stellate neuron morphology using the Golgi–Cox method and several markers of synaptic plasticity using western blotting in the medial amygdala (MeA) and lateral septum (LS), sites involved in social behaviour. On PND 46, 24 h after the last stress exposure, SS rats had increased dendritic arborisation, a greater number of dendrite terminals, and a higher average dendrite branch order in the anterodorsal MeA compared with CTL rats. SS rats had reduced dendritic arborization and a reduced total length of dendrite matter in the anteroventral MeA and a reduced number of dendrite terminals in the posterodorsal MeA compared with CTL rats. Moreover, SS rats had a reduced number of dendritic spines in the dorsal LS compared with CTL rats. SS rats had less synaptophysin in the MeA and more CaMKII in the LS than did CTL rats, and did not differ in spinophilin, PSD95, or glucocorticoid receptor protein expression in the MeA and LS. We discuss how changes in neural structure and in markers of synaptic plasticity the MeA and LS of adolescent SS rats compared with CTL rats may underlie their differences in social behaviour.
Similar content being viewed by others
References
Adekunbi DA, Li XF, Lass G, Shetty K, Adegoke OA, Yeo SH, Colledge WH, Lightman SL, O’byrne KT (2018). Kisspeptin neurones in the posterodorsal medial amygdala modulate sexual partner preference and anxiety in male mice. J Neuroendocrinol 30 (3):e12572
Allen PB, Ouimet CC, Greengard P (1997) Spinophilin, a novel protein phosphatase 1 binding protein localized to dendritic spines. Proc Natl Acad Sci 94(18):9956–9961
Arcego DM, Toniazzo AP, Krolow R, Lampert C, Berlitz C, dos Santos Garcia E, do Couto Nicola F, Hoppe JB, Gaelzer MM, Klein CP, Lazzaretti C (2018) Impact of high-fat diet and early stress on depressive-like behavior and Hippocampal plasticity in adult male rats. Mol Neurobiol 55(4):2740–2753
Bell HC, Pellis SM, Kolb B (2010) Juvenile peer play experience and the development of the orbitofrontal and medial prefrontal cortices. Behav Brain Res 207(1):7–13
Bennur S, Rao BS, Pawlak R, Strickland S, McEwen BS, Chattarji S (2007) Stress-induced spine loss in the medial amygdala is mediated by tissue-plasminogen activator. Neuroscience 144(1):8–16
Bialy M, Sachs BD (2002) Androgen implants in medial amygdala briefly maintain noncontact erection in castrated male rats. Horm Behav 42(3):345–355
Bredewold R, Smith CJ, Dumais KM, Veenema AH (2014) Sex-specific modulation of juvenile social play behavior by vasopressin and oxytocin depends on social context. Front Behav Neurosci 8:216
Burton CL, Chatterjee D, Chatterjee-Chakraborty M, Lovic V, Grella SL, Steiner M, Fleming AS (2007) Prenatal restraint stress and motherless rearing disrupts expression of plasticity markers and stress-induced corticosterone release in adult female Sprague–Dawley rats. Brain Res 1158:28–38
Cansler HL, Maksimova MA, Meeks JP (2017) Experience-dependent plasticity in accessory olfactory bulb interneurons following male-male social interaction. J Neurosci 28:1031–1037
Canteras NS, Simerly RB, Swanson LW (1995) Organization of projections from the medial nucleus of the amygdala: a PHAL study in the rat. J Comp Neurol 360(2):213–245
Chiba S, Numakawa T, Ninomiya M, Richards MC, Wakabayashi C, Kunugi H (2012) Chronic restraint stress causes anxiety-and depression-like behaviors, downregulates glucocorticoid receptor expression, and attenuates glutamate release induced by brain-derived neurotrophic factor in the prefrontal cortex. Prog Neuro-Psychopharmacol Biol Psychiatry 39(1):112–119
Cumming MJ, Thompson MA, McCormick CM (2014) Adolescent social instability stress increases aggression in a food competition task in adult male Long-Evans rats. Dev Psychobiol 56(7):1575–1588
Cádiz-Moretti B, Otero-García M, Martínez-García F, Lanuza E (2016) Afferent projections to the different medial amygdala subdivisions: a retrograde tracing study in the mouse. Brain Struct Funct 221(2):1033–1065
Dall’Oglio A, Gehlen G, Achaval M, Rasia-Filho AA (2008a) Dendritic branching features of posterodorsal medial amygdala neurons of adult male and female rats: further data based on the Golgi method. Neurosci Lett 430(2):151–156
Dall’Oglio A, Gehlen G, Achaval M, Rasia-Filho AA (2008b) Dendritic branching features of Golgi-impregnated neurons from the “ventral” medial amygdala subnuclei of adult male and female rats. Neurosci Lett 439(3):287–292
Dass SA, Vyas A (2014) Copulation or sensory cues from the female augment Fos expression in arginine vasopressin neurons of the posterodorsal medial amygdala of male rats. Front Zool 11(1):42
Dayas CV, Buller KM, Day TA (1999) Neuroendocrine responses to an emotional stressor: evidence for involvement of the medial but not the central amygdala. Eur J Neurosci 11(7):2312–2322
De Vries GJ, Buds RM, Swaab DF (1981) Ontogeny of the vasopressinergic neurons of the suprachiasmatic nucleus and their extrahypothalamic projections in the rat brain—presence of a sex difference in the lateral septum. Brain Res 218(1–2):67–78
Donato J Jr, Cavalcante JC, Silva RJ, Teixeira AS, Bittencourt JC, Elias CF (2010) Male and female odors induce Fos expression in chemically defined neuronal population. Physiol Behav 99(1):67–77
Eiland L, Ramroop J, Hill MN, Manley J, McEwen BS (2012) Chronic juvenile stress produces corticolimbic dendritic architectural remodeling and modulates emotional behavior in male and female rats. Psychoneuroendocrinology 37(1):39–47
Einon D, Potegal M (1991) Enhanced defense in adult rats deprived of playfighting experience as juveniles. Aggress Behav 17(1):27–40
Fischer M, Kaech S, Wagner U, Brinkhaus H, Matus A (2000) Glutamate receptors regulate actin-based plasticity in dendritic spines. Nat Neurosci 3(9):887–894
Fujiwara M, Nitta A, Chiba A (2016) Regulation of sexual odor preference by sex steroids in the posterodorsal medial amygdala in female rats. Horm Behav 82:46–55
Fukunaga K, Muller D, Miyamoto E (1996) CaM kinase II in long-term potentiation. Neurochem Int 28(4):343–358
Gibb R, Kolb B (1998) A method for vibratome sectioning of Golgi–Cox stained whole rat brain. J Neurosci Methods 79(1):1–4
Green MR, Barnes B, McCormick CM (2013) Social instability stress in adolescence increases anxiety and reduces social interactions in adulthood in male Long–Evans rats. Dev Psychobiol 55(8):849–859
Guzmán YF, Tronson NC, Jovasevic V, Sato K, Guedea AL, Mizukami H, Nishimori K, Radulovic J (2013) Fear-enhancing effects of septal oxytocin receptors. Nat Neurosci 16(9):1185
He J, Crews FT (2007) Neurogenesis decreases during brain maturation from adolescence to adulthood. Pharmacol Biochem Behav 86(2):327–333
Herman JP, Ostrander MM, Mueller NK, Figueiredo H (2005) Limbic system mechanisms of stress regulation: hypothalamo-pituitary-adrenocortical axis. Prog Neuro-Psychopharmacol Biol Psychiatry 29(8):1201–1213
Hines M, Allen LS, Gorski RA (1992) Sex differences in subregions of the medial nucleus of the amygdala and the bed nucleus of the stria terminalis of the rat. Brain Res 579(2):321–326
Hodges TE, McCormick CM (2015) Adolescent and adult male rats habituate to repeated isolation, but only adolescents sensitize to partner unfamiliarity. Horm Behav 69:16–30
Hodges TE, McCormick CM (2019) Stress and social development in adolescence in a rodent model. Chapter in OC. In: Schultheiss, Mehta P (eds) International handbook of social neuroendocrinology. Taylor & Francis, Routledge, pp 479–503
Hodges TE, Baumbach JL, Marcolin ML, Bredewold R, Veenema AH, McCormick CM (2017) Social instability stress in adolescent male rats reduces social interaction and social recognition performance and increases oxytocin receptor binding. Neuroscience 359:172–182
Hodges TE, Baumbach JL, McCormick CM (2018) Predictors of social instability stress effects on social interaction and anxiety in adolescent male rats. Dev Psychobiol 60(6):1–13
Hosokawa N, Chiba A (2005) Effects of sexual experience on conspecific odor preference and estrous odor-induced activation of the vomeronasal projection pathway and the nucleus accumbens in male rats. Brain Res 1066(1–2):101–108
Hosokawa N, Chiba A (2010) Androgen receptor blockade in the posterodorsal medial amygdala impairs sexual odor preference in male rats. Horm Behav 58(3):493–500
Iñiguez SD, Aubry A, Riggs LM, Alipio JB, Zanca RM, Flores-Ramirez FJ, Hernandez MA, Nieto SJ, Musheyev D, Serrano PA (2016) Social defeat stress induces depression-like behavior and alters spine morphology in the hippocampus of adolescent male C57BL/6 mice. Neurobiol Stress 5:54–64
Kalman E, Keay KA (2017) Hippocampal volume, social interactions, and the expression of the normal repertoire of resident–intruder behavior. Brain Behav 7(9):e00775
Kang N, Baum MJ, Cherry JA (2009) A direct main olfactory bulb projection to the ‘vomeronasal’amygdala in female mice selectively responds to volatile pheromones from males. Eur J Neurosci 29(3):624–634
Kellogg CK, Awatramani GB, Piekut DT (1998) Adolescent development alters stressor-induced Fos immunoreactivity in rat brain. Neuroscience 83(3):681–689
Kennedy MB (1998) Signal transduction molecules at the glutamatergic postsynaptic membrane. Brain Res Rev 26(2–3):243–257
Kim KC, Kim P, Go HS, Choi CS, Park JH, Kim HJ, Jeon SJ, dela Pena IC, Han SH, Cheong JH, Ryu JH (2013) Male-specific alteration in excitatory post-synaptic development and social interaction in pre-natal valproic acid exposure model of autism spectrum disorder. J Neurochem 124(6):832–843
Kim H, Yi JH, Choi K, Hong S, Shin KS, Kang SJ (2014) Regional differences in acute corticosterone-induced dendritic remodeling in the rat brain and their behavioral consequences. BMC Neurosci 15(1):65
Knapska E, Radwanska K, Werka T, Kaczmarek L (2007) Functional internal complexity of amygdala: focus on gene activity mapping after behavioral training and drugs of abuse. Physiol Rev 87(4):1113–1173
Koss WA, Belden CE, Hristov AD, Juraska JM (2014) Dendritic remodeling in the adolescent medial prefrontal cortex and the basolateral amygdala of male and female rats. Synapse 68(2):61–72
Lau T, Bigio B, Zelli D, McEwen BS, Nasca C (2017) Stress-induced structural plasticity of medial amygdala stellate neurons and rapid prevention by a candidate antidepressant. Mol Psychiatry 22(2):227
Leite-Morris KA, Kobrin KL, Guy MD, Young AJ, Heinrichs SC, Kaplan GB (2014) Extinction of opiate reward reduces dendritic arborization and c-Fos expression in the nucleus accumbens core. Behav Brain Res 263:51–59
Leussis MP, Andersen SL (2008) Is adolescence a sensitive period for depression? Behavioral and neuroanatomical findings from a social stress model. Synapse 62(1):22–30
Leussis MP, Lawson K, Stone K, Andersen SL (2008) The enduring effects of an adolescent social stressor on synaptic density, part II: Poststress reversal of synaptic loss in the cortex by adinazolam and MK-801. Synapse 62(3):185–192
Lisman JE, Zhabotinsky AM (2001) A model of synaptic memory: a CaMKII/PP1 switch that potentiates transmission by organizing an AMPA receptor anchoring assembly. Neuron 31(2):191–201
Lukas M, Toth I, Veenema AH, Neumann ID (2013) Oxytocin mediates rodent social memory within the lateral septum and the medial amygdala depending on the relevance of the social stimulus: male juvenile versus female adult conspecifics. Psychoneuroendocrinology 38(6):916–926
Lukkes JL, Mokin MV, Scholl JL, Forster GL (2009) Adult rats exposed to early-life social isolation exhibit increased anxiety and conditioned fear behavior, and altered hormonal stress responses. Horm Behav 55(1):248–256
Maras PM, Molet J, Chen Y, Rice C, Ji SG, Solodkin A, Baram TZ (2014) Preferential loss of dorsal-hippocampus synapses underlies memory impairments provoked by short, multimodal stress. Mol Psychiatry 19(7):811
Maras PM, Petrulis A (2010a) Anatomical connections between the anterior and posterodorsal sub-regions of the medial amygdala: integration of odor and hormone signals. Neuroscience 170(2):610–622
Maras PM, Petrulis A (2010b) Lesions that functionally disconnect the anterior and posterodorsal sub-regions of the medial amygdala eliminate opposite-sex odor preference in male Syrian hamsters (Mesocricetus auratus). Neuroscience 165(4):1052–1062
Marcuzzo S, Dall’Oglio A, Ribeiro MF, Achaval M, Rasia-Filho AA (2007) Dendritic spines in the posterodorsal medial amygdala after restraint stress and ageing in rats. Neurosci Lett 424(1):16–21
Markham JA, Morris JR, Juraska JM (2007) Neuron number decreases in the rat ventral, but not dorsal, medial prefrontal cortex between adolescence and adulthood. Neuroscience 144(3):961–968
Maroun M, Wagner S (2016) Oxytocin and memory of emotional stimuli: some dance to remember, some dance to forget. Biol Psychiatry 79(3):203–212
Martinez M, Phillips PJ, Herbert J (1998) Adaptation in patterns of c-fos expression in the brain associated with exposure to either single or repeated social stress in male rats. Eur J Neurosci 10(1):20–33
Mathews IZ, Wilton A, Styles A, McCormick CM (2008) Increased depressive behaviour in females and heightened corticosterone release in males to swim stress after adolescent social stress in rats. Behav Brain Res 190(1):33–40
Mattison HA, Popovkina D, Kao JP, Thompson SM (2014) The role of glutamate in the morphological and physiological development of dendritic spines. Eur J Neurosci 39(11):1761–1770
McCormick CM (2010) An animal model of social instability stress in adolescence and risk for drugs of abuse. Physiol Behav 99(2):194–203
McCormick CM, Cameron NM, Thompson MA, Cumming MJ, Hodges TE, Langett M (2017) The sexual preference of female rats is influenced by males’ adolescent social stress history and social status. Horm Behav 89:30–37
McCormick CM, Green MR, Cameron NM, Nixon F, Levy MJ, Clark RA (2013) Deficits in male sexual behavior in adulthood after social instability stress in adolescence in rats. Horm Behav 63(1):5–12
McCormick CM, Hodges TE, Simone JJ (2015) Peer pressures: Social instability stress in adolescence and social deficits in adulthood in a rodent model. Dev Cognit Neurosci 11:2–11
McCormick CM, Merrick A, Secen J, Helmreich DL (2007) Social instability in adolescence alters the central and peripheral hypothalamic-pituitary-adrenal responses to a repeated homotypic stressor in male and female rats. J Neuroendocrinol 19(2):116–126
McCormick CM, Robarts D, Kopeikina K, Kelsey JE (2005) Long-lasting, sex-and age-specific effects of social stressors on corticosterone responses to restraint and on locomotor responses to psychostimulants in rats. Horm Behav 48(1):64–74
McCormick CM, Smith C, Mathews IZ (2008) Effects of chronic social stress in adolescence on anxiety and neuroendocrine response to mild stress in male and female rats. Behav Brain Res 187(2):228–238
McCormick CM, Thomas CM, Sheridan CS, Nixon F, Flynn JA, Mathews IZ (2012) Social instability stress in adolescent male rats alters hippocampal neurogenesis and produces deficits in spatial location memory in adulthood. Hippocampus 22(6):1300–1312
McEwen BS, Nasca C, Gray JD (2016) Stress effects on neuronal structure: hippocampus, amygdala, and prefrontal cortex. Neuropsychopharmacology 41(1):3
Meredith M, Westberry JM (2004) Distinctive responses in the medial amygdala to same-species and different-species pheromones. J Neurosci 24(25):5719–5725
Mizoguchi K, Ishige A, Aburada M, Tabira T (2003) Chronic stress attenuates glucocorticoid negative feedback: involvement of the prefrontal cortex and hippocampus. Neuroscience 119(3):887–897
Mizukami S, Nishizuka M, Arai Y (1983) Sexual difference in nuclear volume and its ontogeny in the rat amygdala. Exp Neurol 79(2):569–575
Mohedano-Moriano A, Pro-Sistiaga P, Úbeda-Bañón I, Crespo C, Insausti R, Martinez-Marcos A (2007) Segregated pathways to the vomeronasal amygdala: differential projections from the anterior and posterior divisions of the accessory olfactory bulb. Eur J Neurosci 25(7):2065–2080
Monnerie H, Shashidhara S, Le Roux PD (2003) Effect of excess extracellular glutamate on dendrite growth from cerebral cortical neurons at 3 days in vitro: Involvement of NMDA receptors. J Neurosci Res 74(5):688–700
Navone F, Jahn R, Di Gioia G, Stukenbrok H, Greengard P, De Camilli P (1986) Protein p38: an integral membrane protein specific for small vesicles of neurons and neuroendocrine cells. J Cell Biol 103(6):2511–2527
Newman SW (1999) The medial extended amygdala in male reproductive behavior a node in the mammalian social behavior network. Ann New York Acad Sci 877(1):242–257
O’connell LA, Hofmann HA (2011) The vertebrate mesolimbic reward system and social behavior network: a comparative synthesis. J Comp Neurol 519(18):3599–3639
Padival MA, Blume SR, Vantrease JE, Rosenkranz JA (2015) Qualitatively different effect of repeated stress during adolescence on principal neuron morphology across lateral and basal nuclei of the rat amygdala. Neuroscience 291:128–145
Padival M, Quinette D, Rosenkranz JA (2013) Effects of repeated stress on excitatory drive of basal amygdala neurons in vivo. Neuropsychopharmacology 38(9):1748
Paxinos G, Watson C (2005) The rat brain in stereotaxic coordinates. Elsevier, Sydney
Pellis SM, Pellis VC (2017) What is play fighting and what is it good for? Learn Behav 45(4):355–366
Pellis SM, Pellis VC, Himmler BT (2014) How play makes for a more adaptable brain: A comparative and neural perspective. Am J Play 7(1):73
Phelan KD, Hasuo H, Twery MJ, Gallagher JP (1989) Projection neurons in the rat dorsolateral septal nucleus possess recurrent axon collaterals. Neurosci Lett 97(3):259–265
Pro-Sistiaga P, Mohedano-Moriano A, Ubeda-Bañon I, del mar Arroyo-Jimenez M, Marcos P, Artacho-Pérula E, Crespo C, Insausti R, Martinez-Marcos A (2007) Convergence of olfactory and vomeronasal projections in the rat basal telencephalon. J Comp Neurol 504(4):346–362
Radley JJ, Morrison JH (2005) Repeated stress and structural plasticity in the brain. Ageing Res Rev 4(2):271–287
Sano K, Nakata M, Musatov S, Morishita M, Sakamoto T, Tsukahara S, Ogawa S (2016) Pubertal activation of estrogen receptor α in the medial amygdala is essential for the full expression of male social behavior in mice. Proc Natl Acad Sci 113(27):7632–7637
Scordalakes EM, Shetty SJ, Rissman EF (2002) Roles of estrogen receptor α and androgen receptor in the regulation of neuronal nitric oxide synthase. J Comp Neurol 453(4):336–344
Shahar-Gold H, Gur R, Wagner S (2013) Rapid and reversible impairments of short-and long-term social recognition memory are caused by acute isolation of adult rats via distinct mechanisms. PloS One 8(5):e65085
Sheehan TP, Chambers RA, Russell DS (2004) Regulation of affect by the lateral septum: implications for neuropsychiatry. Brain Res Rev 46(1):71–117
Sisk CL (2016) Hormone-dependent adolescent organization of socio-sexual behaviors in mammals. Curr Opin Neurobiol 38:63–68
Solomon MB, Jones K, Packard BA, Herman JP (2010) The medial amygdala modulates body weight but not neuroendocrine responses to chronic stress. J Neuroendocrinol 22(1):13–23
Tata DA, Anderson BJ (2010) The effects of chronic glucocorticoid exposure on dendritic length, synapse numbers and glial volume in animal models: implications for hippocampal volume reductions in depression. Physiol Behav 99(2):186–193
Tran TT, Srivareerat M, Alhaider IA, Alkadhi KA (2011) Chronic psychosocial stress enhances long-term depression in a subthreshold amyloid-beta rat model of Alzheimer’s disease. J Neurochem 119(2):408–416
Tripathi SJ, Chakraborty S, Srikumar BN, Raju TR, Rao BS (2018) Prevention of chronic immobilization stress-induced enhanced expression of glucocorticoid receptors in the prefrontal cortex by inactivation of basolateral amygdala. J Chem Neuroanat.( EPub ahead of print)
Tsai SF, Huang TY, Chang CY, Hsu YC, Chen SJ, Yu L, Kuo YM, Jen CJ (2014) Social instability stress differentially affects amygdalar neuron adaptations and memory performance in adolescent and adult rats. Front Behav Neurosci 8:27
Tseng CY, Firestein BL (2011) The role of PSD-95 and cypin in morphological changes in dendrites following sublethal NMDA exposure. J Neurosci 31(43):15468–15480
Tulogdi Á, Tóth M, Barsvári B, Biró L, Mikics É, Haller J (2014) Effects of resocialization on post-weaning social isolation-induced abnormal aggression and social deficits in rats. Dev Psychobiol 56(1):49–57
Unger EK, Burke KJ, Yang CF, Bender KJ, Fuller PM, Shah NM (2015) Medial amygdalar aromatase neurons regulate aggression in both sexes. Cell Rep 10(4):453–462
van den Berg CL, Hol T, Van Ree JM, Spruijt BM, Everts H, Koolhaas JM (1999) Play is indispensable for an adequate development of coping with social challenges in the rat. Dev Psychobiol 34(2):129–138
Veenema AH, Bredewold R, De Vries GJ (2012) Vasopressin regulates social recognition in juvenile and adult rats of both sexes, but in sex-and age-specific ways. Horm Behav 61(1):50–56
Veenema AH, Neumann ID (2008) Central vasopressin and oxytocin release: regulation of complex social behaviours. Prog Brain Res 170:261–276
Veening JG, Coolen LM, de Jong TR, Joosten HW, de Boer SF, Koolhaas JM, Olivier B (2005) Do similar neural systems subserve aggressive and sexual behaviour in male rats? Insights from c-Fos and pharmacological studies. Eur J Pharmacol 526(1–3):226–239
Verney C, Gaspar P, Alvarez C, Berger B (1987) Postnatal sequential development of dopaminergic and enkephalinergic perineuronal formations in the lateral septal nucleus of the rat correlated with local neuronal maturation. Anat Embryol 176(4):463–475
Wall VL, Fischer EK, Bland ST (2012) Isolation rearing attenuates social interaction-induced expression of immediate early gene protein products in the medial prefrontal cortex of male and female rats. Physiol Behav 107(3):440–450
Wiedenmann B, Franke WW, Kuhn C, Moll R, Gould VE (1986) Synaptophysin: a marker protein for neuroendocrine cells and neoplasms. Proc Natl Acad Sci 83(10):3500–3504
Willing J, Juraska JM (2015) The timing of neuronal loss across adolescence in the medial prefrontal cortex of male and female rats. Neuroscience 301:268–275
Xu H, He J, Richardson JS, Li XM (2004) The response of synaptophysin and microtubule-associated protein 1 to restraint stress in rat hippocampus and its modulation by venlafaxine. J Neurochem 91(6):1380–1388
Zoicas I, Slattery DA, Neumann ID (2014) Brain oxytocin in social fear conditioning and its extinction: involvement of the lateral septum. Neuropsychopharmacology 39:3027–3035
Zoladz PR, Park CR, Halonen JD, Salim S, Alzoubi KH, Srivareerat M, Fleshner M, Alkadhi KA, Diamond DM (2012) Differential expression of molecular markers of synaptic plasticity in the hippocampus, prefrontal cortex, and amygdala in response to spatial learning, predator exposure, and stress-induced amnesia. Hippocampus 22(3):577–589
Acknowledgements
CMM holds a Natural Sciences and Engineering Research Council (NSERC) Discovery Grant that supported the research. TEH holds a NSERC graduate scholarship. The authors have no conflicts of interest to declare.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Hodges, T.E., Louth, E.L., Bailey, C.D.C. et al. Adolescent social instability stress alters markers of synaptic plasticity and dendritic structure in the medial amygdala and lateral septum in male rats. Brain Struct Funct 224, 643–659 (2019). https://doi.org/10.1007/s00429-018-1789-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00429-018-1789-8