Abstract
The hippocampal complex of birds is a narrow-curved strip of tissue that plays a crucial role in learning, memory, spatial navigation, and emotional and sexual behavior. This study was conducted to evaluate the effect of unpredictable chronic mild stress in multipolar neurons of 3-, 5-, 7-, and 9-week-old chick’s hippocampal complex. This study revealed that chronic stress results in neuronal remodeling by causing alterations in dendritic field, axonal length, secondary branching, corrected spine number, and dendritic branching at 25, 50, 75, and 100 µm. Due to stress, the overall dendritic length was significantly retracted in 3-week-old chick, whereas no significant difference was observed in 5- and 7-week-old chick, but again it was significantly retracted in 9-week-old chick along with the axonal length. So, this study indicates that during initial days of stress exposure, the dendritic field shows retraction, but when the stress continues up to a certain level, the neurons undergo structural modifications so that chicks adapt and survive in stressful conditions. The repeated exposure to chronic stress for longer duration leads to the neuronal structural disruption by retraction in the dendritic length as well as axonal length. Another characteristic which leads to structural alterations is the dendritic spines which significantly decreased in all age groups of stressed chicks and eventually leads to less synaptic connections, disturbance in physiology, and neurology, which affects the learning, memory, and coping ability of an individual.
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The authors have shared new data in this research article. The data that support the findings of this study are available on request from the corresponding author. The data are not publicly available due to privacy or ethical restrictions.
References
Atoji Y, Wild JM (2006) Anatomy of the avian hippocampal formation. Rev Neurosci 17:3–15. https://doi.org/10.1515/REVNEURO.2006.17.1-2.3
Atoji Y, Yamamoto Y, Suzuki Y (2001) Distribution of NADPH diaphorase-containing neurons in the pigeon central nervous system. J Chem Neuroanat 21:1–22. https://doi.org/10.1016/S0891-0618(00)00103-4
Atoji Y, Martin Wild J, Yamamoto Y, Suzuki Y (2002) Intratelencephalic connections of the hippocampus in pigeons (Columba livia). J Comp Neurol 447:177–199. https://doi.org/10.1002/cne.10239
Bingman VP, Yates G (1992) Hippocampal lesions impair navigational learning in experienced homing pigeons. Behav Neurosci 106:229–232. https://doi.org/10.1037/0735-7044.106.1.229
Bingman VP, Bagnoli P, Ioale P, Casini G (1989) Behavioral and anatomical studies of the avian hippocampus. Neurol Neurobiol 52:379–394
Bingman VP, Gagliardo A, Hough GE et al (2005) The avian hippocampus, homing in pigeons and the memory representation of large-scale space. Integr Comp Biol 45:555–564. https://doi.org/10.1093/icb/45.3.555
Bliss TVP, Lomo T (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the unanaesthetized rabbit following stimulation of the perforant path. J Physiol 232:357–374. https://doi.org/10.1113/jphysiol.1973.sp010274
Campbell CBG, Hodos W (1970) The concept of homology and the evolution of the nervous system. Brain Behav Evol 3:353–367. https://doi.org/10.1159/000125482
Casini G, Fontanesi G, Bingman VP et al (1997) The neuroethology of cognitive maps: Contributions from research on the hippocampus and homing pigeon navigation. Arch Ital Biol 135:73–92
Chand P, Srivastava UC (2010) Morphological characteristics of the projection neurons in the hyperpallium apicale of the strawberry finch Estrilda amandava. Natl Acad Sci Lett 33:377–382
Chand P, Maurya RC, Srivastava UC (2013) Neuronal morphology and spine density of the visual wulst of the strawberry finch, estrilda amandava. Proc Natl Acad Sci India Sect B-Biol Sci 83:627–642. https://doi.org/10.1007/s40011-013-0188-4
Conrad CD, LeDoux JE, Magariños AM, McEwen BS (1999) Repeated restraint stress facilitates fear conditioning independently of causing hippocampal CA3 dendritic atrophy. Behav Neurosci 113:902–913. https://doi.org/10.1037/0735-7044.113.5.902
Craigie EH (1930) Studies on the brain of the kiwi (Apteryx australis). J Comp Neurol 49:223–357. https://doi.org/10.1002/cne.900490202
Craigie EH (1934) The hippocampal and parahippocajipal. J Comp Neurol 61:563
Das G, Reuhl K (2013) The golgi-cox method. Neural Dev Methods Protoc Methods Mol Biol 1018:313–321. https://doi.org/10.1007/978-1-62703-444-9_29
Einat H, Kronfeld-Schor N, Eilam D (2006) Sand rats see the light: short photoperiod induces a depression-like response in a diurnal rodent. Behav Brain Res 173:153–157. https://doi.org/10.1016/j.bbr.2006.06.006
Feldman ML, Peters A (1979) A technique for estimating total spine numbers on golgi-impregnated dendrites. J Comp Neurol 188:527–542. https://doi.org/10.1002/cne.901880403
Fosser NS, Brusco A, Ríos H (2005) Darkness induced neuroplastic changes in the serotoninergic system of the chick retina. Dev Brain Res 160:211–218. https://doi.org/10.1016/j.devbrainres.2005.09.007
Frisone DF, Frye CA, Zimmerberg B (2002) Social isolation stress during the third week of life has age-dependent effects on spatial learning in rats. Behav Brain Res 128:153–160. https://doi.org/10.1016/S0166-4328(01)00315-1
Golgi C (1873) Sulla sostanza grigia del cervello. Gazz Med Ital Lomb 6:244–246
Goodson JL, Evans AK, Lindberg L (2004) Chemoarchitectonic subdivisions of the songbird septum and a comparative overview of septum chemical anatomy in jawed vertebrates. J Comp Neurol 473:293–314. https://doi.org/10.1002/cne.20061
Gualtieri F, Armstrong EA, Longmoor GK et al (2019) Unpredictable chronic mild stress suppresses the incorporation of new neurons at the caudal pole of the chicken hippocampal formation. Sci Rep 9:1–13. https://doi.org/10.1038/s41598-019-43584-x
Horner CH, Arbuthnott E (1991) Methods of estimation of spine density–are spines evenly distributed throughout the dendritic field? J Anat 177:179–184
Kaleta EF, Redmann T (2008) Approaches to determine the sex prior to and after incubation of chicken eggs and of day-old chicks. Worlds Poult Sci J 64:391–399. https://doi.org/10.1017/S0043933908000111
Kallen B (1962) II. Embryogenesis of brain nuclei in the chick telencephalon. Ergeb Anat Entwicklungsgesch 36:62–82
Kanamori T, Togashi K, Koizumi H, Emoto K (2015) Dendritic Remodeling: Lessons from Invertebrate Model Systems. Elsevier Ltd
Karssen AM, Meijer OC, Berry A et al (2005) Low doses of dexamethasone can produce a hypocorticosteroid state in the brain. Endocrinology 146:5587–5595. https://doi.org/10.1210/en.2005-0501
Kerr DS, Campbell LW, Applegate MD et al (1991) Chronic stress-induced acceleration of electrophysiologic and morphometric biomarkers of hippocampal aging. J Neurosci 11:1316–1324. https://doi.org/10.1523/jneurosci.11-05-01316.1991
Krebs JR, Sherry DF, Healy SD et al (1989) Hippocampal specialization of food-storing birds. Proc Natl Acad Sci U S A 86:1388–1392. https://doi.org/10.1073/pnas.86.4.1388
Kumar A, Arya H, Tamta K, Maurya RC (2021) Acute stress-induced neuronal plasticity in the corticoid complex of 15-day-old chick, Gallus domesticus. J Anat 239:869–891. https://doi.org/10.1111/joa.13483
Kumar A, Tamta K, Arya H, Maurya RC (2023) Acute-stress induces the structural plasticity in hippocampal neurons of 15 and 30-day-old chick. Gallus Gallus Domest Ann Anat 245:151996. https://doi.org/10.1016/j.aanat.2022.151996
Lambert KG, Buckelew SK, Staffiso-Sandoz G et al (1998) Activity-stress induces atrophy of apical dendrites of hippocampal pyramidal neurons in male rats. Physiol Behav 65:43–49. https://doi.org/10.1016/S0031-9384(98)00114-0
Law AJ, Ph D, Weickert CS et al (2004) Reduced spinophilin but not microtubule-associated protein 2 expression in the hippocampal formation in schizophrenia and mood disorders : molecular evidence for a pathology of dendritic spines. AJP 161:1848–1855
Leuner B, Shors TJ (2004) New spines, new memories benedetta leuner and tracey. J Shors 29:117–130
Leuner B, Caponiti JM, Gould E (2012) Oxytocin stimulates adult neurogenesis even under conditions of stress and elevated glucocorticoids. Hippocampus 22:861–868. https://doi.org/10.1002/hipo.20947
Levine ND, Rademacher DJ, Collier TJ et al (2013) Advances in thin tissue Golgi-Cox impregnation: fast, reliable methods for multi-assay analyses in rodent and non-human primate brain. J Neurosci Methods 213:214–227. https://doi.org/10.1016/j.jneumeth.2012.12.001
Lipkind D, Nottebohm F, Rado R, Barnea A (2002) Social change affects the survival of new neurons in the forebrain of adult songbirds. Behav Brain Res 133:31–43. https://doi.org/10.1016/S0166-4328(01)00416-8
Liston C, Gan WB (2011) Glucocorticoids are critical regulators of dendritic spine development and plasticity in vivo. Proc Natl Acad Sci U S A 108:16074–16079. https://doi.org/10.1073/pnas.1110444108
Ma S, Ter MA, Gahr M (2017) Power-law scaling of calling dynamics in zebra finches. Sci Rep 7:1–11. https://doi.org/10.1038/s41598-017-08389-w
Magarin ̃os AM, McEwen BS, (1995) Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: comparison of stressors. Neuroscience 69:83–88. https://doi.org/10.1016/0306-4522(95)00256-I
Magariños AM, McEwen BS, Flügge G, Fuchs E (1996) Chronic psychosocial stress causes apical dendritic atrophy of hippocampal CA3 pyramidal neurons in subordinate tree shrews. J Neurosci 16:3534–3540. https://doi.org/10.1523/jneurosci.16-10-03534.1996
Mahmmoud RR, Sase S, Aher YD et al (2015) Spatial and working memory is linked to spine density and mushroom spines. PLoS ONE. https://doi.org/10.1371/journal.pone.0139739
McEwen BS (1998) Protective and damaging effects of stress mediators. N Engl J Med 338:171–179. https://doi.org/10.1056/nejm199801153380307
McEwen BS (1999) Stress and hippocampal plasticity. Annu Rev Neurosci 22:105–122. https://doi.org/10.1146/annurev.neuro.22.1.105
McEwen BS (2006) Protective and damaging effects of stress mediators: central role of the brain. Dialog Clin Neurosci 8:367–381. https://doi.org/10.31887/dcns.2006.8.4/bmcewen
McEwen BS (2007) Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol Rev 87:873–904. https://doi.org/10.1152/physrev.00041.2006
McEwen BS, Chattarji S (2004) Molecular mechanisms of neuroplasticity and pharmacological implications: the example of tianeptine. Eur Neuropsychopharmacol 14:497–502. https://doi.org/10.1016/j.euroneuro.2004.09.008
McEwen BS, Wingfield JC (2003) The concept of allostasis in biology and biomedicine. Horm Behav 43:2–15. https://doi.org/10.1016/S0018-506X(02)00024-7
McEwen BS, Bowles NP, Gray JD et al (2015) Mechanisms of stress in the brain. Nat Neurosci 18:1353–1363. https://doi.org/10.1038/nn.4086
Mcewen BS, Gianaros PJ (2010) Central role of the brain in stress and adaptation: Links to socioeconomic status, health, and disease. Ann N Y Acad Sci 1186:190–222. https://doi.org/10.1111/j.1749-6632.2009.05331.x
McKittrick CR, Magariños AM, Blanchard DC et al (2000) Chronic social stress reduces dendritic arbors in CA3 of hippocampus and decreases binding to serotonin transporter sites. Synapse 36:85
Mendelson SD, McKittrick CR, McEwen BS (1993) Autoradiographic analyses of the effects of estradiol benzoate on [3H]paroxetine binding in the cerebral cortex and dorsal hippocampus of gonadectomized male and female rats. Brain Res 601:299–302. https://doi.org/10.1016/0006-8993(93)91724-7
Molla R, Rodriguez J, Calvet S, Garcia-Verdugo JM (1986) Neuronal types of the cerebral cortex of the adult chicken (Gallus gallus). A Golgi Study J Hirnforsch 27:381–390
Montagnese CM, Krebs JR, Meyer G (1996) The dorsomedial and dorsolateral forebrain of the zebra finch, Taeniopygia guttata: a Golgi study. Cell Tissue Res 283:263–282. https://doi.org/10.1007/s004410050537
Mujahid A, Furuse M (2009) Behavioral responses of neonatal chicks exposed to low environmental temperature. Poult Sci 88:917–922. https://doi.org/10.3382/ps.2008-00472
Ojha K, Singh KP (2021) Neuronal diversity, dendro-spinous characterization in the hippocampal complex of Coracias benghalensis. J Appl Biol Biotechnol 9:112–116. https://doi.org/10.7324/JABB.2021.9415
Patel D, Anilkumar S, Chattarji S, Buwalda B (2018) Repeated social stress leads to contrasting patterns of structural plasticity in the amygdala and hippocampus. Behav Brain Res 347:314–324. https://doi.org/10.1016/j.bbr.2018.03.034
Radley JJ, Sisti HM, Hao J et al (2004) Chronic behavioral stress induces apical dendritic reorganization in pyramidal neurons of the medial prefrontal cortex. Neuroscience 125:1–6. https://doi.org/10.1016/j.neuroscience.2004.01.006
Rall W (1978) Dendritic spines and synaptic potency. Stud Neurophysiol Cambridge Univ Press Cambridge 3:203–209
Robertson BA, Rathbone L, Cirillo G et al (2017) Food restriction reduces neurogenesis in the avian hippocampal formation. PLoS ONE 12:1–19. https://doi.org/10.1371/journal.pone.0189158
Roth TC, Stocker K, Mauck R (2016) Morphological changes in hippocampal cytoarchitecture as a function of spatial treatment in birds. Dev Neurobiol 77:93–101. https://doi.org/10.1002/dneu.22413
Seeman T, Epel E, Gruenewald T et al (2010) Socio-economic differentials in peripheral biology: cumulative allostatic load. Ann N Y Acad Sci 1186:223–239. https://doi.org/10.1111/j.1749-6632.2009.05341.x
Sousa N, Lukoyanov NV, Madeira MD et al (2000) Reorganization of the morphology of hippocampal neurites and synapses after stress-induced damage correlates with behavioral improvement. Neuroscience 97:253–266. https://doi.org/10.1016/S0306-4522(00)00050-6
Srivastava UC, Chand P, Maurya RC (2007) Cytoarchitectonic organization and morphology of the cells of hippocampal complex in strawberry finch, Estrilda amandava. Cell Mol Biol 53:103–120. https://doi.org/10.1170/T824
Srivastava UC, Chand P, Maurya RC (2009) Neuronal classes in the corticoid complex of the telencephalon of the strawberry finch, Estrilda amandava. Cell Tissue Res 336:393–409. https://doi.org/10.1007/s00441-009-0790-1
Srivastava UC, Singh D, Kumar P (2014) Neuronal classes and their specialization in the corticoid complex of a food-storing bird, the Indian House Crow (Corvus splendens). Can J Zool 92:423–432. https://doi.org/10.1139/cjz-2013-0116
Sterling P, Eyer J (1988) Allostasis: A New Paradigm to Explain Arousal Pathology. In: Handbook of Life Stress, Cognition and Health. pp 629–639
Sunanda RMS, Raju TR (1995) Effect of chronic restraint stress on dendritic spines and excrescences of hippocampal CA3 pyramidal neurons-a quantitative study. Brain Res 694:312–317. https://doi.org/10.1016/0006-8993(95)00822-8
Székely AD, Krebs JR (1996) Efferent connectivity of the hippocampal formation of the zebra finch (Taenopygia guttata): an anterograde pathway tracing study using Phaseolus vulgaris leucoagglutinin. J Comp Neurol 368:198–214. https://doi.org/10.1002/(SICI)1096-9861(19960429)368:2%3c198::AID-CNE3%3e3.0.CO;2-Z
Tömböl T, Davies DC, Németh A et al (2000a) A comparative Golgi study of chicken (Gallus domesticus) and homing pigeon (Columba livia) hippocampus. Anat Embryol (berl) 201:85–101. https://doi.org/10.1007/PL00008235
Tömböl T, Davies DC, Németh A et al (2000b) A Golgi and a combined Golgi/GABA immunogold study of local circuit neurons in the homing pigeon hippocampus. Anat Embryol (berl) 201:181–196. https://doi.org/10.1007/s004290050017
Tracy AL, Jarrard LE, Davidson TL (2001) The hippocampus and motivation revisited: Appetite and activity. Behav Brain Res 127:13–23. https://doi.org/10.1016/S0166-4328(01)00364-3
von Bohlen und Halbach O, (2009) Structure and function of dendritic spines within the hippocampus. Ann Anat 191:518–531. https://doi.org/10.1016/j.aanat.2009.08.006
Watanabe Y, Gould E, Daniels DC et al (1992) Tianeptine attenuates stress-induced morphological changes in the hippocampus. Eur J Pharmacol 222:157–162. https://doi.org/10.1016/0014-2999(92)90830-W
Acknowledgements
The authors acknowledge the Head of the Department of Zoology, Soban Singh Jeena, University Almora, and Kumaun University, Nainital for the support during the experiment. The authors also thank the Institutional Animal Ethical Committee (IAEC) of Kumaun University, Nainital for approving the research work.
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Hemlata Arya contributed to investigation, methodology, visualization, writing – original draft preparation, and writing – review and editing. Kavita Tamta and Adarsh Kumar was involved in methodology, visualization, and writing – review and editing. Shweta Arya performed visualization and writing – review and editing. Dr. Ram Chandra Maurya contributed to conceptualization, data curation, formal analysis, methodology, project administration, software, supervision, validation, and writing – review and editing.
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All the experimental procedures were carried out according to the Institutional Animal Ethical Committee (IAEC) guidelines of Kumaun University, Nainital (Protocol no. KUDOPS/157).
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Arya, H., Tamta, K., Kumar, A. et al. Unpredictable chronic mild stress shows neuronal remodeling in multipolar projection neurons of hippocampal complex in postnatal chicks. Anat Sci Int (2024). https://doi.org/10.1007/s12565-024-00758-6
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DOI: https://doi.org/10.1007/s12565-024-00758-6