Stress-induced structural plasticity of medial amygdala stellate neurons and rapid prevention by a candidate antidepressant

Molecular Psychiatry

Volumn 22, Issue 2, 2017, Pages 227-234

  Lau, T ^a   Bigio, B ^a   Zelli, D ^a   McEwen, B S ^a   Nasca, C ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LEVACECARNINE; ACETYLCARNITINE; ANTIDEPRESSANT AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIDEPRESSANT ACTIVITY; ARTICLE; BASOLATERAL AMYGDALA; BEHAVIOR DISORDER; CHRONIC STRESS; CONTROLLED STUDY; COPING BEHAVIOR; IMMOBILIZATION STRESS; MALE; MEDIAL AMYGDALA; MOUSE; NERVE CELL; NERVE CELL PLASTICITY; NONHUMAN; PASSIVE AVOIDANCE; PROPHYLAXIS; PYRAMIDAL NERVE CELL; SOCIAL INTERACTION; STELLATE NEURON; AMYGDALA; ANIMAL; ANXIETY; BRAIN; C57BL MOUSE; DENDRITE; DEPRESSION; FEAR; HIPPOCAMPUS; MENTAL STRESS; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY;

ACETYLCARNITINE; AMYGDALA; ANIMALS; ANTIDEPRESSIVE AGENTS; ANXIETY; BASOLATERAL NUCLEAR COMPLEX; BRAIN; CORTICOMEDIAL NUCLEAR COMPLEX; DENDRITES; DEPRESSION; FEAR; HIPPOCAMPUS; MALE; MICE; MICE, INBRED C57BL; NEURONAL PLASTICITY; NEURONS; PYRAMIDAL CELLS; STRESS, PSYCHOLOGICAL;

EID: 84973120173     PISSN: 13594184     EISSN: 14765578     Source Type: Journal    
DOI: 10.1038/mp.2016.68     Document Type: Article

References (46)

1. McEwen BS. Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol Rev 2007; 87: 873-904.
2. McEwen BS. Stress, sex, and neural adaptation to a changing environment: mechanisms of neuronal remodeling. Ann NY Acad Sci 2010; 1204: 38-59.
3. McEwen BS, Gray JD, Nasca C. Recognizing resilience: learning from the effects of stress on the brain. Neurobiol Stress 2015; 1: 1-11.
4. Southwick SM, Charney DS. The science of resilience: implications for the prevention and treatment of depression. Science 2012; 338: 79-82.
5. McEwen BS. Stress and hippocampal plasticity. Ann Rev Neurosci 1999; 22: 105-122.
6. Radley JJ, Sisti HM, Hao J, Rocher AB, McCall T, Hof PR, et al. Chronic behavioral stress induces apical dendritic reorganization in pyramidal neurons of the medial prefrontal cortex.Neuroscience 2004; 125: 1-6.
7. Sheline YI, Wang PW, Gado MH, Csernansky JG, Vannier MW. Hippocampal atrophy in recurrent major depression. Proc Natl Acad Sci USA 1996; 93: 3908-3913.
8. McEwen BS, Nasca C, Gray JD. Stress effects on neuronal structure: hippocampus, amygdala, and prefrontal cortex. Neuropsychopharmacology 2015; 41: 3-23.
9. Vyas A, Mitra R, Shankaranarayana Rao BS, Chattarji S. Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. J Neurosci 2002; 22: 6810-6818.
10. Phillips RG, LeDoux JE. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci 1992; 106: 274-85.
11. Vinkers CH, Bijlsma EY, Houtepen LC, Westphal KG, Veening JG, Groenink L, et al. Medial amygdala lesions differentially influence stress responsivity and sensorimotor gating in rats. Physiol Behav 2010; 99: 395-401.
12. Wang Y, Zhao S, Wu Z, Feng Y, Zhao C, Zhang C. Oxytocin in the regulation of social behaviours in medial amygdala-lesioned mice via the inhibition of the extracellular signal-regulated kinase signalling pathway. Clin Exp Pharmacol Physiol 2015; 42: 465-474.
13. Pitkanen A, Savander V, LeDoux JE. Organization of intra-amygdaloid circuitries in the rat: an emerging framework for understanding functions of the amygdala. Trends Neurosci 1997; 20: 517-523.
14. Vyas A, Jadhav S, Chattarji S. Prolonged behavioral stress enhances synaptic connectivity in the basolateral amygdala. Neuroscience 2006; 143: 387-393.
15. Mitra R, Jadhav S, McEwen BS, Vyas A, Chattarji S. Stress duration modulates the spatiotemporal patterns of spine formation in the basolateral amygdala. Proc Natl Acad Sci USA 2005; 102: 9371-9376.
16. Bennur S, Shankaranarayana Rao BS, Pawlak R, Strickland S, McEwen BS, Chattarji S. Stress-induced spine loss in the medial amygdala is mediated by tissueplasminogen activator. Neuroscience 2007; 144: 8-16.
17. Felix-Ortiz AC, Tye KM. Amygdala inputs to the ventral hippocampus bidirectionally modulate social behavior. J Neurosci 2014; 34: 586-595.
18. Tejeda HA, O'Donnell P. Amygdala inputs to the prefrontal cortex elicit heterosynaptic suppression of hippocampal inputs. J Neurosci 2014; 34: 14365-14374.
19. Nasca C, Xenos D, Barone Y, Caruso A, Scaccianoce S, Matrisciano F, et al. L-acetylcarnitine causes rapid antidepressant effects through the epigenetic induction of mGlu2 receptors. Proc Natl Acad Sci USA 2013; 110: 4804-4809.
20. Russo SJ, Charney DS. Next generation antidepressants. Proc Natl Acad Sci USA 2013; 110: 4441-4442.
21. Flight MH. Antidepressant epigenetic action. Nat Rev Neurosci 2013; 14: 226.
22. Nasca C, Bigio B, Zelli D, Nicoletti F, McEwen BS. Mind the gap: glucocorticoids modulate hippocampal glutamate tone underlying individual differences in stress susceptibility. Mol Psychiatry 2015; 20: 755-763.
23. McEwen BS, Nasca C, Hodes GE, Kana V, Nestler EJ, Russo SJ. Glucocorticoids-IL6 crosstalk allows identification of inherent individual differences that predict and promote vulnerability to social stress. SfN Abstract 2015.
24. Nasca C, Orlando R, Marchiafava M, Boldrini P, Battaglia G, Scaccianoce S, et al. Exposure to predator odor and resulting anxiety enhances the expression of the alpha2 delta subunit of voltage-sensitive calcium channels in the amygdala. J Neurochem 2013; 125: 649-656.
25. Hodes GE, Pfau ML, Leboeuf M, Golden SA, Christoffel DJ, Bregman D, et al. Individual differences in the peripheral immune system promote resilience versus susceptibility to social stress. Proc Natl Acad Sci USA 2014; 111: 16136-16141.
26. Lein ES, Hawrylycz MJ, Ao N, Ayres M, Bensinger A, Bernard A, et al. Genome-wide atlas of gene expression in the adult mouse brain. Nature 445: 168-176.
27. Magarinos AM, McEwen BS. Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: involvement of glucocorticoid secretion and excitatory amino acid receptors. Neuroscience 1995; 69: 89-98.
28. Goldwater DS, Pavlides C, Hunter RG, Bloss EB, Hof PR, McEwen BS, et al. Structural and functional alterations to rat medial prefrontal cortex following chronic restraint stress and recovery. Neuroscience 2009; 164: 798-808.
29. Sah P, Faber ES, Loped De Armentia M, Power J. The amygdaloid complex: anatomy and physiology. Physiol Rev 2003; 83: 803-834.
30. Nasca C, Zelli D, Bigio B, Piccinin S, Scaccianoce S, Nisticò R, et al. Stress dynamically regulates behavior and glutamatergic gene expression in hippocampus by opening a window of epigenetic plasticity. Proc Natl Acad Sci USA 2015; 112: 14960-14965.
31. Kishi T, Tsumori T, Yokota S, Yasui Y. Topographical projection from the hippocampal formation to the amygdala: a combined anterograde and retrograde tracing study in the rat. J Comp Neurol 2006; 496: 349-368.
32. O'Leary OF, Cryan JF. A ventral view on antidepressant action: roles for adult hippocampal neurogenesis along the dorsoventral axis. Trends Pharmacol Sci 2014; 35: 675-687.
33. Pettegrew JW, Levine J, McClure RJ. Acetyl-L-carnitine physical-chemical, metabolic, and therapeutic properties: relevance for its mode of action in Alzheimer's disease and geriatric depression. Mol Psychiatry 2000; 5: 616-632.
34. Wang W, Lu Y, Xue Z, Li C, Wang C, Zhao X, et al. Rapid-acting antidepressant-like effects of acetyl-L-carnitine mediated by PI3K/AKT/BDNF/VGF signaling pathway in mice. Neuroscience 2015; 285: 281-291.
35. Schaevitz LR, Nicolai R, Lopez CM, D'Iddio S, Iannoni E, Berger-Sweeney JE. Acetyl-L-carnitine improves behavior and dendritic morphology in a mouse model of Rett syndrome. PLoS ONE 2012; 7: e51586.
36. Fritz IB, McEwen BS. Effects of carnitine on fatty-acid oxidation by muscle. Science 1959; 129: 334-335.
37. Nasca C, Zelli D, Lau T, McEwen BS. mGlu2 is a key mediator in the responses to next-generation antidepressant treatments: epigenetic mechanisms of neuronal plasticity. SfN Abstract 2014; 2014.
38. McEwen BS. Stress-induced remodeling of hippocampal CA3 pyramidal neurons. Brain Res 2015; pii: S0006-8993(15)00982-8.
39. Magarinõs AM, McEwen BS, Saboureau M, Pevet P. Rapid and reversible changes in intrahippocampal connectivity during the course of hibernation in European hamsters. Proc Natl Acad Sci USA 2006; 103: 18775-18780.
40. Arendt T, Stieler J, Strijkstra AM, Hut RA, Rudiger J, Van der Zee EA, et al. Reversible paired helical filament-like phosphorylation of tau is an adaptive process associated with neuronal plasticity in hibernating animals. J Neurosci 2003; 23: 6972-6981.
41. Steger MF, Kashdan TB. Depression and everyday social activity, belonging, and well-being. J Counsel Psychol 2009; 56: 289-300.
42. Bickart KC, Wright CI, Dautoff RJ, Dickerson BC, Barrett LF. Amygdala volume and social network size in humans. Nat Neurosci 2011; 14: 163-164.
43. Krishnan V, Han MH, Graham DL, Berton O, Renthal W, Russo SJ, et al. Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell 2007; 131: 391-404.
44. Swanson LW, Petrovich GD. What is the amygdala Trends Neurosci 1998; 8: 323-331
45. Mouly AM, Sullivan R. Memory and plasticity in the olfactory system: from infancy to adulthood. In: Menini A (ed). The Neurobiology of Olfaction, Chap 15. CRC Press: Boca Raton, FL, USA, 2010.
46. Li CI, Maglinao TL, Takahashi LK. Medial amygdala modulation of predator odorinduced unconditioned fear in the rat. Behav Neurosci 2004; 118: 324-332.