Abstract
The hippocampus is a brain structure involved in the regulation of hypothalamic-pituitary-adrenal (HPA) axis and stress response. It plays an important role in the formation of declarative, spatial and contextual memory, as well as in the processing of emotional information. As a part of the limbic system, it is a very susceptible structure towards the effects of various stressors. The molecular mechanisms of structural and functional alternations that occur in the hippocampus under chronic stress imply an increased level of circulating glucocorticoids (GCs), which is an HPA axis response to stress. Certain data show that changes induced by chronic stress may be independent from the GCs levels, opening the possibility of existence of other poorly explored mechanisms and pathways through which stressors act. The hippocampal GABAergic parvalbumin-positive (PV+) interneurons represent an especially vulnerable population of neurons in chronic stress, which may be of key importance in the development of mood disorders. However, cellular and molecular hippocampal changes that arise as a consequence of chronic stress still represent a large and unexplored area. This review discusses the current knowledge about the PV+ interneurons of the hippocampus and the influence of chronic stress on this intriguing population of neurons.
Acknowledgments
This work was supported by the Ministry of Education and Science of the Republic of Serbia, Contracts No. 175061 and 173044. The authors wish to express their sincere gratitude to M. Arch. Vuk Bogunović for helping in designing Figure 1A.
Conflict of interest statement: The authors of this manuscript have no conflict of interest to declare.
References
Andersen, S.L. and Navalta, C.P. (2004). Altering the course of neurodevelopment: a framework for understanding the enduring effects of psychotropic drugs. Int. J. Dev. Neurosci. 22, 423–440.10.1016/j.ijdevneu.2004.06.002Search in Google Scholar PubMed
Baraban, S.C., Hollopeter, G., Erickson, J.C., Schwartzkroin, P.A., and Palmiter, R.D. (1997). Knock-out mice reveal a critical antiepileptic role for neuropeptide Y. J. Neurosci. 17, 8927–8936.10.1523/JNEUROSCI.17-23-08927.1997Search in Google Scholar
Bartos, M., Vida, I., and Jonas, P. (2007). Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat. Rev. Neurosci. 8, 45–56.10.1038/nrn2044Search in Google Scholar PubMed
Behrens, M.M., Ali, S.S., Dao, D.N., Lucero, J., Shekhtman, G., Quick, K.L., and Dugan, LL. (2007). Ketamine-induced loss of phenotype of fast-spiking interneurons is mediated by NADPH-oxidase. Science 318, 1645–1647.10.1126/science.1148045Search in Google Scholar PubMed
Bergström, A., Jayatissa, M.N., Thykjaer, T., and Wiborg, O. (2007). Molecular pathways associated with stress resilience and drug resistance in the chronic mild stress rat model of depression: a gene expression study. J. Mol. Neurosci. 33, 201–215.10.1007/s12031-007-0065-9Search in Google Scholar PubMed
Binder, E.B. and Nemeroff, C.B. (2010). The CRF system, stress, depression and anxiety-insights from human genetic studies. Mol. Psychiatry 15, 574–588.10.1038/mp.2009.141Search in Google Scholar PubMed PubMed Central
Bowers, G., Cullinan, W.E., and Herman, J.P. (1998). Region-specific regulation of glutamic acid decarboxylase (GAD) mRNA expression in central stress circuits. J. Neurosci. 18, 5938–5947.10.1523/JNEUROSCI.18-15-05938.1998Search in Google Scholar
Brambilla, P., Perez, J., Barale, F., Schettini, G., and Soares, J.C. (2003). GABAergic dysfunction in mood disorders. Mol. Psychiatry 8, 715, 721–737.10.1038/sj.mp.4001362Search in Google Scholar PubMed
Bremner, J.D., Narayan, M., Anderson, E.R., Staib, L.H., Miller, H.L., and Charney, D.S. (2000). Hippocampal volume reduction in major depression. Am. J. Psychiatry 157, 115–118.10.1176/ajp.157.1.115Search in Google Scholar PubMed
Brenhouse, H.C. and Andersen, S.L. (2011). Nonsteroidal anti-inflammatory treatment prevents delayed effects of early life stress in rats. Biol. Psychiatry 70, 434–440.10.1016/j.biopsych.2011.05.006Search in Google Scholar PubMed PubMed Central
Cadet, J.L. and Brannock, C. (1998). Free radicals and the pathobiology of brain dopamine systems. Neurochem. Int. 32, 117–131.10.1016/S0197-0186(97)00031-4Search in Google Scholar
Calabretta, B., Kaczmarek, L., Mars, W., Ochoa, D., Gibson, C.W., Hirschhorn, R.R., and Baserga, R. (1985). Cell-cycle-specific genes differentially expressed in human leukemias. Proc. Natl. Acad. Sci. USA 82, 4463–4467.10.1073/pnas.82.13.4463Search in Google Scholar
Campbell, S. and MacQueen, G. (2004). The role of the hippocampus in the pathophysiology of major depression. J. Psychiatry Neurosci. 29, 417–426.Search in Google Scholar
Carnevali, L., Mastorci, F., Graiani, G., Razzoli, M., Trombini, M., Pico-Alfonso, M.A., Arban, R., Grippo, A.J., Quaini, F., and Sgoifo. A. (2012). Social defeat and isolation induce clear signs of a depression-like state, but modest cardiac alterations in wild-type rats. Physiol. Behav. 106, 142–150.10.1016/j.physbeh.2012.01.022Search in Google Scholar
Celio, M.R. (1990). Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35, 375–475.10.1016/0306-4522(90)90091-HSearch in Google Scholar
Charmandari, E., Tsigos, C., and Chrousos, G. (2005). Endocrinology of the stress response. Annu. Rev. Physiol. 67, 259–284.10.1146/annurev.physiol.67.040403.120816Search in Google Scholar
Choi, Y., Chen, H.V., and Lipton, S.A. (2001). Three pairs of cysteine residues mediate both redox and zn2+ modulation of the nmda receptor. J. Neurosci. 21, 392–400.10.1523/JNEUROSCI.21-02-00392.2001Search in Google Scholar
Cobb, S.R., Halasy, K., Vida, I., Nyiri, G., Tamás, G., Buhl, E.H., and Somogyi, P. (1997). Synaptic effects of identified interneurons innervating both interneurons and pyramidal cells in the rat hippocampus. Neuroscience 79, 629–648.10.1016/S0306-4522(97)00055-9Search in Google Scholar
Conrad, C.D., Grote, K.A., Hobbs, R.J., and Ferayorni, A. (2003). Sex differences in spatial and non-spatial Y-maze performance after chronic stress. Neurobiol. Learn. Mem. 79, 32–40.10.1016/S1074-7427(02)00018-7Search in Google Scholar
Cowell, R.M., Blake, K.R., and Russell, J.W. (2007). Localization of the transcriptional coactivator PGC-1alpha to GABAergic neurons during maturation of the rat brain. J. Comp. Neurol. 502, 1–18.10.1002/cne.21211Search in Google Scholar PubMed
Cowell, R.M., Talati, P., Blake, K.R., Meador-Woodruff, J.H., and Russell, J.W. (2009). Identification of novel targets for PGC-1alpha and histone deacetylase inhibitors in neuroblastoma cells. Biochem. Biophys. Res. Commun. 379, 578–582.10.1016/j.bbrc.2008.12.109Search in Google Scholar PubMed PubMed Central
Czeh, B., Simon, M., van der Hart, M.G., Schmelting, B., Hesselink, M.B., and Fuchs, E. (2005). Chronic stress decreases the number of parvalbumin-immunoreactive interneurons in the hippocampus: prevention by treatment with a substance P receptor (NK1) antagonist. Neuropsychopharmacology 30, 67–79.10.1038/sj.npp.1300581Search in Google Scholar PubMed
Czéh, B., Varga, Z.K.K., Henningsen, K., Kovács, G.L., Miseta, A., and Wiborg, O. (2015). Chronic stress reduces the number of GABAergic interneurons in the adult rat hippocampus, dorsal-ventral and region-specific differences. Hippocampus 25, 393–405.10.1002/hipo.22382Search in Google Scholar PubMed
De Foubert, G., Carney, S.L., Robinson, C.S., Destexhe, E.J., Tomlinson, R., Hicks, C.A., Murray, T.K., Gaillard, J.P., Deville, C., Xhenseval, V., et al. (2004). Fluoxetine-induced change in rat brain expression of brain-derived neurotrophic factor varies depending on length of treatment. Neuroscience 128, 597–604.10.1016/j.neuroscience.2004.06.054Search in Google Scholar PubMed
de Kloet, E.R., Joëls, M., and Holsboer, F. (2005). Stress and the brain: from adaptation to disease. Nat. Rev. Neurosci. 6, 463-475.10.1038/nrn1683Search in Google Scholar PubMed
Denenberg, V.H. and Smith, S.A. (1963). Effects of infantile stimulation and age upon behavior. J. Comp. Physiol. Psychol. 56, 307–312.10.1037/h0041461Search in Google Scholar PubMed
Do, K.Q., Cabungcal, J.H., Frank, A., Steullet, P., and Cuenod, M. (2009). Redox dysregulation, neurodevelopment, and schizophrenia. Curr. Opin. Neurobiol. 19, 220–230.10.1016/j.conb.2009.05.001Search in Google Scholar PubMed
Dugan, L.L., Ali, S.S., Shekhtman, G., Roberts, A.J., Lucero, J., Quick, K.L., and Behrens, M.M. (2009). IL-6 mediated degeneration of forebrain GABAergic interneurons and cognitive impairment in aged mice through activation of neuronal NADPH oxidase. PLoS One 4, e5518.10.1371/journal.pone.0005518Search in Google Scholar PubMed PubMed Central
Duman, R.S. (2014). Pathophysiology of depression and innovative treatments: remodeling glutamatergic synaptic connections. Dialogues Clin. Neurosci. 16, 11–27.10.31887/DCNS.2014.16.1/rdumanSearch in Google Scholar
El Falougy, H., Kubikova, E., and Benuska, J. (2008). The microscopical structure of the hippocampus in the rat. Bratisl. Lek. Listy. 109, 106–110.Search in Google Scholar
Filipović, D., Gavrilović, L., Dronjak, S., and Radojcić, M.B. (2005). Brain glucocorticoid receptor and heat shock protein 70 levels in rats exposed to acute, chronic or combined stress. Neuropsychobiology 51, 107–114.10.1159/000084168Search in Google Scholar PubMed
Filipović, D., Zlatković, J., Inta, D., Bjelobaba, I., Stojiljkovic, M., and Gass, P. (2011). Chronic isolation stress predisposes the frontal cortex but not the hippocampus to the potentially detrimental release of cytochrome c from mitochondria and the activation of caspase-3. J. Neurosci. Res. 89, 1461–1470.10.1002/jnr.22687Search in Google Scholar PubMed
Filipović, D., Zlatković, J., Gass, P., and Inta, D. (2013). The differential effects of acute vs. chronic stress and their combination on hippocampal parvalbumin and inducible heat shock protein 70 expression. Neuroscience 236, 47–54.10.1016/j.neuroscience.2013.01.033Search in Google Scholar
Freund, T.F. and Buzsáki, G. (1996). Interneurons of the hippocampus. Hippocampus 6, 347–470.10.1002/(SICI)1098-1063(1996)6:4<347::AID-HIPO1>3.0.CO;2-ISearch in Google Scholar
Freund, T.F. (2003). Interneuron diversity series: rhythm and mood in perisomatic inhibition. Trends Neurosci. 26, 489–495.10.1016/S0166-2236(03)00227-3Search in Google Scholar
Fukuda, T. and Kosaka, T. (2000). Gap junctions linking the dendritic network of GABAergic interneurons in the hippocampus. J. Neurosci. 20, 1519–1528.10.1523/JNEUROSCI.20-04-01519.2000Search in Google Scholar
Giachino, C., Canalia, N., Capone, F., Fasolo, A., Alleva, E., Riva, M.A., Cirulli, F., and Peretto, P. (2007). Maternal deprivation and early handling affect density of calcium binding protein-containing neurons in selected brain regions and emotional behavior in periadolescent rats. Neuroscience 145, 568–578.10.1016/j.neuroscience.2006.12.042Search in Google Scholar
Godavarthi, S.K., Sharma, A., and Jana, N.R. (2014). Reversal of reduced parvalbumin neurons in hippocampus and amygdala of Angelman syndrome model mice by chronic treatment of fluoxetine. J. Neurochem. 130, 444–454.10.1111/jnc.12726Search in Google Scholar
Gould, E. and Tanapat, P. (1999). Stress and hippocampal neurogenesis. Biol. Psychiatry 46, 1472–1479.10.1016/S0006-3223(99)00247-4Search in Google Scholar
Groeneweg, F.L., Karst, H., de Kloet, E.R., and Joëls, M. (2011). Rapid non-genomic effects of corticosteroids and their role in the central stress response. J. Endocrinol. 209, 153–167.10.1530/JOE-10-0472Search in Google Scholar
Groeneweg, F.L., Karst, H., de Kloet, E.R., and Joëls, M. (2012). Mineralocorticoid and glucocorticoid receptors at the neuronal membrane, regulators of nongenomic corticosteroid signalling. Mol. Cell. Endocrinol. 350, 299–309.10.1016/j.mce.2011.06.020Search in Google Scholar
Gulyás, A.I., Buzsáki, G., Freund, T.F., and Hirase, H. (2006). Populations of hippocampal inhibitory neurons express different levels of cytochrome c. Eur. J. Neurosci. 23, 2581–2594.10.1111/j.1460-9568.2006.04814.xSearch in Google Scholar
Haiech, J., Derancourt, J., Pechère, J.F., and Demaille, J.G. (1979). Magnesium and calcium binding to parvalbumins: evidence for differences between parvalbumins and an explanation of their relaxing function. Biochemistry. 18, 2752–2758.10.1021/bi00580a010Search in Google Scholar PubMed
Harte, M.K., Powell, S.B., Swerdlow, N.R., Geyer, M.A., and Reynolds, G.P. (2007). Deficits in parvalbumin and calbindin immunoreactive cells in the hippocampus of isolation reared rats. J. Neural Transm. 114, 893–898.10.1007/s00702-007-0627-6Search in Google Scholar PubMed
Heinrich, L.M. and Gullone, E. (2006). The clinical significance of loneliness: a literature review. Clin. Psychol. Rev. 26, 695–718.10.1016/j.cpr.2006.04.002Search in Google Scholar PubMed
Herman, J.P., Patel, P.D., Akil, H., and Watson, S.J. (1989). Localization and regulation of glucocorticoid and mineralocorticoid receptor messenger RNAs in the hippocampal formation of the rat. Mol. Endocrinol. 3, 1886–1894.10.1210/mend-3-11-1886Search in Google Scholar PubMed
Hirrlinger, J., Schulz, J.B., and Dringen, R. (2002). Effects of dopamine on the glutathione metabolism of cultured astroglial cells: implications for Parkinson’s disease. J. Neurochem. 82, 458–467.10.1046/j.1471-4159.2002.01013.xSearch in Google Scholar PubMed
Holm, M.M., Nieto-Gonzalez, J.L., Vardya, I., Henningsen, K., Jayatissa, M.N., Wiborg, O., and Jensen, K. (2011). Hippocampal GABAergic dysfunction in a rat chronic mild stress model of depression. Hippocampus 21(4), 422–433.10.1002/hipo.20758Search in Google Scholar PubMed
Hu, W., Zhang, M., Czéh, B., Flügge, G., and Zhang, W. (2010). Stress impairs GABAergic network function in the hippocampus by activating nongenomic glucocorticoid receptors and affecting the integrity of the parvalbumin-expressing neuronal network. Neuropsychopharmacology 35, 1693–1707.10.1038/npp.2010.31Search in Google Scholar PubMed PubMed Central
Jayatissa, M.N., Bisgaard, C., Tingstrom, A., Papp, M., and Wiborg, O. (2006). Hippocampal cytogenesis correlates to escitalopram-mediated recovery in a chronic mild stress rat model of depression. Neuropsychopharmacology 31, 2395–2404.10.1038/sj.npp.1301041Search in Google Scholar PubMed
Jayatissa, M.N., Bisgaard, C.F., West, M.J., and Wiborg, O. (2008). The number of granule cells in rat hippocampus is reduced after chronic mild stress and re-established after chronic escitalopram treatment. Neuropharmacology 54, 530–541.10.1016/j.neuropharm.2007.11.009Search in Google Scholar PubMed
Jiang, M. and Swann, J.W. (2005). A role for L-type calcium channels in the maturation of parvalbumin-containing hippocampal interneurons. Neuroscience 135, 839–850.10.1016/j.neuroscience.2005.06.073Search in Google Scholar PubMed
Joëls, M. and Baram, T.Z. (2009). The neuro-symphony of stress. Nat. Rev. Neurosci. 10, 459–466.10.1038/nrn2632Search in Google Scholar
Joëls, M., Karst, H., Alfarez, D., Heine, V.M., Qin, Y., van Riel, E., Verkuyl, M., Lucassen, P.J., and Krugers, H.J. (2004). Effects of chronic stress on structure and cell function in rat hippocampus and hypothalamus. Stress 7, 221–231.10.1080/10253890500070005Search in Google Scholar
Joëls, M., Karst, H., Krugers, H.J., and Lucassen, P.J. (2007). Chronic stress: implications for neuronal morphology, function and neurogenesis. Front. Neuroendocrinol. 28, 72–96.10.1016/j.yfrne.2007.04.001Search in Google Scholar
Karst, H., Berger, S., Turiault, M., Tronche, F., Schütz, G., and Joëls, M. (2005). Mineralocorticoid receptors are indispensable for nongenomic modulation of hippocampal glutamate transmission by corticosterone. Proc. Natl. Acad. Sci. USA 102, 19204–19207.10.1073/pnas.0507572102Search in Google Scholar
Kawaguchi, Y., Katsumaru, H., Kosaka, T., Heizmann, C.W., and Hama, K. (1987). Fast spiking cells in rat hippocampus (CA1 region) contain the calcium-binding protein parvalbumin. Brain Res. 416, 369–374.10.1016/0006-8993(87)90921-8Search in Google Scholar
Keilhoff, G., Becker, A., Grecksch, G., Wolf, G., and Bernstein, H.G. (2004). Repeated application of ketamine to rats induces changes in the hippocampal expression of parvalbumin, neuronal nitric oxide synthase and cFOS similar to those found in human schizophrenia. Neuroscience 126, 591–598.10.1016/j.neuroscience.2004.03.039Search in Google Scholar
Kinney, J.W., Davis, C.N., Tabarean, I., Conti, B., Bartfai, T., and Behrens, M.M. (2006). A specific role for NR2A-containing NMDA receptors in the maintenance of parvalbumin and GAD67 immunoreactivity in cultured interneurons. J. Neurosci. 26, 1604–1615.10.1523/JNEUROSCI.4722-05.2006Search in Google Scholar
Klomp, A., Václavů, L., Meerhoff, G.F., Reneman, L., and Lucassen, P.J. (2014). Effects of chronic fluoxetine treatment on neurogenesis and tryptophan hydroxylase expression in adolescent and adult rats. PLoS One 9, e97603.10.1371/journal.pone.0097603Search in Google Scholar
Kosaka, T., Kosaka, K., Tateishi, K., Hamaoka, Y., Yanaihara, N., Wu, J.Y., and Hama, K. (1985). GABAergic neurons containing CCK-8-like and/or VIP-like immunoreactivities in the rat hippocampus and dentate gyrus. J. Comp. Neurol. 239, 420–430.10.1002/cne.902390408Search in Google Scholar
Kosaka, T., Katsumaru, H., Hama, K., Wu, J.Y., and Heizmann, C.W. (1987). GABAergic neurons containing the Ca2+-binding protein parvalbumin in the rat hippocampus and dentate gyrus. Brain Res. 419, 119–130.10.1016/0006-8993(87)90575-0Search in Google Scholar
Krügers, H.J., Koolhaas, J.M., Medema, R.M., and Korf, J. (1996). Prolonged subordination stress increases Calbindin-D28k immunoreactivity in the rat hippocampal CA1 area. Brain Res. 729, 289–293.10.1016/0006-8993(96)00583-5Search in Google Scholar
Landisman, C.E., Long, M.A., Beierlein, M., Deans, M.R., Paul, D.L., and Connors, B.W. (2002). Electrical synapses in the thalamic reticular nucleus. J. Neurosci. 22, 1002–1009.10.1523/JNEUROSCI.22-03-01002.2002Search in Google Scholar
Lasztóczi, B., Tukker, J.J., Somogyi, P., Klausberger, T. (2011). Terminal field and firing selectivity of cholecystokinin-expressing interneurons in the hippocampal CA3 area. J. Neurosci. 31, 18073–18093.10.1523/JNEUROSCI.3573-11.2011Search in Google Scholar
Lephart, E.D. and Watson, M.A. (1999). Maternal separation: hypothalamic-preoptic area and hippocampal calbindin-D28K and calretinin in male and female infantile rats. Neurosci. Lett. 267, 41–44.10.1016/S0304-3940(99)00326-2Search in Google Scholar
Lewis, D.A., Curley, A.A., Glausier, J.R., and Volk, D.W. (2012). Cortical parvalbumin interneurons and cognitive dysfunction in schizophrenia. Trends Neurosci. 35, 57–67.10.1016/j.tins.2011.10.004Search in Google Scholar
Li, Y., Mu, Y., and Gage, F.H. (2009). Development of neural circuits in the adult hippocampus. Curr. Top. Dev. Biol. 87, 149–174.10.1016/S0070-2153(09)01205-8Search in Google Scholar
Luine, V.N., Beck, K.D., Bowman, R.E., Frankfurt, M., and Maclusky, N.J. (2007). Chronic stress and neural function: accounting for sex and age. J. Neuroendocrinol. 19, 743–751.10.1111/j.1365-2826.2007.01594.xSearch in Google Scholar PubMed
MacQueen, G.M., Campbell, S., McEwen, B.S., Macdonald, K., Amano, S., Joffe, R.T., Nahmias, C., and Young, L.T. (2003). Course of illness, hippocampal function, and hippocampal volume in major depression. Proc. Natl. Acad. Sci. USA 100, 1387–1392.10.1073/pnas.0337481100Search in Google Scholar PubMed PubMed Central
Magariños, A.M., Verdugo, J.M., and McEwen, B.S. (1997). Chronic stress alters synaptic terminal structure in hippocampus. Proc. Natl. Acad. Sci. USA 94, 14002–14008.10.1073/pnas.94.25.14002Search in Google Scholar PubMed PubMed Central
Maggio, N. and Segal, M. (2012). Cellular basis of a rapid effect of mineralocorticosteroid receptors activation on LTP in ventral hippocampal slices. Hippocampus 22, 267–275.10.1002/hipo.20893Search in Google Scholar PubMed
Markram, H., Toledo-Rodriguez, M., Wang, Y., Gupta, A., Silberberg, G., and Wu, C. (2004). Interneurons of the neocortical inhibitory system. Nat. Rev. Neurosci. 5, 793–807.10.1038/nrn1519Search in Google Scholar
McEwen, B.S. (1999). Stress and hippocampal plasticity. Annu. Rev. Neurosci. 22, 105–122.10.1146/annurev.neuro.22.1.105Search in Google Scholar
McEwen, B.S. (2006). Protective and damaging effects of stress mediators: central role of the brain. Dialogues Clin. Neurosci. 8, 367–381.10.1016/S0079-6123(08)62128-7Search in Google Scholar
Megías, M., Emri, Z., Freund, T.F., and Gulyás, A.I. (2001). Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells. Neuroscience 102, 527–540.10.1016/S0306-4522(00)00496-6Search in Google Scholar
Meyer, A.H., Katona, I., Blatow, M., Rozov, A., and Monyer, H. (2002). In vivo labeling of parvalbumin-positive interneurons and analysis of electrical coupling in identified neurons. J. Neurosci. 22, 7055–7064.10.1523/JNEUROSCI.22-16-07055.2002Search in Google Scholar
Milner, T.A., Burstein, S.R., Marrone, G.F., Khalid, S., Gonzalez, A.D., Williams, T.J., Schierberl, K.C., Torres-Reveron, A., Gonzales, K.L., McEwen, B.S., et al. (2013). Stress differentially alters mu opioid receptor density and trafficking in parvalbumin-containing interneurons in the female and male rat hippocampus. Synapse 67, 757–772.10.1002/syn.21683Search in Google Scholar
Nguyen, R., Morrissey, M.D., Mahadevan, V., Cajanding, J.D., Woodin, M.A., Yeomans, J.S., Takehara-Nishiuchi, K., and Kim, J.C. (2014). Parvalbumin and GAD65 interneuron inhibition in the ventral hippocampus induces distinct behavioral deficits relevant to schizophrenia. J. Neurosci. 34, 14948–14960.10.1523/JNEUROSCI.2204-14.2014Search in Google Scholar
Nowak, B., Zadrożna, M., Ossowska, G., Sowa-Kućma, M., Gruca, P., Papp, M., Dybala, M., Pilc, A., Nowak, G. (2010). Alterations in hippocampal calcium-binding neurons induced by stress models of depression: a preliminary assessment. Pharmacol. Rep. 62, 1204–1210.10.1016/S1734-1140(10)70383-2Search in Google Scholar
Ogren, S.O., Kuteeva, E., Elvander-Tottie, E., and Hökfelt, T. (2010). Neuropeptides in learning and memory processes with focus on galanin. Eur. J. Pharmacol. 626, 9–17.10.1016/j.ejphar.2009.09.070Search in Google Scholar PubMed
Orchinik, M., Carroll, S.S., Li, Y.H., McEwen, B.S., and Weiland, N.G. (2001). Heterogeneity of hippocampal GABA(A) receptors: regulation by corticosterone. J. Neurosci. 21, 330–339.10.1523/JNEUROSCI.21-01-00330.2001Search in Google Scholar
Pinto, V., Costa, J.C., Morgado, P., Mota, C., Miranda, A., Bravo, F.V., Oliveira, T.G., Cerqueira, J.J., and Sousa, N. (2015). Differential impact of chronic stress along the hippocampal dorsal-ventral axis. Brain Struct. Funct. 220, 1205–1212.10.1007/s00429-014-0713-0Search in Google Scholar
Plotsky, P.M. and Meaney, M.J. (1993). Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats. Brain Res. Mol. Brain Res. 18, 195–200.10.1016/0169-328X(93)90189-VSearch in Google Scholar
Rabinovic, A.D. and Hastings, T.G. (1998). Role of endogenous glutathione in the oxidation of dopamine. J. Neurochem. 71, 2071–2078.10.1046/j.1471-4159.1998.71052071.xSearch in Google Scholar PubMed
Reul, J.M. and de Kloet, E.R. (1985). Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. Endocrinology 117, 2505–2511.10.1210/endo-117-6-2505Search in Google Scholar PubMed
Ribak, C.E., Nitsch, R., and Seress, L. (1990). Proportion of parvalbumin-positive basket cells in the GABAergic innervation of pyramidal and granule cells of the rat hippocampal formation. J. Comp. Neurol. 300, 449–461.10.1002/cne.903000402Search in Google Scholar PubMed
Roceri, M., Cirulli, F., Pessina, C., Peretto, P., Racagni, G., and Riva, M.A. (2004). Postnatal repeated maternal deprivation produces age-dependent changes of brain-derived neurotrophic factor expression in selected rat brain regions. Biol. Psychiatry 55, 708–714.10.1016/j.biopsych.2003.12.011Search in Google Scholar PubMed
Rotaru, D.C., Lewis, D.A., and Gonzalez-Burgos, G. (2012). The role of glutamatergic inputs onto parvalbumin-positive interneurons: relevance for schizophrenia. Rev. Neurosci. 23, 97–109.10.1515/revneuro-2011-0059Search in Google Scholar PubMed PubMed Central
Sartorius, A., Mahlstedt, M.M., Vollmayr, B., Henn, F.A., and Ende, G. (2007). Elevated spectroscopic glutamate/gamma-amino butyric acid in rats bred for learned helplessness. Neuroreport 18, 1469–1473.10.1097/WNR.0b013e3282742153Search in Google Scholar PubMed
Scarr, E. (2001). Neurochemical Abnormalities in the Hippocampal Formation with Schizophrenia. Pharmacology and Therapeutics in the New Millennium. S.K. Gupta, ed. (Springer Science & Business Media).Search in Google Scholar
Schiavone, S., Sorce, S., Dubois-Dauphin, M., Jaquet, V., Colaianna, M., Zotti, M., Cuomo, V., Trabace, L., and Krause, K.H. (2009). Involvement of NOX2 in the development of behavioral and pathologic alterations in isolated rats. Biol. Psychiatry 66, 384–392.10.1016/j.biopsych.2009.04.033Search in Google Scholar PubMed
Schwaller, B., Meyer, M., and Schiffmann, S. (2002). “New” functions for “old” proteins: the role of the calcium-binding proteins calbindin D-28k, calretinin and parvalbumin, in cerebellar physiology. Studies with knockout mice. Cerebellum 1, 241–258.10.1080/147342202320883551Search in Google Scholar PubMed
Scotti, A.L., Kalt, G., Bollag, O., Nitsch, C. (1997). Parvalbumin disappears from GABAergic CA1 neurons of the gerbil hippocampus with seizure onset while its presence persists in the perforant path. Brain Res. 760, 109–117.10.1016/S0006-8993(97)00309-0Search in Google Scholar
Seress, L., Abrahám, H., Paleszter, M., and Gallyas, F. (2001). Granule cells are the main source of excitatory input to a subpopulation of GABAergic hippocampal neurons as revealed by electron microscopic double staining for zinc histochemistry and parvalbumin immunocytochemistry. Exp. Brain Res. 136, 456–462.10.1007/s002210000601Search in Google Scholar
Sheline, Y.I., Gado, M.H., and Kraemer, H.C. (2003). Untreated depression and hippocampal volume loss. Am. J. Psychiatry 160, 1516–1518.10.1176/appi.ajp.160.8.1516Search in Google Scholar
Sik, A., Penttonen, M., Ylinen, A., and Buzsáki, G. (1995). Hippocampal CA1 interneurons: an in vivo intracellular labeling study. J. Neurosci. 15, 6651–6665.10.1523/JNEUROSCI.15-10-06651.1995Search in Google Scholar
Soghomonian, J.J. and Martin, D.L. (1998). Two isoforms of glutamate decarboxylase: why? Trends Pharmacol. Sci. 19, 500–505.10.1016/S0165-6147(98)01270-XSearch in Google Scholar
Spasojevic, N., Gavrilovic, L.J., Varagic, V., and Dronjak, S. (2007). Effects of chronic diazepam treatments on behavior on individually housed rats. Arch. Biol. Sci. 59, 113–117.10.2298/ABS0702113SSearch in Google Scholar
Stepan, J., Dine, J., and Eder, M. (2015). Functional optical probing of the hippocampal trisynaptic circuit in vitro: network dynamics, filter properties, and polysynaptic induction of CA1 LTP. Front. Neurosci. 9, 160.10.3389/fnins.2015.00160Search in Google Scholar PubMed PubMed Central
Steullet, P., Neijt, H.C., Cuénod, M., and Do, K.Q. (2006). Synaptic plasticity impairment and hypofunction of NMDA receptors induced by glutathione deficit: relevance to schizophrenia. Neuroscience 137, 807–819.10.1016/j.neuroscience.2005.10.014Search in Google Scholar PubMed
Steullet, P., Lavoie, S., Kraftsik, R., Guidi, R., Gysin, R., Cuénod, M., and Do, K.Q. (2008). A glutathione deficit alters dopamine modulation of L-type calcium channels via D2 and ryanodine receptors in neurons. Free Radic. Biol. Med. 44, 1042–1054.10.1016/j.freeradbiomed.2007.12.006Search in Google Scholar PubMed
Steullet, P., Cabungcal, J.H., Kulak, A., Kraftsik, R., Chen, Y., Dalton, T.P., Cuenod, M., and Do, K.Q. (2010). Redox dysregulation affects the ventral but not dorsal hippocampus: impairment of parvalbumin neurons, gamma oscillations, and related behaviors. J. Neurosci. 30, 2547–2558.10.1523/JNEUROSCI.3857-09.2010Search in Google Scholar PubMed PubMed Central
St-Pierre, J., Drori, S., Uldry, M., Silvaggi, J.M., Rhee, J., Jäger S., Handschin, C., Zheng, K., Lin, J., Yang, W., et al. (2006). Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell 127, 397–408.10.1016/j.cell.2006.09.024Search in Google Scholar
Szabadits, E., Cserép, C., Ludányi, A., Katona, I., Gracia-Llanes, J., Freund, T.F., and Nyíri, G. (2007). Hippocampal GABAergic synapses possess the molecular machinery for retrograde nitric oxide signaling. J. Neurosci. 27, 8101–8111.10.1523/JNEUROSCI.1912-07.2007Search in Google Scholar
Tamás, G., Buhl, E.H., Lörincz, A., and Somogyi, P. (2000). Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons. Nat. Neurosci. 3, 366–371.10.1038/73936Search in Google Scholar
Tukker, J.J., Lasztóczi, B., Katona, L., Roberts, J.D.B., Pissadaki, E.K., Dalezios, Y., Márton, L., Zhang, L., Klausberger, T., and Somogyi, P. (2013). Distinct dendritic arborization and in vivo firing patterns of parvalbumin-expressing basket cells in the hippocampal area CA3. J. Neurosci. 33, 6809–6825.10.1523/JNEUROSCI.5052-12.2013Search in Google Scholar
van der Hart, M.G.C, Czéh, B., de Biurrun, G., Michaelis, T., Watanabe, T., Natt, O., Frahm, J., and Fuchs, E. (2002). Substance P receptor antagonist and clomipramine prevent stress-induced alterations in cerebral metabolites, cytogenesis in the dentate gyrus and hippocampal volume. Mol. Psychiatry 7, 933–941.10.1038/sj.mp.4001130Search in Google Scholar
Venance, L., Rozov, A., Blatow, M., Burnashev, N., Feldmeyer, D., and Monyer, H. (2000). Connexin expression in electrically coupled postnatal rat brain neurons. Proc. Natl. Acad. Sci. USA 97, 10260–10265.10.1073/pnas.160037097Search in Google Scholar
Vito, P., Lacanà, E., and D’Adamio, L. (1996). Interfering with apoptosis: Ca(2+)-binding protein ALG-2 and Alzheimer’s disease gene ALG-3. Science 271, 521–525.10.1126/science.271.5248.521Search in Google Scholar
Vyas, A., Mitra, R., Shankaranarayana Rao, B.S., and Chattarji, S. (2002). Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. J. Neurosci. 22, 6810–6818.10.1523/JNEUROSCI.22-15-06810.2002Search in Google Scholar
Wang, D. and Fawcett, J. (2012). The perineuronal net and the control of CNS plasticity. Cell Tissue Res. 349, 147–160.10.1007/s00441-012-1375-ySearch in Google Scholar
Watanabe, Y., Gould, E., and McEwen, B.S. (1992). Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain. Res. 588, 341–345.10.1016/0006-8993(92)91597-8Search in Google Scholar
Wood, G.E., Young, L.T., Reagan, L.P., Chen, B., and McEwen, B.S. (2004). Stress-induced structural remodeling in hippocampus: prevention by lithium treatment. Proc. Natl. Acad. Sci. USA 101, 3973–3978.10.1073/pnas.0400208101Search in Google Scholar
Yamada, J., Ohgomori, T., and Jinno, S. (2015). Perineuronal nets affect parvalbumin expression in GABAergic neurons of the mouse hippocampus. Eur. J. Neurosci. 41, 368–378.10.1111/ejn.12792Search in Google Scholar
Zhang, Z.J. and Reynolds, G.P. (2002). A selective decrease in the relative density of parvalbumin-immunoreactive neurons in the hippocampus in schizophrenia. Schizophr. Res. 55, 1–10.10.1016/S0920-9964(01)00188-8Search in Google Scholar
Zimmer, D.B., Cornwall, E.H., Landar, A., and Song, W. (1995). The S100 protein family: history, function, and expression. Brain Res. Bull. 37, 417–429.10.1016/0361-9230(95)00040-2Search in Google Scholar
Zlatković, J., Todorović, N., Bošković, M., Pajović, S.B., Demajo, M., and Filipović, D. (2014). Different susceptibility of prefrontal cortex and hippocampus to oxidative stress following chronic social isolation stress. Mol. Cell. Biochem. 393, 43–57.10.1007/s11010-014-2045-zSearch in Google Scholar PubMed
©2016 by De Gruyter
Articles in the same Issue
- Frontmatter
- The multi-facet aspects of cell sentience and their relevance for the integrative brain actions: role of membrane protein energy landscape
- Current advances in cell electrophysiology: applications for the analysis of intercellular communications within the neurovascular unit
- Putative duality of presynaptic events
- Emotion regulation strategies in trauma-related disorders: pathways linking neurobiology and clinical manifestations
- Chronic stress, hippocampus and parvalbumin-positive interneurons: what do we know so far?
- Endogenous spontaneous ultraweak photon emission in the formation of eye-specific retinogeniculate projections before birth
- The mental time travel continuum: on the architecture, capacity, versatility and extension of the mental bridge into the past and future
- Cognitive function in schizophrenia: conflicting findings and future directions
- Recent progress on the role of GABAergic neurotransmission in the pathogenesis of Alzheimer’s disease
Articles in the same Issue
- Frontmatter
- The multi-facet aspects of cell sentience and their relevance for the integrative brain actions: role of membrane protein energy landscape
- Current advances in cell electrophysiology: applications for the analysis of intercellular communications within the neurovascular unit
- Putative duality of presynaptic events
- Emotion regulation strategies in trauma-related disorders: pathways linking neurobiology and clinical manifestations
- Chronic stress, hippocampus and parvalbumin-positive interneurons: what do we know so far?
- Endogenous spontaneous ultraweak photon emission in the formation of eye-specific retinogeniculate projections before birth
- The mental time travel continuum: on the architecture, capacity, versatility and extension of the mental bridge into the past and future
- Cognitive function in schizophrenia: conflicting findings and future directions
- Recent progress on the role of GABAergic neurotransmission in the pathogenesis of Alzheimer’s disease