Skip to main content
Top
Published in: Brain Structure and Function 5/2017

01-07-2017 | Original Article

Acute restraint stress decreases c-fos immunoreactivity in hilar mossy cells of the adult dentate gyrus

Authors: Jillian N. Moretto, Áine M. Duffy, Helen E. Scharfman

Published in: Brain Structure and Function | Issue 5/2017

Login to get access

Abstract

Although a great deal of information is available about the circuitry of the mossy cells (MCs) of the dentate gyrus (DG) hilus, their activity in vivo is not clear. The immediate early gene c-fos can be used to gain insight into the activity of MCs in vivo, because c-fos protein expression reflects increased neuronal activity. In prior work, it was identified that control rats that were perfusion-fixed after removal from their home cage exhibited c-fos immunoreactivity (ir) in the DG in a spatially stereotyped pattern: ventral MCs and dorsal granule cells (GCs) expressed c-fos protein (Duffy et al., Hippocampus 23:649–655, 2013). In this study, we hypothesized that restraint stress would alter c-fos-ir, because MCs express glucocorticoid type 2 receptors and the DG is considered to be involved in behaviors related to stress or anxiety. We show that acute restraint using a transparent nose cone for just 10 min led to reduced c-fos-ir in ventral MCs compared to control rats. In these comparisons, c-fos-ir was evaluated 30 min after the 10 min-long period of restraint, and if evaluation was later than 30 min c-fos-ir was no longer suppressed. Granule cells (GCs) also showed suppressed c-fos-ir after acute restraint, but it was different than MCs, because the suppression persisted for over 30 min after the restraint. We conclude that c-fos protein expression is rapidly and transiently reduced in ventral hilar MCs after a brief period of restraint, and suppressed longer in dorsal GCs.
Literature
go back to reference Acsady L, Katona I, Martinez-Guijarro FJ, Buzsaki G, Freund TF (2000) Unusual target selectivity of perisomatic inhibitory cells in the hilar region of the rat hippocampus. J Neurosci 20:6907–6919PubMed Acsady L, Katona I, Martinez-Guijarro FJ, Buzsaki G, Freund TF (2000) Unusual target selectivity of perisomatic inhibitory cells in the hilar region of the rat hippocampus. J Neurosci 20:6907–6919PubMed
go back to reference Amaral D (1978) A Golgi study of cell types in the hilar region of the hippocampus in the rat. J Comp Neurol 15:851–914CrossRef Amaral D (1978) A Golgi study of cell types in the hilar region of the hippocampus in the rat. J Comp Neurol 15:851–914CrossRef
go back to reference Amaral DG, Scharfman HE, Lavenex P (2007) The dentate gyrus: fundamental neuroanatomical organization (dentate gyrus for dummies). Prog Brain Res 163:3–22CrossRefPubMedPubMedCentral Amaral DG, Scharfman HE, Lavenex P (2007) The dentate gyrus: fundamental neuroanatomical organization (dentate gyrus for dummies). Prog Brain Res 163:3–22CrossRefPubMedPubMedCentral
go back to reference Baille-Le Crom V, Collombet JM, Burckhart MF, Foquin A, Pernot-Marino I, Rondouin G, Lallement G (1996) Time course and regional expression of c-fos and HSP 70 in hippocampus and piriform cortex following soman-induced seizures. J Neurosci Res 45:513–524CrossRefPubMed Baille-Le Crom V, Collombet JM, Burckhart MF, Foquin A, Pernot-Marino I, Rondouin G, Lallement G (1996) Time course and regional expression of c-fos and HSP 70 in hippocampus and piriform cortex following soman-induced seizures. J Neurosci Res 45:513–524CrossRefPubMed
go back to reference Bain M, Dwyer S, Rusak B (2004) Restraint stress affects hippocampal cell proliferation differently in rats and mice. Neurosci Lett 368:7–10CrossRefPubMed Bain M, Dwyer S, Rusak B (2004) Restraint stress affects hippocampal cell proliferation differently in rats and mice. Neurosci Lett 368:7–10CrossRefPubMed
go back to reference Barouk S, Hintz T, Li P, Duffy A, Maclusky N, Scharfman H (2011) 17β-estradiol increases astrocytic vascular endothelial growth factor (VEGF) in adult female rat hippocampus. Endocrinology 152:1745–1751CrossRefPubMedPubMedCentral Barouk S, Hintz T, Li P, Duffy A, Maclusky N, Scharfman H (2011) 17β-estradiol increases astrocytic vascular endothelial growth factor (VEGF) in adult female rat hippocampus. Endocrinology 152:1745–1751CrossRefPubMedPubMedCentral
go back to reference Blackstad JB, Osen KK, Scharfman HE, Storm-Mathisen J, Blackstad TW, Leergaard TB (2016) Observations on hippocampal mossy cells in mink (neovison vison) with special reference to dendrites ascending to the granular and molecular layers. Hippocampus 26:229–245CrossRefPubMed Blackstad JB, Osen KK, Scharfman HE, Storm-Mathisen J, Blackstad TW, Leergaard TB (2016) Observations on hippocampal mossy cells in mink (neovison vison) with special reference to dendrites ascending to the granular and molecular layers. Hippocampus 26:229–245CrossRefPubMed
go back to reference Buckmaster PS, Jongen-Relo AL (1999) Highly specific neuron loss preserves lateral inhibitory circuits in the dentate gyrus of kainate-induced epileptic rats. J Neurosci 19:9519–9529PubMed Buckmaster PS, Jongen-Relo AL (1999) Highly specific neuron loss preserves lateral inhibitory circuits in the dentate gyrus of kainate-induced epileptic rats. J Neurosci 19:9519–9529PubMed
go back to reference Buckmaster P, Wenzel H, Kunkel D, Schwartzkroin P (1996) Axon arbors and synaptic connections of hippocampal mossy cells in the rat in vivo. J Comp Neurol 366:271–292CrossRefPubMed Buckmaster P, Wenzel H, Kunkel D, Schwartzkroin P (1996) Axon arbors and synaptic connections of hippocampal mossy cells in the rat in vivo. J Comp Neurol 366:271–292CrossRefPubMed
go back to reference Buzsaki G, Eidelberg E (1981) Commissural projection to the dentate gyrus of the rat: evidence for feed-forward inhibition. Brain Res 230:346–350CrossRefPubMed Buzsaki G, Eidelberg E (1981) Commissural projection to the dentate gyrus of the rat: evidence for feed-forward inhibition. Brain Res 230:346–350CrossRefPubMed
go back to reference Celio MR (1990) Calbindin D-28 k and parvalbumin in the rat nervous system. Neuroscience 35:375–475CrossRefPubMed Celio MR (1990) Calbindin D-28 k and parvalbumin in the rat nervous system. Neuroscience 35:375–475CrossRefPubMed
go back to reference Chowdhury GM, Fujioka T, Nakamura S (2000) Induction and adaptation of fos expression in the rat brain by two types of acute restraint stress. Brain Res Bull 52:171–182CrossRefPubMed Chowdhury GM, Fujioka T, Nakamura S (2000) Induction and adaptation of fos expression in the rat brain by two types of acute restraint stress. Brain Res Bull 52:171–182CrossRefPubMed
go back to reference Collaco-Moraes Y, De Belleroche J (1995) Differential temporal patterns of expression of immediate early genes in cerebral cortex induced by intracerebral excitotoxin injection: sensitivity to dexamethasone and MK-801. Neuropharmacology 34:521–531CrossRefPubMed Collaco-Moraes Y, De Belleroche J (1995) Differential temporal patterns of expression of immediate early genes in cerebral cortex induced by intracerebral excitotoxin injection: sensitivity to dexamethasone and MK-801. Neuropharmacology 34:521–531CrossRefPubMed
go back to reference Conrad C, McEwen B (2000) Acute stress increases neuropeptide Y mRNA within the arcuate nucleus and hilus of the dentate gyrus. Mol Brain Res 79:102–109CrossRefPubMed Conrad C, McEwen B (2000) Acute stress increases neuropeptide Y mRNA within the arcuate nucleus and hilus of the dentate gyrus. Mol Brain Res 79:102–109CrossRefPubMed
go back to reference Deller T, Katona I, Cozzari C, Frotscher M, Freund TF (1999) Cholinergic innervation of mossy cells in the rat fascia dentata. Hippocampus 9:314–320CrossRefPubMed Deller T, Katona I, Cozzari C, Frotscher M, Freund TF (1999) Cholinergic innervation of mossy cells in the rat fascia dentata. Hippocampus 9:314–320CrossRefPubMed
go back to reference Douglas RM, McNaughton BL, Goddard GV (1983) Commissural inhibition and facilitation of granule cell discharge in fascia dentata. J Comp Neurol 219:285–294CrossRefPubMed Douglas RM, McNaughton BL, Goddard GV (1983) Commissural inhibition and facilitation of granule cell discharge in fascia dentata. J Comp Neurol 219:285–294CrossRefPubMed
go back to reference Dragunow M, Faull R (1989) The use of c-fos as a metabolic marker in neuronal pathway tracing. J Neurosci Methods 29:261–265CrossRefPubMed Dragunow M, Faull R (1989) The use of c-fos as a metabolic marker in neuronal pathway tracing. J Neurosci Methods 29:261–265CrossRefPubMed
go back to reference Fa M, Xia L, Anunu R, Kehat O, Kriebel M, Volkmer H, Richter-Levin G (2014) Stress modulation of hippocampal activity–spotlight on the dentate gyrus. Neurobiol Learn Mem 112:53–60CrossRefPubMed Fa M, Xia L, Anunu R, Kehat O, Kriebel M, Volkmer H, Richter-Levin G (2014) Stress modulation of hippocampal activity–spotlight on the dentate gyrus. Neurobiol Learn Mem 112:53–60CrossRefPubMed
go back to reference Fevurly RD, Spencer RL (2004) Fos expression is selectively and differentially regulated by endogenous glucocorticoids in the paraventricular nucleus of the hypothalamus and the dentate gyrus. J Neuroendocrinol 16:970–979CrossRefPubMed Fevurly RD, Spencer RL (2004) Fos expression is selectively and differentially regulated by endogenous glucocorticoids in the paraventricular nucleus of the hypothalamus and the dentate gyrus. J Neuroendocrinol 16:970–979CrossRefPubMed
go back to reference Frotscher M, Seress L, Schwerdtfeger WK, Buhl E (1991) The mossy cells of the fascia dentata: a comparative study of their fine structure and synaptic connections in rodents and primates. J Comp Neurol 312:145–163CrossRefPubMed Frotscher M, Seress L, Schwerdtfeger WK, Buhl E (1991) The mossy cells of the fascia dentata: a comparative study of their fine structure and synaptic connections in rodents and primates. J Comp Neurol 312:145–163CrossRefPubMed
go back to reference Fujikawa T, Soya H, Fukuoka H, Alam K, Yoshizato H, McEwen B, Nakashima K (2000) A biphasic regulation of receptor mRNA expressions for growth hormone, glucocorticoid and mineralocorticoid in the rat dentate gyrus during acute stress. Brain Res 874:186–193CrossRefPubMed Fujikawa T, Soya H, Fukuoka H, Alam K, Yoshizato H, McEwen B, Nakashima K (2000) A biphasic regulation of receptor mRNA expressions for growth hormone, glucocorticoid and mineralocorticoid in the rat dentate gyrus during acute stress. Brain Res 874:186–193CrossRefPubMed
go back to reference Herman J, Watson S (1995) Stress regulation of mineralocorticoid receptor heteronuclear RNA in rat hippocampus. Brain Res 677:243–249CrossRefPubMed Herman J, Watson S (1995) Stress regulation of mineralocorticoid receptor heteronuclear RNA in rat hippocampus. Brain Res 677:243–249CrossRefPubMed
go back to reference Hoffman AN, Anouti DP, Lacagnina MJ, Nikulina EM, Hammer RP Jr, Conrad CD (2013) Experience-dependent effects of context and restraint stress on corticolimbic c-fos expression. Stress 16:587–591CrossRefPubMedPubMedCentral Hoffman AN, Anouti DP, Lacagnina MJ, Nikulina EM, Hammer RP Jr, Conrad CD (2013) Experience-dependent effects of context and restraint stress on corticolimbic c-fos expression. Stress 16:587–591CrossRefPubMedPubMedCentral
go back to reference Hölscher C (1999) Stress impairs performance in spatial water maze learning tasks. Behav Brain Res 100:225–235CrossRefPubMed Hölscher C (1999) Stress impairs performance in spatial water maze learning tasks. Behav Brain Res 100:225–235CrossRefPubMed
go back to reference Hsu T-T, Lee C-T, Tai M-H, Lien C-C (2016) Differential recruitment of dentate gyrus interneuron types by commissural versus perforant pathways. Cereb Cortex 26:2715–2727CrossRefPubMed Hsu T-T, Lee C-T, Tai M-H, Lien C-C (2016) Differential recruitment of dentate gyrus interneuron types by commissural versus perforant pathways. Cereb Cortex 26:2715–2727CrossRefPubMed
go back to reference Jiao Y, Nadler JV (2007) Stereological analysis of Glur2-immunoreactive hilar neurons in the pilocarpine model of temporal lobe epilepsy: correlation of cell loss with mossy fiber sprouting. Exp Neurol 205:569–582CrossRefPubMedPubMedCentral Jiao Y, Nadler JV (2007) Stereological analysis of Glur2-immunoreactive hilar neurons in the pilocarpine model of temporal lobe epilepsy: correlation of cell loss with mossy fiber sprouting. Exp Neurol 205:569–582CrossRefPubMedPubMedCentral
go back to reference Jinde S, Zsiros V, Jiang Z, Nakao K, Pickel J, Kohno K, Belforte JE, Nakazawa K (2012) Hilar mossy cell degeneration causes transient dentate granule cell hyperexcitability and impaired pattern separation. Neuron 76:1189–1200CrossRefPubMedPubMedCentral Jinde S, Zsiros V, Jiang Z, Nakao K, Pickel J, Kohno K, Belforte JE, Nakazawa K (2012) Hilar mossy cell degeneration causes transient dentate granule cell hyperexcitability and impaired pattern separation. Neuron 76:1189–1200CrossRefPubMedPubMedCentral
go back to reference Kheirbek MA, Drew LJ, Burghardt NS, Costantini DO, Tannenholz L, Ahmari SE, Zeng H, Fenton AA, Hen R (2013) Differential control of learning and anxiety along the dorso-ventral axis of the dentate gyrus. Neuron 77:955–968CrossRefPubMedPubMedCentral Kheirbek MA, Drew LJ, Burghardt NS, Costantini DO, Tannenholz L, Ahmari SE, Zeng H, Fenton AA, Hen R (2013) Differential control of learning and anxiety along the dorso-ventral axis of the dentate gyrus. Neuron 77:955–968CrossRefPubMedPubMedCentral
go back to reference Laurberg S, Sorensen KE (1981) Associational and commissural collaterals of neurons in the hippocampal formation (hilus fasciae dentatae and subfield CA3). Brain Res 212:287–300CrossRefPubMed Laurberg S, Sorensen KE (1981) Associational and commissural collaterals of neurons in the hippocampal formation (hilus fasciae dentatae and subfield CA3). Brain Res 212:287–300CrossRefPubMed
go back to reference Law J, Ibarguen-Vargas Y, Belzung C, Surget A (2016) Decline of hippocampal stress reactivity and neuronal ensemble coherence in a mouse model of depression. Psychoneuroendocrinology 67:113–123CrossRefPubMed Law J, Ibarguen-Vargas Y, Belzung C, Surget A (2016) Decline of hippocampal stress reactivity and neuronal ensemble coherence in a mouse model of depression. Psychoneuroendocrinology 67:113–123CrossRefPubMed
go back to reference Le Gal La Salle G (1988) Long-lasting and sequential increase of c-fos oncoprotein expression in kainic acid-induced status epilepticus. Neurosci Lett 88:127–130CrossRefPubMed Le Gal La Salle G (1988) Long-lasting and sequential increase of c-fos oncoprotein expression in kainic acid-induced status epilepticus. Neurosci Lett 88:127–130CrossRefPubMed
go back to reference Leranth C, Szeidemann Z, Hsu M, Buzsáki G (1996) AMPA receptors in the rat and primate hippocampus: a possible absence of glur2/3 subunits in most interneurons. Neuroscience 70:631–652CrossRefPubMed Leranth C, Szeidemann Z, Hsu M, Buzsáki G (1996) AMPA receptors in the rat and primate hippocampus: a possible absence of glur2/3 subunits in most interneurons. Neuroscience 70:631–652CrossRefPubMed
go back to reference McCloskey DP, Hintz TM, Pierce JP, Scharfman HE (2006) Stereological methods reveal the robust size and stability of ectopic hilar granule cells after pilocarpine-induced status epilepticus in the adult rat. Eur J Neurosci 24:2203–2210CrossRefPubMedPubMedCentral McCloskey DP, Hintz TM, Pierce JP, Scharfman HE (2006) Stereological methods reveal the robust size and stability of ectopic hilar granule cells after pilocarpine-induced status epilepticus in the adult rat. Eur J Neurosci 24:2203–2210CrossRefPubMedPubMedCentral
go back to reference McEwen BS, Nasca C, Gray JD (2016) Stress effects on neuronal structure: hippocampus, amygdala, and prefrontal cortex. Neuropsychopharmacology 41:3–23CrossRefPubMed McEwen BS, Nasca C, Gray JD (2016) Stress effects on neuronal structure: hippocampus, amygdala, and prefrontal cortex. Neuropsychopharmacology 41:3–23CrossRefPubMed
go back to reference Mizukawa K, Takayama H, Sato H, Ota Z, Haba K, Ogawa N (1989) Alterations of muscarinic cholinergic receptors in the hippocampal formation of stressed rat: in vitro quantitative autoradiographic analysis. Brain Res 478:187–192CrossRefPubMed Mizukawa K, Takayama H, Sato H, Ota Z, Haba K, Ogawa N (1989) Alterations of muscarinic cholinergic receptors in the hippocampal formation of stressed rat: in vitro quantitative autoradiographic analysis. Brain Res 478:187–192CrossRefPubMed
go back to reference Nativio P, Pascale E, Maffei A, Scaccianoce S, Passarelli F (2012) Effect of stress on hippocampal nociceptin expression in the rat. Stress 15:378–384CrossRefPubMed Nativio P, Pascale E, Maffei A, Scaccianoce S, Passarelli F (2012) Effect of stress on hippocampal nociceptin expression in the rat. Stress 15:378–384CrossRefPubMed
go back to reference Patel A, Bulloch K (2003) Type II glucocorticoid receptor immunoreactivity in the mossy cells of the rat and the mouse hippocampus. Hippocampus 13:59–66CrossRefPubMed Patel A, Bulloch K (2003) Type II glucocorticoid receptor immunoreactivity in the mossy cells of the rat and the mouse hippocampus. Hippocampus 13:59–66CrossRefPubMed
go back to reference Paxinos G, Watson C (2007) The rat brain in stereotaxic coordinates. Elsevier Academic Press, New York Paxinos G, Watson C (2007) The rat brain in stereotaxic coordinates. Elsevier Academic Press, New York
go back to reference Preston GA, Lyon TT, Yin Y, Lang JE, Solomon G, Annab L, Srinivasan DG, Alcorta DA, Barrett JC (1996) Induction of apoptosis by c-fos protein. Mol Cell Biol 16:211–218CrossRefPubMedPubMedCentral Preston GA, Lyon TT, Yin Y, Lang JE, Solomon G, Annab L, Srinivasan DG, Alcorta DA, Barrett JC (1996) Induction of apoptosis by c-fos protein. Mol Cell Biol 16:211–218CrossRefPubMedPubMedCentral
go back to reference Reul JM, de Kloet ER (1985) Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. Endocrinology 117:2505–2511CrossRefPubMed Reul JM, de Kloet ER (1985) Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. Endocrinology 117:2505–2511CrossRefPubMed
go back to reference Reul JM, Collins A, Saliba RS, Mifsud KR, Carter SD, Gutierrez-Mecinas M, Qian X, Linthorst AC (2015) Glucocorticoids, epigenetic control and stress resilience. Neurobiol Stress 1:44–59CrossRefPubMed Reul JM, Collins A, Saliba RS, Mifsud KR, Carter SD, Gutierrez-Mecinas M, Qian X, Linthorst AC (2015) Glucocorticoids, epigenetic control and stress resilience. Neurobiol Stress 1:44–59CrossRefPubMed
go back to reference Ribak CE, Seress L, Amaral DG (1985) The development, ultrastructure and synaptic connections of the mossy cells of the dentate gyrus. J Neurocytol 14:835–857CrossRefPubMed Ribak CE, Seress L, Amaral DG (1985) The development, ultrastructure and synaptic connections of the mossy cells of the dentate gyrus. J Neurocytol 14:835–857CrossRefPubMed
go back to reference Scharfman HE (1991) Dentate hilar cells with dendrites in the molecular layer have lower thresholds for synaptic activation by perforant path than granule cells. J Neurosci 11:1660–1673PubMed Scharfman HE (1991) Dentate hilar cells with dendrites in the molecular layer have lower thresholds for synaptic activation by perforant path than granule cells. J Neurosci 11:1660–1673PubMed
go back to reference Scharfman HE (1993) Characteristics of spontaneous and evoked EPSPs recorded from dentate spiny hilar cells in rat hippocampal slices. J Neurophysiol 70:742–757PubMedPubMedCentral Scharfman HE (1993) Characteristics of spontaneous and evoked EPSPs recorded from dentate spiny hilar cells in rat hippocampal slices. J Neurophysiol 70:742–757PubMedPubMedCentral
go back to reference Scharfman HE (1994) Evidence from simultaneous intracellular recordings in rat hippocampal slices that area CA3 pyramidal cells innervate dentate hilar mossy cells. J Neurophysiol 72:2167–2180PubMed Scharfman HE (1994) Evidence from simultaneous intracellular recordings in rat hippocampal slices that area CA3 pyramidal cells innervate dentate hilar mossy cells. J Neurophysiol 72:2167–2180PubMed
go back to reference Scharfman HE, Myers CE (2012) Hilar mossy cells of the dentate gyrus: a historical perspective. Front Neural Circuits 6:106PubMed Scharfman HE, Myers CE (2012) Hilar mossy cells of the dentate gyrus: a historical perspective. Front Neural Circuits 6:106PubMed
go back to reference Scharfman HE, Schwartzkroin PA (1989) Protection of dentate hilar cells from prolonged stimulation by intracellular calcium chelation. Science 246:257–260CrossRefPubMed Scharfman HE, Schwartzkroin PA (1989) Protection of dentate hilar cells from prolonged stimulation by intracellular calcium chelation. Science 246:257–260CrossRefPubMed
go back to reference Scharfman HE, Sollas AL, Goodman JH (2002) Spontaneous recurrent seizures after pilocarpine-induced status epilepticus activate calbindin-immunoreactive hilar cells of the rat dentate gyrus. Neuroscience 111:71–81CrossRefPubMed Scharfman HE, Sollas AL, Goodman JH (2002) Spontaneous recurrent seizures after pilocarpine-induced status epilepticus activate calbindin-immunoreactive hilar cells of the rat dentate gyrus. Neuroscience 111:71–81CrossRefPubMed
go back to reference Sloviter RS (1991) Permanently altered hippocampal structure, excitability, and inhibition after experimental status epilepticus in the rat: the “dormant basket cell” hypothesis and its possible relevance to temporal lobe epilepsy. Hippocampus 1:41–66CrossRefPubMed Sloviter RS (1991) Permanently altered hippocampal structure, excitability, and inhibition after experimental status epilepticus in the rat: the “dormant basket cell” hypothesis and its possible relevance to temporal lobe epilepsy. Hippocampus 1:41–66CrossRefPubMed
go back to reference Soriano E, Frotscher M (1994) Mossy cells of the rat fascia dentata are glutamate-immunoreactive. Hippocampus 4:65–69CrossRefPubMed Soriano E, Frotscher M (1994) Mossy cells of the rat fascia dentata are glutamate-immunoreactive. Hippocampus 4:65–69CrossRefPubMed
go back to reference Strange B, Witter M, Lein E, Moser E (2014) Functional organization of the hippocampal longitudinal axis. Nat Rev Neurosci 15:655–669CrossRefPubMed Strange B, Witter M, Lein E, Moser E (2014) Functional organization of the hippocampal longitudinal axis. Nat Rev Neurosci 15:655–669CrossRefPubMed
go back to reference Strowbridge BW, Schwartzkroin PA (1996) Transient potentiation of spontaneous EPSPs in rat mossy cells induced by depolarization of a single neurone. J Physiol 494(Pt 2):493–510CrossRefPubMedPubMedCentral Strowbridge BW, Schwartzkroin PA (1996) Transient potentiation of spontaneous EPSPs in rat mossy cells induced by depolarization of a single neurone. J Physiol 494(Pt 2):493–510CrossRefPubMedPubMedCentral
go back to reference Tse Y-C, Lai C-H, Lai S-K, Liu J-X, Yung KKL, Shum DKY, Chan Y-S (2008) Developmental expression of NMDA and AMPA receptor subunits in vestibular nuclear neurons that encode gravity-related horizontal orientations. J Comp Neurol 508:343–364CrossRefPubMed Tse Y-C, Lai C-H, Lai S-K, Liu J-X, Yung KKL, Shum DKY, Chan Y-S (2008) Developmental expression of NMDA and AMPA receptor subunits in vestibular nuclear neurons that encode gravity-related horizontal orientations. J Comp Neurol 508:343–364CrossRefPubMed
go back to reference Volz F, Bock HH, Gierthmuehlen M, Zentner J, Haas CA, Freiman TM (2011) Stereologic estimation of hippocampal GluR2/3- and calretinin-immunoreactive hilar neurons (presumptive mossy cells) in two mouse models of temporal lobe epilepsy. Epilepsia 52:1579–1589CrossRefPubMed Volz F, Bock HH, Gierthmuehlen M, Zentner J, Haas CA, Freiman TM (2011) Stereologic estimation of hippocampal GluR2/3- and calretinin-immunoreactive hilar neurons (presumptive mossy cells) in two mouse models of temporal lobe epilepsy. Epilepsia 52:1579–1589CrossRefPubMed
go back to reference Walling SG, Brown RA, Miyasaka N, Yoshihara Y, Harley CW (2012) Selective wheat germ agglutinin (wga) uptake in the hippocampus from the locus coeruleus of dopamine-beta-hydroxylase-wga transgenic mice. Front Behav Neurosci 6:23CrossRefPubMedPubMedCentral Walling SG, Brown RA, Miyasaka N, Yoshihara Y, Harley CW (2012) Selective wheat germ agglutinin (wga) uptake in the hippocampus from the locus coeruleus of dopamine-beta-hydroxylase-wga transgenic mice. Front Behav Neurosci 6:23CrossRefPubMedPubMedCentral
go back to reference Wenzel HJ, Buckmaster PS, Anderson NL, Wenzel ME, Schwartzkroin PA (1997) Ultrastructural localization of neurotransmitter immunoreactivity in mossy cell axons and their synaptic targets in the rat dentate gyrus. Hippocampus 7:559–570CrossRefPubMed Wenzel HJ, Buckmaster PS, Anderson NL, Wenzel ME, Schwartzkroin PA (1997) Ultrastructural localization of neurotransmitter immunoreactivity in mossy cell axons and their synaptic targets in the rat dentate gyrus. Hippocampus 7:559–570CrossRefPubMed
go back to reference Whisler RL, Chen M, Beiqing L, Carle KW (1997) Impaired induction of c-fos/c-jun genes and of transcriptional regulatory proteins binding distinct c-fos/c-jun promoter elements in activated human t cells during aging. Cell Immunol 175:41–50CrossRefPubMed Whisler RL, Chen M, Beiqing L, Carle KW (1997) Impaired induction of c-fos/c-jun genes and of transcriptional regulatory proteins binding distinct c-fos/c-jun promoter elements in activated human t cells during aging. Cell Immunol 175:41–50CrossRefPubMed
go back to reference Yarom O, Maroun M, Richter-Levin G (2008) Exposure to forced swim stress alters local circuit activity and plasticity in the dentate gyrus of the hippocampus. Neural Plasticity 2008:194097CrossRefPubMedPubMedCentral Yarom O, Maroun M, Richter-Levin G (2008) Exposure to forced swim stress alters local circuit activity and plasticity in the dentate gyrus of the hippocampus. Neural Plasticity 2008:194097CrossRefPubMedPubMedCentral
go back to reference Zimmer LA, Ennis M, El-Etri M, Shipley MT (1997) Anatomical localization and time course of fos expression following soman-induced seizures. J Comp Neurol 378:468–481CrossRefPubMed Zimmer LA, Ennis M, El-Etri M, Shipley MT (1997) Anatomical localization and time course of fos expression following soman-induced seizures. J Comp Neurol 378:468–481CrossRefPubMed
Metadata
Title
Acute restraint stress decreases c-fos immunoreactivity in hilar mossy cells of the adult dentate gyrus
Authors
Jillian N. Moretto
Áine M. Duffy
Helen E. Scharfman
Publication date
01-07-2017
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 5/2017
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-016-1349-z

Other articles of this Issue 5/2017

Brain Structure and Function 5/2017 Go to the issue