Dentate Gyrus Local Circuit is Implicated in Learning Under Stress—a Role for Neurofascin

Molecular Neurobiology

Volumn 53, Issue 2, 2016, Pages 842-850

  Zitman, Femke M P ^a   Lucas, Morgan ^a   Trinks, Sabine ^b   Grosse Ophoff, Laura ^a   Kriebel, Martin ^b   Volkmer, Hansjürgen ^b   Richter Levin, Gal ^a  

^a UNIVERSITY OF HAIFA   (Israel)

^b UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Axon initial segment (AIS); GABAA receptor clustering; Hippocampus; Learning impairment

Indexed keywords

CELL ADHESION MOLECULE; NEUROFASCIN; UNCLASSIFIED DRUG; 4 AMINOBUTYRIC ACID RECEPTOR; NERVE GROWTH FACTOR; NFASC PROTEIN, RAT;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; ELECTROPHYSIOLOGY; ENZYME INHIBITION; FEEDBACK SYSTEM; IN VIVO STUDY; LEARNING; LEARNING AND MEMORY TEST; MALE; NONHUMAN; RAT; STRESS; TASK PERFORMANCE; TWO WAY SHUTTLE AVOIDANCE TASK; ANIMAL; ANIMAL BEHAVIOR; AVOIDANCE BEHAVIOR; AXON; ELECTROSTIMULATION; GENE SILENCING; LONG TERM POTENTIATION; MENTAL STRESS; METABOLISM; NERVE TRACT; SPRAGUE DAWLEY RAT;

ANIMALS; AVOIDANCE LEARNING; AXONS; BEHAVIOR, ANIMAL; CELL ADHESION MOLECULES; DENTATE GYRUS; ELECTRIC STIMULATION; GABAERGIC NEURONS; GENE KNOCKDOWN TECHNIQUES; LEARNING; LONG-TERM POTENTIATION; MALE; NERVE GROWTH FACTORS; NEURAL PATHWAYS; RATS, SPRAGUE-DAWLEY; STRESS, PSYCHOLOGICAL;

EID: 84958114153     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-014-9044-7     Document Type: Article

References (26)

1. Halasy K, Somogyi P (1993) Subdivisions in the multiple GABAergic innervation of granule cells in the dentate gyrus of the rat hippocampus. Eur J Neurosci 5:411–429
2. Nusser Z, Sieghart W, Benke D, Fritschy JM, Somogyi P (1996) Differential synaptic localization of two major gamma-aminobutyric acid type A receptor alpha subunits on hippocampal pyramidal cells. Proc Natl Acad Sci U S A 93:11939–11944
3. Somogyi P, Fritschy JM, Benke D, Roberts JD, Sieghart W (1996) The gamma 2 subunit of the GABAA receptor is concentrated in synaptic junctions containing the alpha 1 and beta 2/3 subunits in hippocampus, cerebellum and globus pallidus. Neuropharmacology 35:1425–1444
4. Buhl EH, Han ZS, Lorinczi Z, Stezhka VV, Karnup SV, Somogyi P (1994) Physiological properties of anatomically identified axo-axonic cells in the rat hippocampus. J Neurophysiol 71:1289–1307
5. Freund TF, Buzsaki G (1996) Interneurons of the hippocampus. Hippocampus 6:347–470
6. Douglas RJ, Martin KAC (1990) Control of neuronal output by inhibition at the axon initial segment. Neural Comput 2:283–292
7. Burkarth N, Kriebel M, Kranz EU, Volkmer H (2007) Neurofascin regulates the formation of gephyrin clusters and their subsequent translocation to the axon hillock of hippocampal neurons. Mol Cell Neurosci 36:59–70
8. Kriebel M, Metzger J, Trinks S, Chugh D, Harvey RJ, Harvey K, Volkmer H (2011) The cell adhesion molecule neurofascin stabilizes axo-axonic GABAergic terminals at the axon initial segment. J Biol Chem 286:24385–24393
9. Buzsaki G, Eidelberg E (1981) Commissural projection to the dentate gyrus of the rat: evidence for feed-forward inhibition. Brain Res 230:346–350
10. Sloviter RS (1991) Feedforward and feedback inhibition of hippocampal principal cell activity evoked by perforant path stimulation: GABA-mediated mechanisms that regulate excitability in vivo. Hippocampus 1:31–40
11. Richter-Levin G, Greenberger V, Segal M (1994) The effects of general and restricted serotonergic lesions on hippocampal electrophysiology and behavior. Brain Res 642:111–116
12. Rosenblum K, Maroun M, Richter-Levin G (1999) Frequency-dependent inhibition in the dentate gyrus is attenuated by the NMDA receptor blocker MK-801 at doses that do not yet affect long-term potentiation. Hippocampus 9:491–494
13. Ribak CE, Seress L, Peterson GM, Seroogy KB, Fallon JH, Schmued LC (1986) A GABAergic inhibitory component within the hippocampal commissural pathway. J Neurosci 6:3492–3498
14. 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 112:53–60
15. Kriebel M, Wuchter J, Trinks S, Volkmer H (2012) Neurofascin: a switch between neuronal plasticity and stability. Int J Biochem Cell Biol 44:694–697
16. Zhu Y, Stornetta RL, Zhu JJ (2004) Chandelier cells control excessive cortical excitation: characteristics of whisker-evoked synaptic responses of layer 2/3 nonpyramidal and pyramidal neurons. J Neurosci 24:5101–5108
17. Szabadics J, Varga C, Molnar G, Olah S, Barzo P, Tamas G (2006) Excitatory effect of GABAergic axo-axonic cells in cortical microcircuits. Science 311:233–235
18. Woodruff AR, McGarry LM, Vogels TP, Inan M, Anderson SA, Yuste R (2011) State-dependent function of neocortical chandelier cells. J Neurosci 31:17872–17886
19. 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 Plast 2008:194097
20. Zitman FM, Richter-Levin G (2013) Age and sex-dependent differences in activity, plasticity and response to stress in the dentate gyrus. Neuroscience 249:21–30
21. Cullinan WE, Wolfe TJ (2000) Chronic stress regulates levels of mRNA transcripts encoding beta subunits of the GABA(A) receptor in the rat stress axis. Brain Res 887:118–124
22. Hsu FC, Zhang GJ, Raol YS, Valentino RJ, Coulter DA, Brooks-Kayal AR (2003) Repeated neonatal handling with maternal separation permanently alters hippocampal GABAA receptors and behavioral stress responses. Proc Natl Acad Sci U S A 100:12213–12218
23. Jacobson-Pick S, Richter-Levin G (2012) Short- and long-term effects of juvenile stressor exposure on the expression of GABAA receptor subunits in rats. Stress 15:416–424
24. Jacobson-Pick S, Elkobi A, Vander S, Rosenblum K, Richter-Levin G (2008) Juvenile stress-induced alteration of maturation of the GABAA receptor alpha subunit in the rat. Int J Neuropsychopharmacol 11:891–903
25. Horovitz O, Tsoory MM, Hall J, Jacobson-Pick S, Richter-Levin G (2012) Post-weaning to pre-pubertal (‘juvenile’) stress: a model of induced predisposition to stress-related disorders. Neuroendocrinology 95:56–64
26. Tsoory M, Cohen H, Richter-Levin G (2007) Juvenile stress induces a predisposition to either anxiety or depressive-like symptoms following stress in adulthood. Eur Neuropsychopharmacol 17:245–256