Gap junctions in the ventral hippocampal-medial prefrontal pathway are involved in anxiety regulation

Journal of Neuroscience

Volumn 34, Issue 47, 2014, Pages 15679-15688

  Schoenfeld, Timothy J ^a   Kloth, Alexander D ^a   Hsueh, Brian ^a   Runkle, Matthew B ^a   Kane, Gary A ^a   Wang, Samuel S H ^a   Gould, Elizabeth ^a  

^a PRINCETON UNIVERSITY   (United States)

Author keywords

Anxiety; Connexin; Gap junctions; Medial prefrontal cortex; Theta rhythm; Ventral hippocampus

Indexed keywords

CONNEXIN 36; GAP JUNCTION PROTEIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY LABELING; ANXIETY; ARTICLE; BEHAVIOR MODIFICATION; BRAIN ELECTROPHYSIOLOGY; BRAIN FUNCTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELEVATED PLUS MAZE TEST; EXERCISE; FUNCTIONAL NEUROIMAGING; HIPPOCAMPUS; HIPPOCAMPUS THETA RHYTHM; MALE; MOUSE; NONHUMAN; OPEN FIELD TEST; PROTEIN EXPRESSION; QUANTITATIVE ASSAY; SIGNAL TRANSDUCTION; VENTROMEDIAL PREFRONTAL CORTEX; ANIMAL; ANIMAL BEHAVIOR; C57BL MOUSE; DRUG EFFECTS; ELECTROENCEPHALOGRAPHY; GAP JUNCTION; GENETICS; NERVE TRACT; PATHOPHYSIOLOGY; PHYSIOLOGY; PREFRONTAL CORTEX; PSYCHOLOGY; RUNNING; THETA RHYTHM;

ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; CONNEXINS; ELECTROENCEPHALOGRAPHY; GAP JUNCTIONS; HIPPOCAMPUS; MALE; MICE; MICE, INBRED C57BL; NEURAL PATHWAYS; PREFRONTAL CORTEX; RUNNING; THETA RHYTHM;

EID: 84911377862     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3234-13.2014     Document Type: Article

References (54)

1. Adhikari A, Topiwala MA, Gordon JA (2010) Synchronized activity between the ventral hippocampus and the medial prefrontal cortex during anxiety. Neuron 65:257-269. CrossRef Medline
2. Allen K, Fuchs EC, Jaschonek H, Bannerman DM, Monyer H (2011) Gap junctions between interneurons are required for normal spatial coding in the hippocampus and short-term spatial memory. J Neurosci 31:6542- 6552. CrossRef Medline
3. Bannerman DM, Grubb M, Deacon RM, Yee BK, Feldon J, Rawlins JN (2003) Ventral hippocampal lesions affect anxiety but not spatial learning. Behav Brain Res 139:197-213. CrossRef Medline
4. Beaumont M, Maccaferri G (2011) Is connexin36 critical for GABAergic hypersynchronization in the hippocampus? J Physiol 589:1663-1680. CrossRef Medline
5. Bissiere S, Zelikowsky M, Ponnusamy R, Jacobs NS, Blair HT, Fanselow MS (2011) Electrical synapses control hippocampal contributions to fear learning and memory. Science 331:87-91. CrossRef Medline
6. Bocian R, Posłuszny A, Kowalczyk T, Gołebiewski H, Konopacki J (2009) The effect of carbenoxolone on hippocampal formation theta rhythm in rats: in vitro and in vivo approaches. Brain Res Bull 78:290 -298. CrossRef Medline
7. Buzsáki G (2002) Theta oscillations in the hippocampus. Neuron 33:325- 340. CrossRef Medline
8. Cloos JM, Ferreira V (2009) Current use of benzodiazepines in anxiety disorders. Curr Opin Psychiatry 22:90 -95. CrossRef Medline
9. Collignon F, Wetjen NM, Cohen-Gadol AA, Cascino GD, Parisi J, Meyer FB, Marsh WR, Roche P, Weigand SD (2006) Altered expression of connexin subtypes in mesial temporal lobe epilepsy in humans. J Neurosurg 105:77- 87. CrossRef Medline
10. Connors BW (2012) Tales of a dirty drug: carbenoxolone, gap junctions, and seizures. Epilepsy Curr 12:66-68. CrossRef Medline
11. Connors BW, LongMA (2004) Electrical synapses in the mammalian brain. Annu Rev Neurosci 27:393- 418. CrossRef Medline
12. Cornwell BR, Arkin N, Overstreet C, Carver FW, Grillon C (2012) Distinct contributions of human hippocampal theta to spatial cognition and anxiety. Hippocampus 22:1848 -1859. CrossRef Medline
13. Crawley JN (1985) Exploratory behavior models of anxiety in mice. Neurosci Biobehav Rev 9:37- 44. CrossRef Medline
14. Cruikshank SJ, Hopperstad M, Younger M, Connors BW, Spray DC, Srinivas M (2004) Potent block of Cx36 and Cx50 gap junction channels by mefloquine. Proc Natl Acad Sci U S A 101:12364 -12369. CrossRef Medline
15. Dragoi G, Carpi D, Recce M, Csicsvari J, Buzsáki G (1999) Interactions between hippocampus and medial septum during sharp wave and theta oscillation in the behaving rat. J Neurosci 19:6191- 6199. Medline
16. Duman CH, Schlesinger L, Russell DS, Duman RS (2008) Voluntary exercise produces antidepressant and anxiolytic behavioral effects in mice. Brain Res 1199:148 -158. CrossRef Medline
17. Ernst C, Nagy C, Kim S, Yang JP, Deng X, Hellstrom IC, Choi KH, Gershenfeld H, Meaney MJ, Turecki G (2011) Dysfunction of astrocyte connexins 30 and 43 in dorsal lateral prefrontal cortex of suicide completers. Biol Psychiatry 70:312-319. CrossRef Medline
18. Fanselow MS, Dong HW (2010) Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65:7-19. CrossRef Medline
19. Franklin KBJ, Paxinos, G (2008) The mouse brain in stereotaxic coordinates, Ed 3. San Diego: Elsevier Academic.
20. Frisch C, De Souza-Silva MA, Söhl G, Güldenagel M, Willecke K, Huston JP, Dere E (2005) Stimulus complexity dependent memory impairment and changes in motor performance after deletion of the neuronal gap junction protein s36 in mice. Behav Brain Res 157:177-185. CrossRef Medline
21. Gordon JA, Lacefield CO, Kentros CG, Hen R (2005) State-dependent alterations in hippocampal oscillations in serotonin 1A receptor-deficient mice. J Neurosci 25:6509-6519. CrossRef Medline
22. Hartwich K, Pollak T, Klausberger T (2009) Distinct firing patterns of identified basket and dendrite-targeting interneurons in the prefrontal cortex during hippocampal theta and local spindle oscillations. J Neurosci 29: 9563-9574. CrossRef Medline
23. Hasler G, Fromm S, Alvarez RP, Luckenbaugh DA, Drevets WC, Grillon C (2007) Cerebral blood flow in immediate and sustained anxiety. J Neurosci 27:6313- 6319. CrossRef Medline
24. Jones MW, Wilson MA (2005) Phase precession of medial prefrontal cortical activity relative to the hippocampal theta rhythm. Hippocampus 15: 867-873. CrossRef Medline
25. Kalisch R, Wiech K, Critchley HD, Seymour B, O'Doherty JP, Oakley DA, Allen P, Dolan RJ (2005) Anxiety reduction through detachment: subjective, physiological, and neural effects. J Cogn Neurosci 17:874-883. CrossRef Medline
26. Kessler RC, Chiu WT, Demler O, Merikangas KR, Walters EE (2005) Prevalence, severity, and comorbidity of twelve-month DSM-IV disorders in the National Comorbidity Survey Replication (NCS-R). Arch Gen Psychiatry 62:617- 627. CrossRef Medline
27. Klausberger T, Magill PJ, Márton LF, Roberts JD, Cobden PM, Buzsáki G, Somogyi P (2003) Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo. Nature 421:844-848. CrossRef Medline
28. Kozorovitskiy Y, Gross CG, Kopil C, Battaglia L, McBreen M, Stranahan AM, Gould E (2005) Experience induces structural and biochemical changes in the adult primate brain. Proc Natl Acad Sci U S A 102:17478 -17482. CrossRef Medline
29. Lodge DJ, BehrensMM,Grace AA (2009) A loss of parvalbumin-containing interneurons is associated with diminished oscillatory activity in an animal model of schizophrenia. J Neurosci 29:2344 -2354. CrossRef Medline
30. Lorenz RA, Jackson CW, SaitzM (2010) Adjunctive use of atypical antipsychotics for treatment-resistant generalized anxiety disorder. Pharmacotherapy 30:942-951. CrossRef Medline
31. Martin FC, Handforth A (2006) Carbenoxolone and mefloquine suppress tremor in the harmaline mouse model of essential tremor. Mov Disord 21:1641-1649. CrossRef Medline
32. Mc Eown K, Treit D (2010) Inactivation of the dorsal or ventral hippocampus with muscimol differentially affects fear and memory. Brain Res 1353: 145-151. CrossRef Medline
33. McEown K, Treit D (2011) Mineralocorticoid receptors in the medial prefrontal cortex and hippocampus mediate rats' unconditioned fear behaviour. Horm Behav 60:581-588. CrossRef Medline
34. McEown K, Treit D (2013) α2 GABAA receptor sub-units in the ventral hippocampus andα5 GABAA receptor sub-units in the dorsal hippocampus mediate anxiety and fear memory. Neuroscience 252:169 -177. CrossRef Medline
35. McNaughton N, Kocsis B, Hajos M (2007) Elicited hippocampal theta rhythm: a screen for anxiolytic and procognitive drugs through changes in hippocampal function? Behav Pharmacol 18:329 -346. CrossRef Medline
36. O' Keefe J (2007) Hippocampal neurophysiology in the behaving animal. In: The hippocampus book (Andersen P, Morris R, Amaral D, Bliss T, O'Keefe J, eds), pp 475-548. Oxford: Oxford UP.
37. Prochnow N, Abdulazim A, Kurtenbach S, Wildförster V, Dvoriantchikova G, Hanske J, Petrasch-Parwez E, Shestopalov VI, Dermietzel R, Manahan- Vaughan D, Zoidl G (2012) Pannexin1 stabilizes synaptic plasticity and is needed for learning. PLoS One 7:e51767. CrossRef Medline
38. Rouach N, Segal M, Koulakoff A, Giaume C, Avignone E (2003) Carbenoxolone blockade of neuronal network activity in culture is not mediated by an action on gap junctions. J Physiol 553:729 -745. CrossRef Medline
39. Salam JN, Fox JH, Detroy EM, Guignon MH, Wohl DF, Falls WA (2009) Voluntary exercise in C57 mice is anxiolytic across several measures of anxiety. Behav Brain Res 197:31- 40. CrossRef Medline
40. Schoenfeld TJ, Rada P, Pieruzzini PR, Hsueh B, Gould E (2013) Physical exercise prevents stress-induced activation of granule neurons and enhances local inhibitory mechanisms in the dentate gyrus. J Neurosci 33: 7770-7777. CrossRef Medline
41. Shah AA, Sjovold T, Treit D (2004) Inactivation of the medial prefrontal cortex with the GABAA receptor agonist muscimol increases open-arm activity in the elevated plus-maze and attenuates shock-probe burying in rats. Brain Res 1028:112-115. CrossRef Medline
42. Söhl G, Maxeiner S, Willecke K (2005) Expression and functions of neuronal gap junctions. Nat Rev Neurosci 6:191-200. CrossRef Medline
43. Sun JD, Liu Y, Yuan YH, Li J, Chen NH (2012) Gap junction dysfunction in the prefrontal cortex induces depressive-like behaviors in rats. Neuropsychopharmacology 37:1305-1320. CrossRef Medline
44. Thompson AJ, Lummis SC (2008) Antimalarial drugs inhibit human 5-HT(3) and GABA(A) but not GABA(C) receptors. Br J Pharmacol 153: 1686-1696. CrossRef Medline
45. Tovar KR, Maher BJ, Westbrook GL (2009) Direct actions of carbenoxolone on synaptic transmission and neuronal membrane properties. J Neurophysiol 102:974 -978. CrossRef Medline
46. Trejo JL, Llorens-Martin MV, Torres-Alemán I (2008) The effects of exercise on spatial learning and anxiety are mediated by an IGF-1 dependent mechanism related to hippocampal neurogenesis. Mol Cell Neurosci 37: 402-411. CrossRef Medline
47. Walf AA, Frye CA (2007) The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nat Protoc 2:322-328. CrossRef Medline
48. Wells CE, Amos DP, Jeewajee A, Douchamps V, Rodgers J, O'Keefe J, Burgess N, Lever C (2013) Novelty and anxiolytic drugs dissociate two components of hippocampal theta in behaving rats. J Neurosci 33:8650-8667. CrossRef Medline
49. Yeung M, Treit D, Dickson CT (2012) A critical test of the hippocampal theta model of anxiolytic drug action. Neuropharmacology 62:155-160. CrossRef Medline
50. Yeung M, Dickson CT, TreitD (2013a) Intrahippocampal infusion of the Ih blocker ZD7288 slows evoked theta rhythm and produces anxiolytic-like effects in the elevated plus maze. Hippocampus 23:278 -286. CrossRef Medline
51. Yeung M, Lu L, Hughes AM, Treit D, Dickson CT (2013b) FG7142, yohimbine, andβCCE produce anxiogenic-like effects in the elevated plus-maze but do not affect brainstem activated hippocampal theta. Neuropharmacology 75:47-52. CrossRef Medline
52. Zhou C, Xiao C, McArdle JJ, Ye JH (2006) Mefloquine enhances nigral gamma-aminobutyric acid release via inhibition of cholinesterase. J Pharmacol Exp Ther 317:1155-1160. CrossRef Medline
53. Zhu XO, McNaughton N (1994) Effects of long-term administration of antidepressants on septal driving of hippocampal RSA. Int J Neurosci 79:91- 98. Medline
54. Zlomuzica A, Tress O, Binder S, Rovira C, Willecke K, Dere E (2012) Changes in object recognition and anxiety-like behaviour in mice expressing a Cx47 mutation that causes Pelizaeus-Merzbacher-like disease. Dev Neurosci 34:277-287. CrossRef Medline