Munc18-1 haploinsufficiency results in enhanced anxiety-like behavior as determined by heart rate responses in mice

Behavioural Brain Research

Volumn 260, Issue , 2014, Pages 44-52

  Hager, Torben ^a,b   Maroteaux, Grégoire ^a   Pont, Paula du ^a   Julsing, Joris ^a   van Vliet, Rick ^a   Stiedl, Oliver ^a  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

^b Sylics (Synaptologics BV)   (Netherlands)

Author keywords

Autonomic measures; Coping style; Diurnal changes; Fear conditioning; Heart rate variability; Nonlinear analysis

Indexed keywords

MEMBRANE PROTEIN; MUNC18 1 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; AUTONOMIC NERVOUS SYSTEM FUNCTION; CONTROLLED STUDY; EMOTION; FEAR; GENE DELETION; HAPLOINSUFFICIENCY; HEART RATE; HEART RATE VARIABILITY; HETEROZYGOSITY; LEARNING DISORDER; MALE; MILD COGNITIVE IMPAIRMENT; MOUSE; NONHUMAN; PRIORITY JOURNAL; REINFORCEMENT; WILD TYPE;

ANALYSIS OF VARIANCE; ANOVA; ANS; AUTONOMIC MEASURES; AUTONOMIC NERVOUS SYSTEM; BEATS PER MINUTE; BPM; CONDITIONED STIMULUS; COPING STYLE; CS; DETRENDED FLUCTUATION ANALYSIS; DFA; DIURNAL CHANGES; ECG; ELECTROCARDIOGRAM; FEAR CONDITIONING; HEART RATE; HEART RATE VARIABILITY; HETEROZYGOUS; HR; HRV; HZ; NONLINEAR ANALYSIS; PARASYMPATHETIC NERVOUS SYSTEM; PNS; POSTTRAUMATIC STRESS DISORDER; PTSD; RMSSD; ROOT MEAN SQUARE SUCCESSIVE DIFFERENCE; SNAP (SOLUBLE NSF ATTACHMENT PROTEIN) RECEPTOR; SNARE; SNS; SOUND PRESSURE LEVEL; SPL; SYMPATHETIC NERVOUS SYSTEM; UNCONDITIONED STIMULUS; US; WILD-TYPE; WT;

ANIMALS; ANXIETY; AUDITORY PERCEPTION; CIRCADIAN RHYTHM; CONDITIONING, CLASSICAL; EXTINCTION, PSYCHOLOGICAL; FEAR; HAPLOINSUFFICIENCY; HEART RATE; MALE; MICE; MICE, INBRED C57BL; MOTOR ACTIVITY; MUNC18 PROTEINS; RECOGNITION (PSYCHOLOGY);

EID: 84890280758     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2013.11.033     Document Type: Article

References (46)

1. Südhof T.C., Rothman J.E. Membrane fusion: grappling with SNARE and SM proteins. Science 2009, 323:474-477.
2. Verhage M., Maia A.S., Plomp J.J., Brussaard A.B., Heeroma J.H., Vermeer H., et al. Synaptic assembly of the brain in the absence of neurotransmitter secretion. Science 2000, 287:864-869.
3. Toonen R.F. Role of Munc18-1 in synaptic vesicle and large dense-core vesicle secretion. Biochem Soc Trans 2003, 31:848-850.
4. Saitsu H., Kato M., Mizuguchi T., Hamada K., Osaka H., Tohyama J., et al. De novo mutations in the gene encoding STXBP1 (MUNC18-1) cause early infantile epileptic encephalopathy. Nat Genet 2008, 40:782-788.
5. Toonen R.F.G., Wierda K., Sons M.S., de Wit H., Cornelisse L.N., Verhage M. Munc18-1 expression levels control synapse recovery by regulating readily releasable pool size. Proc Natl Acad Sci USA 2006, 103:18332-18337.
6. Maroteaux G, Hager T, Hensbroek R, Loos M, Koopmans B, Youn J, et al. Het-erozygous munc18-1 mice exhibit an increased anxiety-like phenotype but no cognitive impairment. 2014 [in preparation].
7. Berntson G.G., Sarter M., Cacioppo J.T. Anxiety and cardiovascular reactivity: the basal forebrain cholinergic link. Behav Brain Res 1998, 94:225-248.
8. Stiedl O., Jansen R.F., Pieneman A.W., Ögren S.O., Meyer M. Assessing emotional states through the heart in mice: implications for cardiovascular dysregulation in affective disorders. Neurosci Biobehav Rev 2009, 33:181-190.
9. Myers K.M., Davis M. Mechanisms of fear extinction. Mol Psychiatry 2007, 12:120-150.
10. Quirk G.J., Mueller D. Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology 2008, 33:56-72.
11. Wittchen H.U., Jacobi F., Rehm J., Gustavsson A., Svensson M., Jönsson B., et al. The size and burden of mental disorders and other disorders of the brain in Europe 2010. Eur Neuropsychopharmacol 2011, 21:655-679.
12. Vieweg W.V., Julius D.A., Fernandez A., Beatty-Brooks M., Hettema J.M., Pandurangi A.K. Posttraumatic stress disorder: clinical features, pathophysiology, and treatment. Am J Med 2006, 119:383-390.
13. Sotres-Bayon F., Cain C.K., LeDoux J.E. Brain mechanisms of fear extinction: historical perspectives on the contribution of prefrontal cortex. Biol Psychiatry 2006, 60:329-336.
14. Maren S. Seeking a spotless mind: extinction, deconsolidation, and erasure of fear memory. Neuron 2011, 70:830-845.
15. Stiedl O., Radulovic J., Lohmann R., Palve M., Birkenfeld K., Kammermeier J., et al. Strain and substrain differences in context- and tone-dependent fear conditioning. Behav Brain Res 1999, 104:1-12.
16. Misane I., Tovote P., Meyer M., Spiess J., Ögren S.O., Stiedl O. Time-dependent involvement of the dorsal hippocampus in trace fear conditioning in mice. Hippocampus 2005, 15:418-426.
17. Chowdhury N., Quinn J.J., Fanselow M.S. Dorsal hippocampus involvement in trace fear conditioning with long, but not short, trace intervals in mice. Behav Neurosci 2005, 119:1396-1402.
18. Rozanski A., Blumenthal J.A., Kaplan J. Impact of psychological factors on the pathogenesis of cardiovascular disease and implications for therapy. Circulation 1999, 99:2192-2217.
19. Cohen H., Kotler M., Matar M.A., Kaplan Z., Loewenthal U., Miodownik H., et al. Analysis of heart rate variability in posttraumatic stress disorder patients in response to a trauma-related reminder. Biol Psychiatry 1997, 44:9.
20. Agorastos A., Boel J.A., Heppner P.S., Hager T., Moeller-Bertram T., Haji U., et al. Diminished vagal activity and blunted diurnal variation of heart rate dynamics in posttraumatic stress disorder. Stress 2013, 16:300-310.
21. Langan Y., Nashef L., Sander J.W. Sudden unexpected death in epilepsy: a series of witnessed deaths. J Neurol Neurosurg Psychiatry 2000, 68:211-213.
22. Dinan A., de Toffol B., Pallix M., Breard G., Babuty D. Cardiac arrest: it's all in the head. Lancet 2008, 371:1476.
23. Kalume F., Westenbroek R.E., Cheah C.S., Yu F.H., Oakley J.C., Scheuer T., et al. Sudden unexpected death in a mouse model of Dravet syndrome. J Clin Invest 2013, 123:1798-1808.
24. Maren S., Holt W. The hippocampus and contextual memory retrieval in Pavlovian conditioning. Behav Brain Res 2000, 110:97-108.
25. Maroteaux G., Loos M., van der Sluis S., Koopmans B., Aarts E., van Gassen K., et al. High-throughput phenotyping of avoidance learning in mice discriminates different genotypes and identifies a novel gene. Genes Brain Behav 2012, 11:772-784.
26. Tovote P., Meyer M., Beck-Sickinger A.G., von Hörsten S., Ögren S.O., Spiess J., et al. Central NPY receptor-mediated alteration of heart rate dynamics in mice during expression of fear conditioned to an auditory cue. Regul Pept 2004, 120:205-214.
27. Lubow R.E., Moore A.U. Latent inhibition: the effect of nonreinforced pre-exposure to the conditional stimulus. J Comp Physiol Psychol 1959, 52:415-419.
28. Peng C.K., Havlin S., Stanley H.E., Goldberger A.L. Quantification of scaling exponents and crossover phenomena in nonstationary heartbeat time series. Chaos 1995, 5:82-87.
29. Meyer M. Fractal scaling in health and disease. Fractals in Biology and Medicine 2002, vol. 3:181-193. Birkhäuser, Basel.
30. Stiedl O., Meyer M. Cardiac dynamics in corticotropin-releasing factor receptor subtype-2 deficient mice. Neuropeptides 2003, 37:3-16.
31. Stiedl O., Meyer M. Fractal dynamics in circadian cardiac time series of corticotropin-releasing factor receptor subtype-2 deficient mice. J Math Biol 2003, 47:169-197.
32. Koolhaas J.M., Bartolumucci A., Buwalda B., de Boer S.F., Flügge G., Korte M., et al. Stress revisited: a critical evaluation of the stress concept. Neurosci Biobehav Rev 2011, 35:1291-1301.
33. Lodhi I.J., Semenkovich C.F. Why we should put clothes on mice. Cell Metab 2009, 9:111-112.
34. Peng C.K., Buldyrev S.V., Hausdorff J.M., Mietus J.E., Simons M., Stanley H.E., et al. Non-equilibrium dynamics as an indispensable characteristic of a healthy biological system. Int Physiol Behav Sci 1994, 29:283-293.
35. Meyer M., Stiedl O. Fractal rigidity by enhanced sympatho-vagal antagonism in heartbeat interval dynamics elicited by central application of corticotropin-releasing factor in mice. J Math Biol 2006, 52:830-874.
36. Kim J.J., Diamond D.M. The stressed hippocampus, synaptic plasticity and lost memories. Nat Rev Neurosci 2002, 3:453-462.
37. Diamond D.M., Campbell A.M., Park C.R., Halonen J., Zoladz P.R. The temporal dynamics model of emotional memory processing: a synthesis on the neurobiological basis of stress-induced amnesia, flashbulb and traumatic memories, and the Yerkes-Dodson Law. Neural Plast 2007, 6080:3.
38. Stiedl O., Spiess J. Effect of tone-dependent fear conditioning on heart rate and behavior of C57BL/6 mice. Behav Neurosci 1997, 111:703-711.
39. 1A receptor-mediated modulation of heart rate dynamics and its adjustment by conditioned and unconditioned fear in mice. Br J Pharmacol 2013, 170:859-870.
40. Lipkind D., Sakov A., Kafkafi N., Elmer G.I., Benjamini Y., Golani I. New replicable anxiety-related measures of wall vs. center behavior of mice in the open field. J Appl Physiol 2004, 97:347-359.
41. Baarendse P.J.J., van Grootheest G., Jansen R.F., Pieneman A.W., Ögren S.O., Verhage M., et al. Differential involvement of the dorsal hippocampus in passive avoidance in C57BL/6J and DBA/2J mice. Hippocampus 2008, 18:11-19.
42. Radulovic J., Kammermeier J., Spiess J. Generalization of fear responses in C57BL/6N mice subjected to one-trial foreground contextual fear conditioning. Behav Brain Res 1998, 95:179-189.
43. Hager T., Manivannan S.N., Youn J., Pieneman A.W., Jansen R.F., Stiedl O. Comparison of conditioned fear behavior of C57BL/6 substrains in classical tests versus an automated home cage (DualCage) environment. Society for Neuroscience Meeting 2012, [abstract 399.01].
44. Koolhaas J.M., de Boer S.F., Buwalda B., van Reenen K. Individual variation in coping with stress: a multidimensional approach of ultimate and proximate mechanisms. Brain Behav Evol 2007, 70:218-226.
45. Urbach Y.K., Bode F.J., Nguyen H.P., Riess O., von Hörsten S. Neurobehavioral tests in rat models of degenerative brain diseases. Methods Mol Biol 2010, 597:333-356.
46. Leblond C.S., Heinrich J., Delorme R., Proepper C., Betancur C., Huguet G., et al. Genetic and functional analyses of SHANK2 mutations suggest a multiple hit model of autism spectrum disorders. PLoS Genet 2012, 8:e1002521.