Effects of combined exposure to pyridostigmine bromide and shaker stress on acoustic startle response, pre-pulse inhibition and open field behavior in mice

Journal of Applied Toxicology

Volumn 27, Issue 3, 2007, Pages 276-283

  Dubovicky, Michal ^a,b   Paton, S ^a   Morris, M ^a   Mach, M ^a,b   Lucot, J B ^a  

^a WRIGHT STATE UNIVERSITY   (United States)

^b INSTITUTE OF EXPERIMENTAL PHARMACOLOGY AND TOXICOLOGY   (Slovakia)

Author keywords

Acoustic startle response; Mice; Open field; Pre pulse inhibition; Pyridostigmine bromide; Stress

Indexed keywords

PYRIDOSTIGMINE;

ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR CHANGE; CONTROLLED STUDY; DRUG EXPOSURE; LOCOMOTION; MALE; MOUSE; NONHUMAN; OPEN FIELD BEHAVIOR; OSMOTIC PUMP; PRIORITY JOURNAL; STARTLE REFLEX; STRESS;

ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; CHOLINESTERASE INHIBITORS; EXPLORATORY BEHAVIOR; INFUSION PUMPS, IMPLANTABLE; INJECTIONS, SUBCUTANEOUS; MALE; MICE; MICE, INBRED C57BL; MOTOR ACTIVITY; MOVEMENT; NEURAL INHIBITION; PYRIDOSTIGMINE BROMIDE; STARTLE REACTION; STRESS, MECHANICAL; TIME FACTORS; TOXICITY TESTS;

MUS;

EID: 34247486646     PISSN: 0260437X     EISSN: 10991263     Source Type: Journal    
DOI: 10.1002/jat.1210     Document Type: Article

References (68)

1. Abou-Donia MB, Goldstein LB, Jones KH, Abdel-Rahman AA, Damodaran TV, Dechkovskaia AM, Bullman SL, Amir BE, Khan WA. 2001. Locomotor and sensorimotor performance deficit in rats following exposure to pyridostigmine bromide, DEET, and permethrin, alone and in combination. Toxicol. Sci. 60: 305-314.
2. Acri JB. 1994. Nicotine modulates effects of stress on acoustic startle reflexes in rats: dependence on dose, stressor and initial reactivity. Psychopharmacology (Berl.) 116: 255-265.
3. Aguilar R, Gil L, Tobena A, Escorihuela RM, Fernandez-Teruel A. 2000. Differential effects of cohort removal stress on the acoustic startle response of the Roman/Verh rat strains. Behav. Genet. 30: 71-75.
4. American Psychiatric Association. 2000. Diagnostic and Statistical Manual of Mental Disorders. American Psychiatric Association: Washington, DC.
5. Beck KD, Brennan FX, Moldow RL, Ottenweller JE, Zhu G, Servatius RJ. 2003. Stress interacts with peripheral cholinesterase inhibitors to cause central nervous system effects. Life Sci. 73: 41-45.
6. Beck KD, Hsu M, Jiao X, Servatius RJ. 2006. Cholinergic overstimulation supports conditioned-facilitated startle but not conditioned hyperalgesia. Pharmacol. Biochem. Behav. 84: 400-405.
7. Bernatova I, Dubovicky M, Price WA, Grubbs RD, Lucot JB, Morris M. 2003. Effect of chronic pyridostigmine bromide treatment on cardiovascular and behavioral parameters in mice. Pharmacol. Biochem. Behav. 74: 901-907.
8. Bernatova I, Key MP, Lucot JB, Morris M. 2002. Circadian differences in stress-induced pressor activity on mice. Hypertension 40: 768-773.
9. Bernatova I, Rigatto KV, Key MP, Morris M. 2004. Stress-induced pressor and corticosterone responses in oxytocin-deficient mice. Exp. Physiol. 89: 549-557.
10. Blick DV, Murphy MR, Brown GC, Yochmowitz MG, Fanton JW, Hartgraves SL. 1994. Acute behavioral toxicity of pyridostigmine or soman in primates. Toxicol. Appl. Pharmacol. 126: 311-318.
11. Breyer-Pfaff U, Maier U, Brinkmann AM, Schuman F. 1985. Pyridostigmine kinetics in healthy subjects and patients with myasthenia gravis. Clin. Pharmacol. Ther. 37: 495-501.
12. Butler R, Braff D, Rausch J, Jenkins M, Sprock J, Meyer M. 1990. Physiological evidence of exaggerated startle response in a subgroup of Vietnam veterans with combat related PTSD. Am. J. Psychiatry 147: 1308-1311.
13. Carlson S, Willott JF. 1998. Caudal pontine reticular formation of C57BL/6J mice: responses to startle stimuli, inhibition by tones, and plasticity. J. Neurophysiol. 79: 2603-2614.
14. Cook JE, Kolka MA, Wenger CB. 1992. Chronic pyridostigmine bromide administration: side effects among soldiers working in desert environment. Mil. Med. 157: 250-254.
15. Davis M. 1989. Sensitization of the acoustic startle reflex by foot-shock. Behav. Neurosci. 103: 495-503.
16. Dubovicky M, Skultetyova S, Jezova D. 1999. Neonatal stress alters habituation of exploratory behavior in adult male but not female rats. Pharmacol. Biochem. Behav. 64: 681-686.
17. Esposito P, Gheorghe D, Kandere K, Pang X, Connolly R, Jacobson S, Theoharides TC. 2001. Acute stress increases permeability of the blood-brain-barrier through activation of brain mast cells. Brain Res. 888: 117-127.
18. Friedman A, Kaufer D, Shemer J, Hendler I, Soreq H, Tur-Kaspa I. 1996. Pyridostigmine bromide brain penetration under stress enhances neuronal excitability and induces early immediate transcriptional response. Nat. Med. 2: 1382-1385.
19. Gilbert SG, Grant-Webster KS. 1995. Neurobehavioral effects of developmental methylmercury exposure. Environ. Health Perspect. 103: 135-142.
20. Golomb BA (ed.). 1999. Pyridostigmine Bromide Vol 2. Rand Corporation: Santa Monica, CA.
21. Grauer E, Alkalai D, Kapon J, Cohen G, Raveh L. 2000. Stress does not enable pyridostigmine to inhibit brain cholinesterase after parenteral administration. Toxicol. Appl. Pharmacol. 164: 301-304.
22. Grillon C, Morgan CA, Southwick SM, Davis M, Charney DS. 1996. Baseline startle amplitude and prepulse inhibition in Vietnam veterans with posttraumatic stress disorder. Psychiat. Res. 64: 169-178.
23. Grubbs RD, Price WA, Mauck BS, Ropp SA, Bernatova I, Paton SJ, Morris M, Lucot JB, Cool DR. 2002. Regional differences in brain cholinesterase activity and protein expression in mice following subacute stress and exposure to pyridostigmine bromide. Bioscience Reviews, US Army Medical Defense: Abstract Program Book: 118.
24. Haley RW, Kurt TL. 1997. Self-reported exposure to neurotoxic chemical combinations in the Gulf war. JAMA 277: 231-237.
25. Hall FS, Huang S, Fong G. 1997. Effects of isolation-rearing on acoustic startle and pre-pulse inhibition in Wistar and fawn hooded rats. Ann. N.Y. Acad. Sci. 821: 542-544.
26. Hardman JG, GoodmanA, Gilman A, Limbird LE. 1995. Goodman and Gilman's Pharmacological Basis of Therapeutics. McGraw-Hill, Health Professions Division: New York.
27. Hoy JB, Cody BA, Karlix JL, Schmidt CJ, Tebbett IR, Toffolo S, van Haaren F, Wielbo D. 1999. Pyridostigmine bromide alters locomotion and thigmotaxis of rats: gender effects. Pharmacol. Biochem. Behav. 63: 401-406.
28. Hoy JB, Cornell JA, Karlix JL, Schmidt CJ, Tebbett IR, van Haaren F. 2000a. Interactions of pyridostigmine bromide, DEET, and permethrin alter locomotor behavior of rats. Vet. Hum. Toxicol. 42: 65-71.
29. Hoy JB, Cornell JA, Karlix JL, Tebbett IR, van Haaren F. 2000b. Repeated coadministrations of pyridostigmine bromide, DEET, and permethrin alter locomotor behavior of rats. Vet. Hum. Toxicol. 42: 72-76.
30. Institute of Medicine. 1995. Health Consequences of Service during the Persian Gulf War: Initial Findings and Recommendations for Immediate Action. National Academy Press: Washington, D.C.
31. Institute of Medicine. 2000. Depleted Uranium, Sarin, Pyridostigmine Bromide, Vaccines. (Vol. I). National Academy Press: Washington, D.C.
32. Jones CK, Shannon HE. 2000. Muscarinic cholinergic modulation of prepulse inhibition of the acoustic startle reflex. J. Pharmacol. Exp. Ther. 294: 1017-1023.
33. Knoke JD, Smith TC, Gray GC, Kaiser KS, Hawksworth AW. 2000. Factor analysis of self-reported symptoms: Does it identify a Gulf War syndrome? Am. J. Epidemiol. 152: 379-388.
34. Koch M. 1999. The neurobiology of startle. Progr. Neurobiol. 59: 107-128.
35. Koch M, Kungel M, Herbert H. 1993. Cholinergic neurons in the pedunculopontine tegmental nucleus are involved in the mediation of prepulse inhibition of the acoustic startle response in the rat. Exp. Brain Res. 97: 71-82.
36. Lallement G, Foquin A, Baubichon D, Burckhart MF, Carpentier P, Canini F. 1998. Heat stress, even extreme, does not induce penetration of pyridostigmine into the brain of guinea pigs. NeuroToxicology 19: 759-766.
37. Lim DK, Hoskins IB, Rockhold W, Ho IK. 1989. Comparative studies of muscarinic and dopamine receptors in three strains of rat. Eur. J. Pharmacol. 165: 279-287.
38. Lingenhohl K, Friauf E. 1994. Giant neurons in the rat reticular formation: a sensorimotor interface in the elementary acoustic startle circuit? J. Neurosci. 14: 1176-1194.
39. Loewenstein-Lichtenstein Y, Schwarz M, Glick D, Norgaard-Pedersen B, Zakut H, Soreq H. 1995. Genetic predisposition to adverse consequences of anti-cholinesterases in 'atypical' BCHE carriers. Nat. Med. 1: 1082-1085.
40. Mach M, Grubbs RD, Price WA, Paton SJ, Lucot JB. 2004. Behavioral changes after acetylcholinesterase inhibition with physostigmine in mice. Pharmacol. Biochem. Behav. 79: 533-540.
41. Mach M, Morris M, Dubovick M, Ujházy E, Lucot B. 2005. Behavioral phenotyping of oxytocin deficient mice exposed to acute shaker stress. In Proceedings of Measuring Behavior 2005, 5th International Conference on Methods and Techniques in Behavioral Research, Noldus LPJJ, Grieco F, Loijens LWS, Zimmerman PH (eds). Noldus Information Technology: Wageningen; 431-432.
42. Morgan CAI, Grillon C, Southwick SM, Davis M, Charney DS. 1996. Exaggerated acoustic startle reflex in Gulf War veterans with posttraumatic stress disorder. Am. J. Psychiatry 153: 64-68.
43. Nakata T, Berard W, Kogosov E, Alexander N. 1993. Cardiovascular change and hypothalamic norepinephrine release in response to environmental stress. Am. J. Physiol. 264: 784-789.
44. Nishioka T, Anselmo-Franci JA, Li P, Callahan MF, Morris M. 1998. Stress increases oxytocin release within the hypothalamic paraventricular nucleus. Brain Res. 781: 56-60.
45. Patrick CJ, Berthot BD, Moore JD. 1996. Diazepam blocks fear-potentiated startle in humans. J. Abnorm. Psychol. 105: 89-96.
46. Rigatto K, Puryer R, Bernatova I, Morris M. 2003. Salt appetite and the renin-angiotensin system: effect of oxytocin deficiency. Hypertension 42: 793-797.
47. Ropp S, Bernatova I, Paton SJ, Price WA, Morris M, Cool DR. 2002. SELDI-TOF mass spectrometry proteomic analysis of pyridostigmine bromide and stress on the HP-axis. Toxicol. Sci. 66: 221-222.
48. Sapolsky RM. 1998. The stress of Gulf War syndrome. Nature 393: 308-309.
49. Schanbacher A, Koch M, Pilz PKD, Schnitzler HU. 1996. Lesions of the amygdala do not affect the enhancement of the acoustic startle response by background noise. Physiol. Behav. 60: 1341-1346.
50. Servatius RJ, Ottenweller JE, Beldowicz D, Guo W, Zhu GP, Natelson BH. 1998. Exaggerated startle responses in rats treated with pyridostigmine bromide. J. Pharmacol. Exp. Ther. 287: 1020-1028.
51. Servatius RJ, Ottenweller JE, Guo W, Beldowicz D, Zhu G, Natelson BH. 2000. Effects of inescapable stress and treatment with pyridostigmine bromide on plasma butyrylcholinesterase and the acoustic startle response in rats. Physiol. Behav. 69: 239-246.
52. Servatius RJ, Ottenweller JE, Natelson BH. 1994. Persistent stress-induced sensitization of adrenocortical and startle responses. Physiol. Behav. 56: 945-954.
53. Servatius R, Ottenweller J, Natelson B. 1995. Delayed startle sensitization distinguishes rats exposed to one or three stress sessions: Further evidence toward an animal model of PTSD. Biol. Psychol. 38: 539-546.
54. Sharma HS, Cervós-Navarro J, Dey PK. 1991. Increased blood-brain barrier permeability following acute short-term swimming exercise in conscious normotensive young rats. Neurosci. Res. 10: 211-221.
55. Shors TJ, Servatius RJ. 1995. Stress-induced sensitization and facilitated learning require NMDA receptor activation. Neuroreport 6: 677-680.
56. Sillanpaa MC, Agar LM, Axelrod BN. 1999. Minnesota Multiphasic Personality Inventory-2 validity patterns: an eluidation of Gulf War syndrome. Mil. Med. 164: 261-263.
57. Sinton CM, Fitch TE, Petty F, Haley RW. 2000. Stressful manipulations that elevate corticosterone reduce blood-brain barrier permeability to pyridostigmine in the rat. Toxicol. Appl. Pharmacol. 165: 99-105.
58. Skultetyova I, Tokarev D, Jezova D. 1998. Stress-induced increase in blood-brain barrier permeability in control and monosodium glutamate-treated rats. Brain Res. Bull. 45: 175-178.
59. Swerdlow NR, Geyer MA. 1998. Using an animal model of deficient sensorimotor gating to study the pathophysiology and new treatments of schizophrenia. Schiz. Bull. 24: 285-301.
60. Taylor P. 1990. Anticholinesterase agents. In Goodman and Gilman's the Pharmacological Basis of Therapeutics. Gilman AG, Rall TW, Nies AS, Taylor P (eds). Pergamon Press: New York; 131-149.
61. van Gaalen MM, Steckler T. 2000. Behavioural analysis of four mouse strains in an anxiety test. Behav. Brain Res. 115: 95-106.
62. van Haaren F, De Jongh R, Hoy JB, Karlix JL, Schmidt CJ, Tebbett IR. 1999. The effects of acute and repeated pyridostigmine bromide administration on response acquisition with immediate and delayed reinforcement. Pharmacol. Biochem. Behav. 62: 389-394.
63. Van Haaren F, Haworth SC, Bennett SM, Cody BA. 2001. The effects of pyridostigmine bromide on progressive ratio performance in male and female rats. Pharmacol. Biochem. Behav. 68: 81-85.
64. Wahlsten D. 2001. Standardizing tests of mouse behavior: Reasons, recommendations, and reality. Physiol. Behav. 73: 695-704.
65. Wenger B, Quigley MD, Kolka MA. 1993. Seven-day pyridostigmine administration and thermoregulation during rest and exercise in dry heat. Aviat. Space Environ. Med. 64: 905-911.
66. Willott JF, Carlson S, Chen H. 1994. Prepulse inhibition of the acoustic startle response in mice: relationship to hearing loss and auditory system plasticity. Behav. Neurosci. 108: 703-713.
67. Wolthuis OL, Groen B, Busker RW, van Helden HP. 1995. Effect of low doses of cholinesterase inhibitors on behavioral performance of robot-tested marmosets. Pharmacol. Biochem. Behav. 51: 443-456.
68. Wolthuis OL, van Wersch R. 1984. Behavioral changes in the rat after low doses of cholinesterase inhibitors. Fundam. Appl. Toxicol. 4: 195-208.