Contrasting effect of prepulse signals on performance of Toxoplasma-infected and Toxoplasma-free subjects in an acoustic reaction times test
Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
25384036
PubMed Central
PMC4226587
DOI
10.1371/journal.pone.0112771
PII: PONE-D-13-51139
Knihovny.cz E-zdroje
- MeSH
- dospělí MeSH
- lidé MeSH
- mladý dospělý MeSH
- reakční čas MeSH
- schizofrenie (psychologie) MeSH
- schizofrenie imunologie parazitologie patofyziologie MeSH
- sexuální faktory MeSH
- Toxoplasma fyziologie MeSH
- toxoplazmóza imunologie parazitologie patofyziologie psychologie MeSH
- úleková reakce fyziologie MeSH
- Check Tag
- dospělí MeSH
- lidé MeSH
- mladý dospělý MeSH
- mužské pohlaví MeSH
- ženské pohlaví MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
BACKGROUND: About 30% of people on Earth have latent toxoplasmosis. Infected subjects do not express any clinical symptoms, however, they carry dormant stages of parasite Toxoplasma for the rest of their life. This form of toxoplasmosis is mostly considered harmless, however, recent studies showed its specific effects on physiology, behaviour and its associations with various diseases, including psychiatric disorders such as schizophrenia. Individuals who suffer from schizophrenia have about 2.7 times higher prevalence of Toxoplasma-seropositivity than controls, which suggests that some traits characteristic of schizophrenic patients, including the sex difference in schizophrenia onset, decrease of grey matter density in specific brain areas and modification of prepulse inhibition of startle reaction could in fact be caused by toxoplasmosis for those patients who are Toxoplasma-seropositive. METHODOLOGY/PRINCIPAL FINDINGS: We measured the effect of prepulse inhibition/facilitation of the startle reaction on reaction times. The students, 170 women and 66 men, were asked to react as quickly as possible to a startling acoustic signal by pressing a computer mouse button. Some of the startling signals were without the prepulse, some were 20 msec. preceded by a short (20 msec.) prepulse signal of lower intensity. Toxoplasma-seropositive subjects had longer reaction times than the controls. Acoustic prepulse shorted the reaction times in all subjects. This effect of prepulse on reaction times was stronger in male subjects and increased with the duration of infection, suggesting that it represented a cumulative effect of latent toxoplasmosis, rather than a fading out after effect of past acute toxoplasmosis. CONCLUSIONS: Different sensitivity of Toxoplasma-seropositive and Toxoplasma-seronegative subjects on effect of prepulses on reaction times (the toxoplasmosis-prepulse interaction) suggested, but of course did not prove, that the alternations of prepulse inhibition of startle reaction observed in schizophrenia patients probably joined the list of schizophrenia symptoms that are in fact caused by latent toxoplasmosis.
Zobrazit více v PubMed
Tenter AM, Heckeroth AR, Weiss LM (2000) Toxoplasma gondii: from animals to humans. Int J Parasitol 30: 1217–1258. PubMed PMC
Flegr J (2013) Influence of latent Toxoplasma infection on human personality, physiology and morphology: pros and cons of the Toxoplasma-human model in studying the manipulation hypothesis. Journal of Experimental Biology 216: 127–133. PubMed
McConkey GA, Martin HL, Bristow GC, Webster JP (2013) Toxoplasma gondii infection and behaviour - location, location, location? Journal of Experimental Biology 216: 113–119. PubMed PMC
Webster JP (2007) The effect of Toxoplasma gondii on animal behavior: Playing cat and mouse. Schizophr Bull 33: 752–756. PubMed PMC
Lindová J, Kuběna AA, Šturcová A, Křivohlavá R, Novotná M, et al. (2010) Pattern of money allocation in experimental games supports the stress hypothesis of gender differences in Toxoplasma gondii-induced behavioural changes. Folia Parasitol 57: 136–142. PubMed
Flegr J, Hrdý I (1994) Influence of chronic toxoplasmosis on some human personality factors. Folia Parasitol 41: 122–126. PubMed
Flegr J (2010) Influence of latent toxoplasmosis on the phenotype of intermediate hosts. Folia Parasitol 57: 81–87. PubMed
Havlíček J, Gašová Z, Smith AP, Zvára K, Flegr J (2001) Decrease of psychomotor performance in subjects with latent ‘asymptomatic’ toxoplasmosis. Parasitology 122: 515–520. PubMed
Flegr J, Preiss M, Klose J (2013) Toxoplasmosis-associated difference in intelligence and personality in men depends on their Rhesus blood group but not ABO blood group. PLoS ONE 8. PubMed PMC
Torrey EF, Yolken RH (2007) Editors’ introduction: Schizophrenia and toxoplasmosis. Schizophr Bull 33: 727–728. PubMed PMC
Yolken RH, Dickerson FB, Torrey EF (2009) Toxoplasma and schizophrenia. Parasite Immunol 31: 706–715. PubMed
Flegr J (2013) How and why Toxoplasma makes us crazy. Trends Parasitol 29: 156–163. PubMed
Webster JP, Kaushik M, Bristow GC, McConkey GA (2013) Toxoplasma gondii infection, from predation to schizophrenia: can animal behaviour help us understand human behaviour? Journal of Experimental Biology 216: 99–112. PubMed PMC
Torrey EF, Bartko JJ, Lun ZR, Yolken RH (2007) Antibodies to Toxoplasma gondii in patients with schizophrenia: A meta-analysis. Schizophr Bull 33: 729–736. PubMed PMC
Torrey EF, Bartko JJ, Yolken RH (2012) Toxoplasma gondii and other risk factors for schizophrenia: An update. Schizophr Bull 38: 642–647. PubMed PMC
Zhou P, Chen ZG, Li HL, Zheng HH, He SY, et al. (2011) Toxoplasma gondii infection in humans in China. Parasit Vect 4: 165. PubMed PMC
Holub D, Flegr J, Dragomirecka E, Rodriguez M, Preiss M, et al. (2013) Differences in onset of disease and severity of psychopathology between toxoplasmosis-related and toxoplasmosis-unrelated schizophrenia. Acta Psychiatr Scand 127: 227–238. PubMed
Horacek J, Flegr J, Tintera J, Verebova K, Spaniel F, et al... (2012) Latent toxoplasmosis reduces gray matter density in schizophrenia but not in controls: Voxel-based-morphometry (VBM) study. World J Biol Psychiatry. PubMed
Wang HL, Wang GH, Li QY, Shu C, Jiang MS, et al. (2006) Prevalence of Toxoplasma infection in first-episode schizophrenia and comparison between Toxoplasma-seropositive and Toxoplasma-seronegative schizophrenia. Acta Psychiatr Scand 114: 40–48. PubMed
Horacek J, Flegr J, Tintera J, Verebova K, Spaniel F, et al. (2012) Latent toxoplasmosis reduces gray matter density in schizophrenia but not in controls: voxel-based-morphometry (VBM) study. The world journal of biological psychiatry: the official journal of the World Federation of Societies of Biological Psychiatry 13: 501–509. PubMed
Turetsky BI, Moberg PJ (2009) An odor-specific threshold deficit implicates abnormal intracellular cyclic AMP signaling in schizophrenia. Am J Psychiatry 166: 226–233. PubMed PMC
Rupp CI (2010) Olfactory function and schizophrenia: an update. Current Opinion in Psychiatry 23: 97–102. PubMed
Flegr J, Lenochová P, Hodný Z, Vondrová M (2011) Fatal attraction phenomenon in humans: cat odour attractiveness increased for Toxoplasma-infected men while decreased for infected women. PLoS Neglect Trop D 5: e1389. PubMed PMC
Berdoy M, Webster JP, Macdonald DW (2000) Fatal attraction in rats infected with Toxoplasma gondii . Proc R Soc Biol Sci Ser B 267: 1591–1594. PubMed PMC
Vyas A, Kim SK, Giacomini N, Boothroyd JC, Sapolsky RM (2007) Behavioral changes induced by Toxoplasma infection of rodents are highly specific to aversion of cat odors. Proc Natl Acad Sci USA 104: 6442–6447. PubMed PMC
House PK, Vyas A, Sapolsky R (2011) Predator cat odors activate sexual arousal pathways in brains of Toxoplasma gondii infected rats. PLoS ONE 6. PubMed PMC
Vyas A (2013) Parasite-augmented mate choice and reduction in innate fear in rats infected by Toxoplasma gondii . Journal of Experimental Biology 216: 120–126. PubMed
Braff DL, Geyer MA, Swerdlow NR (2001) Human studies of prepulse inhibition of startle: normal subjects, patient groups, and pharmacological studies. Psychopharmacology (Berl) 156: 234–258. PubMed
Grillon C, Ameli R, Charney DS, Krystal J, Braff D (1992) Startle gating deficits occur across prepulse intensities in schizophrenic patients. Biol Psychiatry 32: 939–943. PubMed
Braff DL, Swerdlow NR, Geyer MA (1999) Symptom correlates of prepulse inhibition deficits in male schizophrenic patients. Am J Psychiatry 156: 596–602. PubMed
Kumari V, Soni W, Mathew VM, Sharma T (2000) Prepulse inhibition of the startle response in men with schizophrenia: effects of age of onset of illness, symptoms, and medication. Arch Gen Psychiatry 57: 609–614. PubMed
Cadenhead KS, Swerdlow NR, Shafer KM, Diaz M, Braff DL (2000) Modulation of the startle response and startle laterality in relatives of schizophrenic patients and in subjects with schizotypal personality disorder: Evidence of inhibitory deficits. Am J Psychiatry 157: 1660–1668. PubMed
Swerdlow NR, Light GA, Cadenhead KS, Sprock J, Hsieh MH, et al. (2006) Startle gating deficits in a large cohort of patients with schizophrenia: relationship to medications, symptoms, neurocognition, and level of function. Arch Gen Psychiatry 63: 1325–1335. PubMed
Pearce BD, Hubbard S, Rivera HN, Wilkins PP, Fisch MC, et al. (2013) Toxoplasma gondii exposure affects neural processing speed as measured by acoustic startle latency in schizophrenia and controls. Schizophr Res 150: 258–261. PubMed PMC
Willner P (1997) The dopamine hypothesis of schizophrenia: current status, future prospects. Int Clin Psychopharmacol 12: 297–308. PubMed
Nikam SS, Awasthi AK (2008) Evolution of schizophrenia drugs: A focus on dopaminergic systems. Curr Opin Invest Drugs 9: 37–46. PubMed
Gaskell EA, Smith JE, Pinney JW, Westhead DR, McConkey GA (2009) A unique dual activity amino acid hydroxylase in Toxoplasma gondii PLoS ONE. 4: e4801. PubMed PMC
Prandovszky E, Gaskell E, Martin H, Dubey JP, Webster JP, et al. (2011) The neurotropic parasite Toxoplasma gondii increases dopamine metabolism. PLoS ONE 6: e23866. PubMed PMC
Gatkowska J, Wieczorek M, Dziadek B, Dzitko K, Dlugonska H (2013) Sex-dependent neurotransmitter level changes in brains of Toxoplasma gondii infected mice. Exp Parasitol 133: 1–7. PubMed
Skallová A, Kodym P, Frynta D, Flegr J (2006) The role of dopamine in Toxoplasma-induced behavioural alterations in mice: an ethological and ethopharmacological study. Parasitology 133: 525–535. PubMed
Hodková H, Kodym P, Flegr J (2007) Poorer results of mice with latent toxoplasmosis in learning tests: impaired learning processes or the novelty discrimination mechanism? Parasitology 134: 1329–1337. PubMed
Strobl JS, Goodwin DG, Rzigalinski BA, Lindsay DS (2012) Dopamine stimulates propagation of Toxoplasma gondii tachyzoites in human fibroblast and primary neonatal rat astrocyte cell cultures. J Parasitol 98: 1296–1299. PubMed
Flegr J, Preiss M, Klose J, Havlíček J, Vitáková M, et al. (2003) Decreased level of psychobiological factor novelty seeking and lower intelligence in men latently infected with the protozoan parasite Toxoplasma gondii Dopamine, a missing link between schizophrenia and toxoplasmosis? Biol Psychol 63: 253–268. PubMed
Skallová A, Novotná M, Kolbeková P, Gašová Z, Veselý V, et al. (2005) Decreased level of novelty seeking in blood donors infected with Toxoplasma . Neuroendocrinol Lett 26: 480–486. PubMed
Xiao JC, Viscidi RP, Kannan G, Pletnikov MV, Li Y, et al. (2013) The Toxoplasma MAGI peptides induce sex-based humoral immune response in mice and distinguish active from chronic human infection. Microb Infect 15: 74–83. PubMed PMC
Saklayen SS, Mabrouk OS, Pehek EA (2004) Negative feedback regulation of nigrostriatal dopamine release: Mediation by striatal D1 receptors. J Pharmacol Exp Ther 311: 342–348. PubMed
Valls-Sole J, Sole A, Valldeoriola F, Munoz E, Gonzalez LE, et al. (1995) Reaction time and acoustic startle in normal human subjects. Neurosci Lett 195: 97–100. PubMed
Valls-Solé J, Kumru H, Kofler M (2008) Interaction between startle and voluntary reactions in humans. Exp Brain Res 187: 497–507. PubMed
Maslovat D, Kennedy PM, Forgaard CJ, Chua R, Franks IM (2012) The effects of prepulse inhibition timing on the startle reflex and reaction time. Neurosci Lett 513: 243–247. PubMed
Kodym P, Machala L, Roháčová H, Širocká B, Malý M (2007) Evaluation of a commercial IgE ELISA in comparison with IgA and IgM ELISAs, IgG avidity assay and complement fixation for the diagnosis of acute toxoplasmosis. Clin Microbiol Infec 13: 40–47. PubMed
Flegr J, Novotná M, Lindová J, Havlíček J (2008) Neurophysiological effect of the Rh factor. Protective role of the RhD molecule against Toxoplasma-induced impairment of reaction times in women. Neuroendocrinol Lett 29: 475–481. PubMed
Siegel S, Castellan NJ (1988) Nonparametric statistics for the behavioral sciences. New York: McGraw-Hill. xxiii, 399 p.
Kaňková Š, Kodym P, Flegr J (2011) Direct evidence of Toxoplasma-induced changes in serum testosterone in mice. Exp Parasitol 128: 181–183. PubMed
Holub D, Motlova L, Rodriguez M, Dragomirecka E, Preiss M, et al. (2006) Postnatal latent toxoplasmosis in schizophrenia: cognitive and psychopathological correlates. Psychiatrie 10: 66–70.
Foss JA, Ison JR, Torre JP Jr, Wansack S (1989) The acoustic startle response and disruption of aiming: II. Modulation by forewarning and preliminary stimuli. Hum Factors 31: 319–333. PubMed
Filion DL, Dawson ME, Schell AM (1998) The psychological significance of human startle. eyeblink modification: a review Biological Psychology 47: 1–43. PubMed
Valls-Sole J, Valldeoriola F, Molinuevo JL, Cossu G, Nobbe F (1999) Prepulse modulation of the startle reaction and the blink reflex in normal human subjects. Exp Brain Res 129: 49–56. PubMed
Flegr J, Havlíček J (1999) Changes in the personality profile of young women with latent toxoplasmosis. Folia Parasitol 46: 22–28. PubMed
Sun XJ, Lu HJ, Jia BY, Chang ZG, Peng S, et al.. (2013) A comparative study of Toxoplasma gondii seroprevalence in three healthy Chinese populations detected using native and recombinant antigens. Parasit Vect 6. PubMed PMC
Flegr J, Hrdá Š, Kodym P (2005) Influence of latent ‘asymptomatic’ toxoplasmosis on body weight of pregnant women. Folia Parasitol 52: 199–204. PubMed
Novotná M, Havlíček J, Smith AP, Kolbeková P, Skallová A, et al. (2008) Toxoplasma and reaction time: Role of toxoplasmosis in the origin, preservation and geographical distribution of Rh blood group polymorphism. Parasitology 135: 1253–1261. PubMed
Flegr J, Novotná M, Fialová A, Kolbeková P, Gašová Z (2010) The influence of RhD phenotype on toxoplasmosis- and age-associated changes in personality profile of blood donors. Folia Parasitol 57: 143–150. PubMed
Flegr J, Lindová J, Kodym P (2008) Sex-dependent toxoplasmosis-associated differences in testosterone concentration in humans. Parasitology 135: 427–431. PubMed
Thirty years of studying latent toxoplasmosis: behavioural, physiological, and health insights
Latent toxoplasmosis and olfactory functions of Rh positive and Rh negative subjects