Humans with latent toxoplasmosis display altered reward modulation of cognitive control

. 2017 Aug 31 ; 7 (1) : 10170. [epub] 20170831

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid28860577
Odkazy

PubMed 28860577
PubMed Central PMC5579228
DOI 10.1038/s41598-017-10926-6
PII: 10.1038/s41598-017-10926-6
Knihovny.cz E-zdroje

Latent infection with Toxoplasma gondii has repeatedly been shown to be associated with behavioral changes that are commonly attributed to a presumed increase in dopaminergic signaling. Yet, virtually nothing is known about its effects on dopamine-driven reward processing. We therefore assessed behavior and event-related potentials in individuals with vs. without latent toxoplasmosis performing a rewarded control task. The data show that otherwise healthy young adults with latent toxoplasmosis show a greatly diminished response to monetary rewards as compared to their non-infected counterparts. While this selective effect eliminated a toxoplasmosis-induced speed advantage previously observed for non-rewarded behavior, Toxo-positive subjects could still be demonstrated to be superior to Toxo-negative subjects with respect to response accuracy. Event-related potential (ERP) and source localization analyses revealed that this advantage during rewarded behavior was based on increased allocation of processing resources reflected by larger visual late positive component (LPC) amplitudes and associated activity changes in the right temporo-parietal junction (BA40) and left auditory cortex (BA41). Taken together, individuals with latent toxoplasmosis show superior behavioral performance in challenging cognitive control situations but may at the same time have a reduced sensitivity towards motivational effects of rewards, which might be explained by the presumed increase in dopamine.

Zobrazit více v PubMed

Boothroyd JC, Grigg ME. Population biology of Toxoplasma gondii and its relevance to human infection: do different strains cause different disease? Curr. Opin. Microbiol. 2002;5:438–442. doi: 10.1016/S1369-5274(02)00349-1. PubMed DOI

Flegr J. How and why Toxoplasma makes us crazy. Trends Parasitol. 2013;29:156–163. doi: 10.1016/j.pt.2013.01.007. PubMed DOI

Foroutan-Rad M, et al. Toxoplasmosis in Blood Donors: A Systematic Review and Meta-Analysis. Transfus. Med. Rev. 2016;30:116–122. doi: 10.1016/j.tmrv.2016.03.002. PubMed DOI

Webster JP. The effect of Toxoplasma gondii on animal behavior: playing cat and mouse. Schizophr. Bull. 2007;33:752–756. doi: 10.1093/schbul/sbl073. PubMed DOI PMC

Kamerkar, S. & Davis, P. H. Toxoplasma on the brain: understanding host-pathogen interactions in chronic CNS infection. J. Parasitol. Res. 2012, 589295 (2012). PubMed PMC

Parlog A, Schlüter D, Dunay IR. Toxoplasma gondii-induced neuronal alterations. Parasite Immunol. 2015;37:159–170. doi: 10.1111/pim.12157. PubMed DOI

Beste C, Getzmann S, Gajewski PD, Golka K, Falkenstein M. Latent Toxoplasma gondii infection leads to deficits in goal-directed behavior in healthy elderly. Neurobiol. Aging. 2014;35:1037–1044. doi: 10.1016/j.neurobiolaging.2013.11.012. PubMed DOI

McConkey GA, Martin HL, Bristow GC, Webster JP. Toxoplasma gondii infection and behaviour - location, location, location? J. Exp. Biol. 2013;216:113–119. doi: 10.1242/jeb.074153. PubMed DOI PMC

Stock AKH, von Heinegg E, Köhling HL, Beste C. Latent Toxoplasma gondii infection leads to improved action control. Brain. Behav. Immun. 2014;37:103–108. doi: 10.1016/j.bbi.2013.11.004. PubMed DOI

Webster JP, Kaushik M, Bristow GC, McConkey GA. Toxoplasma gondii infection, from predation to schizophrenia: can animal behaviour help us understand human behaviour? J. Exp. Biol. 2013;216:99–112. doi: 10.1242/jeb.074716. PubMed DOI PMC

Tenter AM, Heckeroth AR, Weiss LM. Toxoplasma gondii: from animals to humans. Int. J. Parasitol. 2000;30:1217–1258. doi: 10.1016/S0020-7519(00)00124-7. PubMed DOI PMC

Moore J. Altered Behavioural Responses in Intermediate Hosts–An Acanthoceptalan Parasite Strategy. Am. Nat. 1984;123:572–577. doi: 10.1086/284224. DOI

Webster JP. Rats, cats, people and parasites: the impact of latent toxoplasmosis on behaviour. Microbes Infect. Inst. Pasteur. 2001;3:1037–1045. doi: 10.1016/S1286-4579(01)01459-9. PubMed DOI

Berdoy M, Webster JP, Macdonald DW. Fatal attraction in rats infected with Toxoplasma gondii. Proc. Biol. Sci. 2000;267:1591–1594. doi: 10.1098/rspb.2000.1182. PubMed DOI PMC

Vyas A, Kim S-K, Giacomini N, Boothroyd JC, Sapolsky RM. Behavioral changes induced by Toxoplasma infection of rodents are highly specific to aversion of cat odors. Proc. Natl. Acad. Sci. USA. 2007;104:6442–6447. doi: 10.1073/pnas.0608310104. PubMed DOI PMC

Martin HL, et al. Effect of parasitic infection on dopamine biosynthesis in dopaminergic cells. Neuroscience. 2015;306:50–62. doi: 10.1016/j.neuroscience.2015.08.005. PubMed DOI PMC

Prandovszky E, et al. The neurotropic parasite Toxoplasma gondii increases dopamine metabolism. PloS One. 2011;6 doi: 10.1371/journal.pone.0023866. PubMed DOI PMC

Flegr J. Schizophrenia and Toxoplasma gondii: an undervalued association? Expert Rev. Anti Infect. Ther. 2015;13:817–820. doi: 10.1586/14787210.2015.1051033. PubMed DOI

Horacek J, et al. Latent toxoplasmosis reduces gray matter density in schizophrenia but not in controls: voxel-based-morphometry (VBM) study. World J. Biol. Psychiatry. 2012;13:501–509. doi: 10.3109/15622975.2011.573809. PubMed DOI

Xiao J, et al. Behavioral Abnormalities in a Mouse Model of Chronic Toxoplasmosis Are Associated with MAG1 Antibody Levels and Cyst Burden. PLoS Negl. Trop. Dis. 2016;10 doi: 10.1371/journal.pntd.0004674. PubMed DOI PMC

Schaeffer M, et al. Dynamic imaging of T cell-parasite interactions in the brains of mice chronically infected with Toxoplasma gondii. J. Immunol. Baltim. Md 1950. 2009;182:6379–6393. PubMed

Schlüter D, Deckert M, Hof H, Frei K. Toxoplasma gondii infection of neurons induces neuronal cytokine and chemokine production, but gamma interferon- and tumor necrosis factor-stimulated neurons fail to inhibit the invasion and growth of T. gondii. Infect. Immun. 2001;69:7889–7893. doi: 10.1128/IAI.69.12.7889-7893.2001. PubMed DOI PMC

Henriquez SA, Brett R, Alexander J, Pratt J, Roberts CW. Neuropsychiatric disease and Toxoplasma gondii infection. Neuroimmunomodulation. 2009;16:122–133. doi: 10.1159/000180267. PubMed DOI

Robert-Gangneux F, Dardé M-L. Epidemiology of and diagnostic strategies for toxoplasmosis. Clin. Microbiol. Rev. 2012;25:264–296. doi: 10.1128/CMR.05013-11. PubMed DOI PMC

Iversen, L. L. Dopamine Handbook. (Oxford University Press, (2010).

Gajewski PD, Falkenstein M, Hengstler JG, Golka K. Toxoplasma gondii impairs memory in infected seniors. Brain. Behav. Immun. 2014;36:193–199. doi: 10.1016/j.bbi.2013.11.019. PubMed DOI

Yildiz A, Chmielewski W, Beste C. Dual-task performance is differentially modulated by rewards and punishments. Behav. Brain Res. 2013;250:304–307. doi: 10.1016/j.bbr.2013.05.010. PubMed DOI

Petruo VA, Stock A-K, Münchau A, Beste C. A systems neurophysiology approach to voluntary event coding. NeuroImage. 2016;135:324–332. doi: 10.1016/j.neuroimage.2016.05.007. PubMed DOI

Zhang, R., Stock, A.-K. & Beste, C. The neurophysiological basis of reward effects on backward inhibition processes. NeuroImage, doi:10.1016/j.neuroimage.2016.05.080 (2016). PubMed

Tan D, Vyas A. Toxoplasma gondii infection and testosterone congruently increase tolerance of male rats for risk of reward forfeiture. Horm. Behav. 2016;79:37–44. doi: 10.1016/j.yhbeh.2016.01.003. PubMed DOI

Golcu D, Gebre RZ, Sapolsky RM. Toxoplasma gondii influences aversive behaviors of female rats in an estrus cycle dependent manner. Physiol. Behav. 2014;135:98–103. doi: 10.1016/j.physbeh.2014.05.036. PubMed DOI PMC

Tan D, et al. Infection of male rats with Toxoplasma gondii results in enhanced delay aversion and neural changes in the nucleus accumbens core. Proc. Biol. Sci. 2015;282 doi: 10.1098/rspb.2015.0042. PubMed DOI PMC

Cook TB, et al. ‘Latent’ infection with Toxoplasma gondii: association with trait aggression and impulsivity in healthy adults. J. Psychiatr. Res. 2015;60:87–94. doi: 10.1016/j.jpsychires.2014.09.019. PubMed DOI

Sutterland AL, et al. Beyond the association. Toxoplasma gondii in schizophrenia, bipolar disorder, and addiction: systematic review and meta-analysis. Acta Psychiatr. Scand. 2015;132:161–179. doi: 10.1111/acps.12423. PubMed DOI

Schultz W. Dopamine reward prediction error coding. Dialogues Clin. Neurosci. 2016;18:23–32. PubMed PMC

Gohil K, Dippel G, Beste C. Questioning the role of the frontopolar cortex in multi-component behavior–a TMS/EEG study. Sci. Rep. 2016;6 doi: 10.1038/srep22317. PubMed DOI PMC

Gohil K, Hahne A, Beste C. Improvements of sensorimotor processes during action cascading associated with changes in sensory processing architecture-insights from sensory deprivation. Sci. Rep. 2016;6 doi: 10.1038/srep28259. PubMed DOI PMC

Mückschel M, Stock A-K, Beste C. Psychophysiological mechanisms of interindividual differences in goal activation modes during action cascading. Cereb. Cortex N. Y. N 1991. 2014;24:2120–2129. PubMed

Verleger R, Jaśkowski P, Wascher E. Evidence for an integrative role of P3b in linking reaction to perception. J. Psychophysiol. 2005;19:165–181. doi: 10.1027/0269-8803.19.3.165. DOI

Stock A-K, Arning L, Epplen JT, Beste C. DRD1 and DRD2 Genotypes Modulate Processing Modes of Goal Activation Processes during Action Cascading. J. Neurosci. 2014;34:5335–5341. doi: 10.1523/JNEUROSCI.5140-13.2014. PubMed DOI PMC

Luck SJ, Woodman GF, Vogel EK. Event-related potential studies of attention. Trends Cogn. Sci. 2000;4:432–440. doi: 10.1016/S1364-6613(00)01545-X. PubMed DOI

Beste C, Baune BT, Falkenstein M, Konrad C. Variations in the TNF-α gene (TNF-α −308G → A) affect attention and action selection mechanisms in a dissociated fashion. J. Neurophysiol. 2010;104:2523–2531. doi: 10.1152/jn.00561.2010. PubMed DOI

Gajewski PD, Hengstler JG, Golka K, Falkenstein M, Beste C. The functional tumor necrosis factor-α (308A/G) polymorphism modulates attentional selection in elderly individuals. Neurobiol. Aging. 2013;34:2694.e1–2694.e12. doi: 10.1016/j.neurobiolaging.2013.04.017. PubMed DOI

Yildiz A, et al. Feeling safe in the plane: neural mechanisms underlying superior action control in airplane pilot trainees–a combined EEG/MRS study. Hum. Brain Mapp. 2014;35:5040–5051. doi: 10.1002/hbm.22530. PubMed DOI PMC

Cuthbert BN, Schupp HT, Bradley MM, Birbaumer N, Lang PJ. Brain potentials in affective picture processing: covariation with autonomic arousal and affective report. Biol. Psychol. 2000;52:95–111. doi: 10.1016/S0301-0511(99)00044-7. PubMed DOI

Schupp HT, et al. Affective picture processing: the late positive potential is modulated by motivational relevance. Psychophysiology. 2000;37:257–261. doi: 10.1111/1469-8986.3720257. PubMed DOI

Furley, P., Schnuerch, R. & Gibbons, H. The winner takes it all: Event-related brain potentials reveal enhanced motivated attention toward athletes’ nonverbal signals of leading. Soc. Neurosci., doi:10.1080/17470919.2016.1182586 1–10 (2016). PubMed

Verbruggen F, Schneider DW, Logan GD. How to stop and change a response: the role of goal activation in multitasking. J. Exp. Psychol. Hum. Percept. Perform. 2008;34:1212–1228. doi: 10.1037/0096-1523.34.5.1212. PubMed DOI

Faul F, Erdfelder E, Lang A-G, Buchner A. G*Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav. Res. Methods. 2007;39:175–191. doi: 10.3758/BF03193146. PubMed DOI

Henrickson KJ. Parainfluenza viruses. Clin. Microbiol. Rev. 2003;16:242–264. doi: 10.1128/CMR.16.2.242-264.2003. PubMed DOI PMC

Getzmann, S. & Wascher, E. Visually guided auditory attention in a dynamic ‘cocktail-party’ speech perception task: ERP evidence for age-related differences. Hear. Res. doi:10.1016/j.heares.2016.11.001 (2016). PubMed

Davidson GD, Pitts MA. Auditory event-related potentials associated with perceptual reversals of bistable pitch motion. Front. Hum. Neurosci. 2014;8 doi: 10.3389/fnhum.2014.00572. PubMed DOI PMC

Kaganovich N, Schumaker J, Rowland C. Atypical audiovisual word processing in school-age children with a history of specific language impairment: an event-related potential study. J. Neurodev. Disord. 2016;8 doi: 10.1186/s11689-016-9168-3. PubMed DOI PMC

Donaldson PH, Rinehart NJ, Enticott PG. Noninvasive stimulation of the temporoparietal junction: A systematic review. Neurosci. Biobehav. Rev. 2015;55:547–572. doi: 10.1016/j.neubiorev.2015.05.017. PubMed DOI

Platz T, Schüttauf J, Aschenbach J, Mengdehl C, Lotze M. Effects of inhibitory theta burst TMS to different brain sites involved in visuospatial attention - a combined neuronavigated cTBS and behavioural study. Restor. Neurol. Neurosci. 2016;34:271–285. PubMed

Webb TW, Igelström KM, Schurger A, Graziano MSA. Cortical networks involved in visual awareness independent of visual attention. Proc. Natl. Acad. Sci. USA. 2016;113:13923–13928. doi: 10.1073/pnas.1611505113. PubMed DOI PMC

Collette F, et al. Involvement of both prefrontal and inferior parietal cortex in dual-task performance. Brain Res. Cogn. Brain Res. 2005;24:237–251. doi: 10.1016/j.cogbrainres.2005.01.023. PubMed DOI

Geng JJ, Vossel S. Re-evaluating the role of TPJ in attentional control: contextual updating? Neurosci. Biobehav. Rev. 2013;37:2608–2620. doi: 10.1016/j.neubiorev.2013.08.010. PubMed DOI PMC

Pitts MA, Britz J. Insights from intermittent binocular rivalry and EEG. Front. Hum. Neurosci. 2011;5 doi: 10.3389/fnhum.2011.00107. PubMed DOI PMC

Plack CJ, Barker D, Hall DA. Pitch coding and pitch processing in the human brain. Hear. Res. 2014;307:53–64. doi: 10.1016/j.heares.2013.07.020. PubMed DOI

Wang X, Walker KMM. Neural mechanisms for the abstraction and use of pitch information in auditory cortex. J. Neurosci. Off. J. Soc. Neurosci. 2012;32:13339–13342. doi: 10.1523/JNEUROSCI.3814-12.2012. PubMed DOI PMC

Dodds CM, Morein-Zamir S, Robbins TW. Dissociating inhibition, attention, and response control in the frontoparietal network using functional magnetic resonance imaging. Cereb. Cortex N. Y. N 1991. 2011;21:1155–1165. PubMed PMC

Hampshire A, Chamberlain SR, Monti MM, Duncan J, Owen AM. The role of the right inferior frontal gyrus: inhibition and attentional control. NeuroImage. 2010;50:1313–1319. doi: 10.1016/j.neuroimage.2009.12.109. PubMed DOI PMC

Verbruggen F, Stevens T, Chambers CD. Proactive and reactive stopping when distracted: an attentional account. J. Exp. Psychol. Hum. Percept. Perform. 2014;40:1295–1300. doi: 10.1037/a0036542. PubMed DOI PMC

Mückschel M, Stock A-K, Beste C. Different strategies, but indifferent strategy adaptation during action cascading. Sci. Rep. 2015;5 doi: 10.1038/srep09992. PubMed DOI PMC

Pitts MA, Gavin WJ, Nerger JL. Early top-down influences on bistable perception revealed by event-related potentials. Brain Cogn. 2008;67:11–24. doi: 10.1016/j.bandc.2007.10.004. PubMed DOI

Schacht A, Sommer W. Emotions in word and face processing: early and late cortical responses. Brain Cogn. 2009;69:538–550. doi: 10.1016/j.bandc.2008.11.005. PubMed DOI

Bayer, M. & Schacht, A. Event-related brain responses to emotional words, pictures, and faces – a cross-domain comparison. Front. Psychol. 5, (2014). PubMed PMC

Hinojosa JA, Carretié L, Valcárcel MA, Méndez-Bértolo C, Pozo MA. Electrophysiological differences in the processing of affective information in words and pictures. Cogn. Affect. Behav. Neurosci. 2009;9:173–189. doi: 10.3758/CABN.9.2.173. PubMed DOI

Valdés-Conroy B, Aguado L, Fernández-Cahill M, Romero-Ferreiro V, Diéguez-Risco T. Following the time course of face gender and expression processing: a task-dependent ERP study. Int. J. Psychophysiol. Off. J. Int. Organ. Psychophysiol. 2014;92:59–66. PubMed

Pascual-Marqui RD. Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. Methods Find. Exp. Clin. Pharmacol. 2002;24(Suppl D):5–12. PubMed

Marco-Pallarés J, Grau C, Ruffini G. Combined ICA-LORETA analysis of mismatch negativity. NeuroImage. 2005;25:471–477. doi: 10.1016/j.neuroimage.2004.11.028. PubMed DOI

Sekihara K, Sahani M, Nagarajan SS. Localization bias and spatial resolution of adaptive and non-adaptive spatial filters for MEG source reconstruction. NeuroImage. 2005;25:1056–1067. doi: 10.1016/j.neuroimage.2004.11.051. PubMed DOI PMC

Mazziotta J, et al. A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM) Philos. Trans. R. Soc. Lond. Ser. B. 2001;356:1293–1322. doi: 10.1098/rstb.2001.0915. PubMed DOI PMC

Dippel G, Beste C. A causal role of the right inferior frontal cortex in implementing strategies for multi-component behaviour. Nat. Commun. 2015;6 doi: 10.1038/ncomms7587. PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace