HIV-related decreased brain activity during a semantic memory task is reflected in spontaneous brain functional connectivity

Anna R. Egbert; Agnieszka Pluta; Marta Sobańska; Natalia Gawron; Bogna Szymańska-Kotwica; Emilia Łojek; Harmonia Group

doi:10.5114/hpr.2020.94720

Autor

Anna R. Egbert University of British Columbia, University of Warsaw
Agnieszka Pluta University of Warsaw, World Hearing Center
Marta Sobańska University of Warsaw
Natalia Gawron The Maria Grzegorzewska University
Bogna Szymańska-Kotwica The Central Hospital for Infectious Diseases, Warsaw
Emilia Łojek University of Warsaw
Harmonia Group University of Warsaw, World Hearing Center, The Central Hospital for Infectious Diseases, Warsaw, The Ohio State University, The Cleveland Clinic, Institute of Psychiatry and Neurology, Warsaw

DOI:

https://doi.org/10.5114/hpr.2020.94720

Słowa kluczowe:

neurocognitive, cART, fMRI, functional brain connectivity, hand

Abstrakt

Background
The primary goal was to examine HIV-related changes in brain activation during a semantic memory task. The secondary goal was to assess whether the functional connectivity of the brain regions showing altered activity during the semantic memory task is related to HIV serostatus.

Participants and procedure
The total group of 17 male subjects, aged on average 44 years, included 8 HIV+/cART+ and 9 demographically matched healthy comparators. Participants completed Famous Names Recognition task-functional magnetic resonance imaging (fMRI) and resting state fMRI.

Results
We found an effect of HIV status on brain activation during the semantic memory task, despite comparable accuracy and reaction time across groups. Compared to healthy individuals, in HIV+ participants recognition of famous names elicited less activity in the fronto-striatal network, particularly in the left caudate nucleus (p = .049), left inferior frontal gyrus (p = .047), left thalamus (p = .031) and right thalamus (p = .047), as well as in the left middle occipital gyrus (p = .028). Although an effect of HIV status on functional connectivity of the brain regions showing altered activity during semantic memory task was not observed, resting-state activation of those regions was significantly correlated with performance on cognitive domains of attention, executive functioning, psychomotor speed and semantic skills.

Conclusions
Our findings suggest the presence of functional brain network reorganization in HIV+/cART+ patients, particularly in subcortical regions of the fronto-striatal network, in the absence of neurocognitive decline.

Downloads

Download data is not yet available.

Bibliografia

Abidin, A. Z., DSouza, A. M., Nagarajan, M. B., Wang, L., Qiu, X., Schifitto, G., & Wismüller, A. (2018). Alteration of brain network topology in HIV-associated neurocognitive disorder: a novel functional connectivity perspective. NeuroImage: Clinical, 17, 768–777. https://doi.org/10.1016/j.nicl.2017.11.025.

Antinori, A., Arendt, G., Becker, J. T., Brew, B. J., Byrd, D. A., Cherner, M., Clifford, D. B., Cinque, P., Epstein, L. G., Goodkin, K., Gisslen, M., Grant, I., Heaton, R. K., Joseph, J., Marder, K., Marra, C. M., McArthur, J. C., Nunn, M., Price, R. W., Pulliam, L., Robertson, K. R., Sacktor, N., Valcour, V., & Wojna, V. E. (2007). Updated research nosology for HIV-associated neurocognitive disorders. Neurology, 69, 1789–1799. https://doi.org/10.1212/01.WNL. 0000287431.88658.8b.

Arthurs, O. J., & Boniface, S. (2002). How well do we understand the neural origins of the fMRI BOLD signal? Trends in Neurosciences, 25, 27–31. https:// doi.org/10.1016/S0166-2236(00)01995-0.

Ashburner, J., Barnes, G., Chen, C., Daunizeau, J., Flandin, G., Friston, K., ... & Penny, W. (2017). SPM12 Manual. Retrieved from http://www.fil.ion. ucl.ac.uk/spm/ [accessed April 4, 2018].

Birn, R. M., Molloy, E. K., Patriat, R., Parker, T., Meier, T. B., Kirk, G. R., Nair, V. A., Meyerand, M. E., & Prabhakaran, V. (2013). The effect of scan length on the reliability of resting-state fMRI connectivity estimates. NeuroImage, 83, 550–558. https:// doi.org/10.1016/j.neuroimage.2013.05.099.

Biswal, B., Zerrin Yetkin, F., Haughton, V. M., & Hyde, J. S. (1995). Functional connectivity in the motor cortex of resting human brain using echo‐ planar MRI. Magnetic Resonance in Medicine, 34, 537–541. https://doi.org/10.1002/mrm.1910340409.

Brett, M., Anton, J. L., Valabregue, R., & Poline, J. B. (2002). Region of interest analysis using the MarsBar toolbox for SPM 99. NeuroImage, 16, 497.

Brzeziński, J., Gaul, M., Hornowska, E., Jaworowska, A., Machowski, A., & Zakrzewska, M. (2004). Skala Inteligencji D. Wechslera dla dorosłych. Wersja Zrewidowana. WAIS-R(PL) [The Wechsler Adult Intelligence Scale. Revised Version. WAIS-R(PL)]. Warszawa: Pracownia Testów Psychologicznych PTP.

Chelune, G. J., Heaton, R. K., & Lehman, R. A. W. (1986). Neuropsychological and personality correlates of patients’ complaints of disability. In G. Goldstein & R. E. Tarter (Eds.), Advances in clinical neuropsychology (Vol. 3, pp. 95–126). New York, NY: Plenum Press.

Cole, M. W., Bassett, D. S., Power, J. D., Braver, T. S., & Petersen, S. E. (2014). Intrinsic and task-evoked network architectures of the human brain. Neuron, 83, 238–251. https://doi.org/10.1016/j.neuron. 2014.05.014.

Corsi, P. (1972). Human memory and the medial temporal region of the brain. Dissertation Abstracts International, 34, 891.

D’Elia, L., & Satz, P. (2000). Color trails test. Lutz, FL: Psychological Assessment Resources. Delis, D. C., Kramer, J. H., Kaplan, E., & Ober, B. A. (2000). CVLT-II: California verbal learning test: adult version. San Antonio, TX: Psychological Corporation.

Di, X., & Biswal, B. B. (2015). Characterizations of resting-state modulatory interactions in human brain. Journal of Neurophysiology, 114, 2785–2796. https://doi.org/10.1152/jn.00893.2014.

Dosenbach, N. U., Nardos, B., Cohen, A. L., Fair, D. A., Power, J. D., Church, J. A., Nelson, S. M., Wig, G. S., Vogel, A. C., Lessov-Schlaggar, C. N., Barnes, K. A., Dubis, J. W., Feczko, E., Coalson, R. S., Pruett, J. R., Barch, D. M., Petersen, S. E., & Schlaggar, B. L. (2010). Prediction of individual brain maturity using fMRI. Science, 329, 1358–1361. https://doi. org/10.1126/science.1194144.

Douville, K., Woodard, J. L., Seidenberg, M., Miller, S. K., Leveroni, C. L., Nielson, K. A., Franczak, M., Antuono, P., & Rao, S. M. (2005). Medial temporal lobe activity for recognition of recent and remote famous names: an event-related fMRI study. Neuropsychologia, 43, 693–703. https://doi.org/10.1016/j. neuropsychologia.2004.09.005.

Du Plessis, S., Vink, M., Joska, J. A., Koutsilieri, E., Stein, D. J., & Emsley, R. (2014). HIV infection and the fronto-striatal system: a systematic review and meta-analysis of fMRI studies. AIDS, 28, 803–811. https://doi.org/10.1097/QAD.0000000000000151.

Eaton, W. W., Smith, C., Ybarra, M., Muntaner, C., & Tien, A. (2004). Center for Epidemiologic Studies Depression Scale: review and revision (CESD and CESD-R). In M. E. Maruish (Ed.), The use of psychological testing for treatment planning and outcomes assessment: Instruments for adults (pp. 363–377). Mahwah, NJ: Lawrence Erlbaum Associates Publishers.

Egbert, A. R., Biswal, B., Karunakaran, K., Gohel, S., Pluta, A., Wolak, T., Szymańska, B., Firląg-Burkacka, E., Sobańska, M., Gawron, N., Bieńkowski, P., Sienkiewicz-Jarosz, H., Ścińska-Bieńkowska, A., Bornstein, R., Rao, S., & Łojek, E. (2018). Age and HIV effects on resting state of the brain in relationship to neurocognitive functioning. Behavioural Brain Research, 344, 20–27. https://doi.org/10.1016/j. bbr.2018.02.007.

Folstein, M. F., Folstein, S. E., & McHugh, P. R. (1975). “Mini-mental state”: a practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12, 189–198. https://doi.org/10.1016/0022-3956(75)90026-6.

Fox, M. D., & Raichle, M. E. (2007). Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nature Reviews Neuroscience, 8, 700–711. https://doi.org/10.1038/nrn2201.

Geerligs, L., Rubinov, M., & Henson, R. N. (2015). State and trait components of functional connectivity: Individual differences vary with mental state. Journal of Neuroscience, 35, 13949–13961. https://doi.org/10.1523/JNEUROSCI.1324-15.2015.

Gordon, E. M., Laumann, T. O., Gilmore, A. W., Newbold, D. J., Greene, D. J., Berg, J. J., Ortega, M., HoytDrazen, C., Gratton, C., Sun, H., Hampton, J. M., Coalson, R. S., Nguyen, A. L., McDermott, K. B., Shimony, J. S., Snyder, A. Z., Schlaggar, B. L., Petersen, S. E., Nelson, S. M., & Dosenbach, N. U. F. (2017). Precision functional mapping of individual human brains. Neuron, 95, 791–807. https://doi. org/10.1016/j.neuron.2017.07.011.

Gray, L. R., Roche, M., Flynn, J. K., Wesselingh, S. L., Gorry, P. R., & Churchill, M. J. (2014). Is the central nervous system a reservoir of HIV-1? Current Opinion in HIV and AIDS, 9, 552–558. https://doi. org/10.1097/COH.0000000000000108.

Hakkers, C. S., Arends, J. E., Barth, R. E., Du Plessis, S., Hoepelman, A. I. M., & Vink, M. (2017). Review of functional MRI in HIV: Effects of aging and medication. Journal of Neurovirology, 23, 20–32. https:// doi.org/10.1007/s13365-016-0483-y.

Heaton, R. K. (1981). A manual for the Wisconsin Card Sorting Test. Lutz, FL: Psychological Assessment Resources. Heaton, R. K., Clifford, D. B., Franklin, D. R., Woods, S. P., Ake, C., Vaida, F., Ellis, R. J., Letendre, S. L., Marcotte, T. D., Atkinson, J. H., RiveraMindt, M., Vigil, O. R., Taylor, M. J., Collier, A. C., Marra, C. M., Gelman, B. B., McArthur, J. C., Morgello, S., Simpson, D. M., McCutchan, J. A., Abramson, I., Gamst, A., Fennema-Notestine, C., Jernigan, T. L., Wong, J., & Grant, I. (2010). HIV-associated neurocognitive disorders persist in the era of potent antiretroviral therapy: CHARTER Study. Neurology, 75, 2087–2096. https://doi.org/10.1212/ WNL.0b013e318200d727.

Heaton, R. K., Franklin, D. R., Ellis, R. J., McCutchan, J. A., Letendre, S. L., LeBlanc, S., Corkran, S. H., Duarte, N. A., Clifford, D. B., Woods, S. P., Collier, A. C., Marra, C. M., Morgello, S., Mindt, M. R., Taylor, M. J., Marcotte, T. D., Atkinson, J. H., Wolfson, T., Gelman, B. B., McArthur, J. C., Simpson, D. M., Abramson, I., Gamst, A., Fennema-Notestine, C., Jernigan, T. L., Wong, J., & Grant, I. (2011). HIV-associated neurocognitive disorders before and during the era of combination antiretroviral therapy: Differences in rates, nature, and predictors. Journal of Neurovirology, 17, 3–16. https://doi.org/10.1007/s13365-010-0006-1.

Heaton, R. K., Franklin Jr, D. R., Deutsch, R., Letendre, S., Ellis, R. J., Casaletto, K., Marquine, M. J., Woods, S. P., Vaida, F., Atkinson, J. H., Marcotte, T. D., McCutchan, J. A., Collier, A. C., Marra, C. M., Clifford, D. B., Gelman, B. B., Sacktor, N., Morgello, S., Simpson, D. M., Abramson, I., Gamst, A. C., Fennema-Notestine, C., Smith, D. M., & Grant, I. (2014). Neurocognitive change in the era of HIV combination antiretroviral therapy: the longitudinal CHARTER study. Clinical Infectious Diseases, 60, 473–480. https://doi.org/10.1093/cid/ ciu862.

Ipser, J. C., Brown, G. G., Bischoff-Grethe, A., Connolly, C. G., Ellis, R. J., Heaton, R. K., Grant, I., & Translational Methamphetamine AIDS Research Center (TMARC) Group (2015). HIV infection is associated with attenuated frontostriatal intrinsic connectivity: a preliminary study. Journal of the International Neuropsychological Society, 21, 203–213. https://doi.org/10.1017/S1355617715000156.

Janssen, M. A., Hinne, M., Janssen, R. J., van Gerven, M. A., Steens, S. C., Góraj, B., Koopmans, P. P., & Kessels, R. P. (2017). Resting-state subcortical functional connectivity in HIV-infected patients on long-term cART. Brain Imaging and Behavior, 11, 1555–1560. https://doi.org/10.1007/s11682-016- 9632-4.

Jaworowska, A. (2002). Wisconsin Card Sorting Test (WCST). Manual. Warszawa: Pracownia Testów Psychologicznych PTP. Koziara, K. (2016). Ocena depresyjności w populacji. Psychometryczna ocena polskiej wersji skali CESD-R [Assessment of depressiveness in population. Psychometric evaluation of the Polish version of the CESD-R]. Psychiatria Polska, 50, 1109–1117. https://doi.org/10.12740/PP/61614.

Lacadie, C. M., Fulbright, R. K., Rajeevan, N., Constable, R. T., & Papademetris, X. (2008). More accurate Talairach coordinates for neuroimaging using non-linear registration. NeuroImage, 42, 717–725. https://doi.org/10.1016/j.neuroimage.2008.04.240.

Łojek, E., & Stańczak, J. (2005). Test Płynności Figuralnej Ruffa. Podręcznik [Ruff’s Figural Fluency Test. Manual]. Warszawa: Pracownia Testów Psychologicznych PTP. Łojek, E., & Stańczak, J. (2012). CTT – Kolorowy Test Połączeń wersja dla Dorosłych [The Color Trail Test for Adults]. Warszawa: Pracownia Testów Psychologicznych PTP.

Łojek, E., Stańczak, J., Delis, D. C., Kramer, J. H., & Ober, B. A. (2010). Podręcznik do kalifornijskiego testu uczenia się językowego CVLT Deana C. Delisa, Joela H. Kramera, Edith Kaplan i Beth A. Ober: polska normalizacja [Manual of the California Verbal Learning Test CVLT by Dean C. Delis, Joel H. Kramer, Edith Kaplan and Beth A. Ober: Polish normalization]. Warszawa: Pracownia Testów Psychologicznych PTP.

Matthews, C. G., & Klove, H. (1964). Instruction manual for the adult neuropsychology test battery. Madison, WI: University of Wisconsin Medical School. McArthur, J. C., & Brew, B. J. (2010). HIV-associated neurocognitive disorders: Is there a hidden epidemic? AIDS, 24, 1367–1370. https://doi.org/10.1097/ QAD.0b013e3283391d56.

Melrose, R. J., Tinaz, S., Castelo, J. M. B., Courtney, M. G., & Stern, C. E. (2008). Compromised fronto-striatal functioning in HIV: an fMRI investigation of semantic event sequencing. Behavioural Brain Research, 188, 337–347. https://doi. org/10.1016/j.bbr.2007.11.021.

Nath, A. (2015). Eradication of human immunodeficiency virus from brain reservoirs. Journal of Neurovirology, 21, 227–234. https://doi.org/10.1007/s13365- 014-0291-1.

Ortega, M., Brier, M. R., & Ances, B. M. (2015). Effects of HIV and combination antiretroviral therapy (cART) on cortico-striatal functional connectivity. AIDS, 29, 703–712. https://doi.org/10.1097/ QAD.0000000000000611.

Rao, S. M., Bonner-Jackson, A., Nielson, K. A., Seidenberg, M., Smith, J. C., Woodard, J. L., & Durgerian, S. (2015). Genetic risk for Alzheimer’s disease alters the five-year trajectory of semantic memory activation in cognitively intact elders. NeuroImage, 111, 136– 146. https://doi.org/10.1016/j.neuroimage.2015.02.011.

Ruff, R. M. (1996). Ruff figural fluency test: professional manual. Lutz, FL: Psychological Assessment Resources. Seidenberg, M., Guidotti, L., Nielson, K. A., Woodard, J. L., Durgerian, S., Antuono, P., Zhang, Q., & Rao, S. M. (2009). Semantic memory activation in individuals at risk for developing Alzheimer disease. Neurology, 73, 612-620. https://doi.org/10.1212/ WNL.0b013e3181b389ad.

Stańczak, J. (2010). MMSE: polska normalizacja [MMSE: Polish normalization]. Warszawa: Pracownia Testów Psychologicznych PTP. Szepietowska, E. M., & Gawda, B. (2011). Ścieżkami fluencji słownej [The pathways of verbal fluency]. Lublin: Wydawnictwo UMCS.

Tavor, I., Jones, O. P., Mars, R. B., Smith, S. M., Behrens, T. E., & Jbabdi, S. (2016). Task-free MRI predicts individual differences in brain activity during task performance. Science, 352, 216–220. https://doi.org/10.1126/science.aad8127 UNAIDS (2017). AIDSinfo. Retrieved from http://aidsinfo.unaids.org [accessed January 20, 2019].

Wechsler, D. (1981). WAIS-R manual: Wechsler adult intelligence scale-revised. San Antonio, TX: Psychological Corporation. Wellcome Department of Imaging Neuroscience London (2014). Statistical Parametric Mapping Version 12. Retrieved from http://www.fil.ion.ucl.ac.uk/ spm/software/.

Woodard, J. L., Seidenberg, M., Nielson, K. A., Antuono, P., Guidotti, L., Durgerian, S., Zhang, Q., Lancaster, M., Hantke, N., Butts, A., & Rao, S. M. (2009). Semantic memory activation in amnestic mild cognitive impairment. Brain, 132, 2068–2078. https://doi.org/10.1093/brain/awp157.

Woods, S. P., Moore, D. J., Weber, E., & Grant, I. (2009). Cognitive neuropsychology of HIV-associated neurocognitive disorders. Neuropsychology Review, 19, 152–168. https://doi.org/10.1007/ s11065-009-9102-5.

Yang, Y. L., Deng, H. X., Xing, G. Y., Xia, X. L., & Li, H. F. (2015). Brain functional network connectivity based on a visual task: visual information processing-related brain regions are significantly activated in the task state. Neural Regeneration Research, 10, 298–307. https://doi.org/10.4103/1673-5374.152386.