EEG-Neurofeedback Training and Prolidase in Anxiety Disorders: An Exploratory Study

Authors

  • Pratibha Meena, Ms PhD Scholar, Dept. of Clinical Psychology https://orcid.org/0000-0002-1603-5123
  • Sarada Subramanian, Dr. National Institute of Mental Health and Neurosciences
  • Geetha Desai, Dr. National Institute of Mental Health and Neurosciences
  • Geethu Krishna, Ms National Institute of Mental Health and Neurosciences
  • Jamuna Rajeswaran National Institute of Mental Health and Neurosciences

DOI:

https://doi.org/10.15540/nr.9.3.127

Keywords:

anxiety disorders, prolidase, proline, EEG-neurofeedback training, neurocognitive functions, executive functions

Abstract

Objective: Prolidase is an enzyme that releases proline and is vital in extracellular matrix (ECM) remodeling, fueling white matter dynamics. Serum prolidase activity (SPA) is elevated in various neuropsychiatric conditions and may influence cognitive functions. Aim of the study was to explore the relation of SPA to neuropsychological functioning and its response to treatment in anxiety disorders. Methods: Twenty demographic-matched patients with anxiety were recruited. Six patients were given EEG-neurofeedback training (EEG-NFT), eight were treated pharmacologically (treatment as usual; TAU) with EEG-NFT, and six patients were treated only pharmacologically (TAU group). Beck Anxiety Inventory (BAI) and Beck Depression Inventory (BDI) were used to assess anxiety and comorbid depression, respectively. Results: Symptom reduction was seen in all groups. SPA decreased considerably in EEG-NFT group. Mental speed and spatial working memory negatively correlated with SPA in EEG-NFT group. Focused attention, sustained attention, verbal working memory, and spatial construction ability negatively correlated with SPA in EEG-NFT+TAU group. Mental speed in TAU group was also inversely proportional to SPA. Conclusion: Inverse correlation between SPA and neuropsychological functions in EEG-NFT group is suggestive of prolidase-mediated microstructural changes in white matter, which may have an influence on cognitive enhancement in anxiety disorders (AD).

References

Abdian, H., Rezaei, M., Eskandari, Z., Ramezani, S., Pirzeh, R., & Dadashi, M. (2021). The effect of quantitative electroencephalography-based neurofeedback therapy on anxiety, depression, and emotion regulation in people with generalized anxiety disorder. Basic and Clinical Neuroscience, 12(2), 281–290. https://doi.org/10.32598/bcn.12.2.2378.1

Ault, B., Wang, C. M., & Yawn, B. C. (1987). L-proline depolarizes rat spinal motoneurones by an excitatory amino acid antagonist-sensitive mechanism. British Journal of Pharmacology, 92(2), 319–326. https://doi.org/10.1111/j.1476-5381.1987.tb11326.x

Bavaresco, C. S., Luíz Streck, E., Netto, C. A., & de Wyse, A. T. S. (2005). Chronic hyperprolinemia provokes a memory deficit in the Morris water maze task. Metabolic Brain Disease, 20(1), 73–80. https://doi.org/10.1007/s11011-005-2478-x

Burnside, E. R., & Bradbury, E. J. (2014). Manipulating the extracellular matrix and its role in brain and spinal cord plasticity and repair. Neuropathology and Applied Neurobiology, 40(1), 26–59. https://doi.org/10.1111/nan.12114

Chinard, F. P., 1952. Photometric estimation of proline and ornithine. Journal of Biological Chemistry, 199(1), 91–95. https://doi.org/10.1016/S0021-9258(18)44814-4

Cohen, S. M., & Nadler, J. V. (1997). Proline-induced potentiation of glutamate transmission. Brain Research, 761(2), 271–282. https://doi.org/10.1016/S0006-8993(97)00352-1

Coull, J. T., Frith, C. D., Frackowiak, R. S. J., & Grasby, P. M. (1996). A fronto-parietal network for rapid visual information processing: A PET study of sustained attention and working memory. Neuropsychologia, 34(11), 1085–1095. https://doi.org/10.1016/0028-3932(96)00029-2

Delwing, D., Bavaresco, C. S., Chiarani, F., Wannmacher, C. M. D., Wajner, M., Dutra-Filho, C. S., & Wyse, A. T. S. (2003a). In vivo and in vitro effects of proline on some parameters of oxidative stress in rat brain. Brain Research, 991(1–2), 180–186. https://doi.org/10.1016/j.brainres.2003.08.014

Delwing, D., Bavaresco, C. S., Wannmacher, C. M. D., Wajner, M., Dutra-Filho, C. S., & Wyse, A. T. S. (2003b). Proline induces oxidative stress in cerebral cortex of rats. International Journal of Developmental Neuroscience, 21(2), 105–110. https://doi.org/10.1016/S0736-5748(02)00109-0

Delwing, D., Chiarani, F., Bavaresco, C. S., Wannmacher, C. M., D., Wajner, M., Dutra-Filho, C. S., & Wyse, A. T. S. (2005). Protective effect of antioxidants on brain oxidative damage caused by proline administration. Neuroscience Research, 52(1), 69–74. https://doi.org/10.1016/j.neures.2005.01.011

Delwing, D., Delwing, D., Sanna, R. J., Wofchuk, S., & Wyse, A. T. S. (2007). Proline promotes decrease in glutamate uptake in slices of cerebral cortex and hippocampus of rats. Life sciences, 81(25–26), 1645–1650. https://doi.org/10.1016/j.lfs.2007.09.031

Demerens, C., Stankoff, B., Logak, M., Anglade, P., Allinquant, B., Couraud, F., Zalc, B., & Lubetzki, C. (1996). Induction of myelination in the central nervous system by electrical activity. Proceedings of the National Academy of Sciences of the United States of America, 93(18), 9887–9892. https://doi.org/10.1073/pnas.93.18.9887

Ercan, A. C., Bahceci, B., Polat, S., Cenker, O. C., Bahceci, I., Koroglu, A., Sahin, K., & Hocaoglu, C. (2017). Oxidative status and prolidase activities in generalized anxiety disorder. Asian Journal of Psychiatry, 25, 118–122. https://doi.org/10.1016/j.ajp.2016.10.008

Figueroa-Vargas, A., Cárcamo, C., Henríquez-Ch, R., Zamorano, F., Ciampi, E., Uribe-San-Martin, R., Vásquez, M., Aboitiz, F., & Billeke, P. (2020). Frontoparietal connectivity correlates with working memory performance in multiple sclerosis. Scientific Reports, 10, Article 9310. https://doi.org/10.1038/s41598-020-66279-0

Garakani, A., Murrough, J. W., Freire, R. C., Thom, R. P., Larkin, K., Buono, F. D., & Iosifescu, D. V. (2020). Pharmacotherapy of anxiety disorders: Current and emerging treatment options. Frontiers in Psychiatry, 11, Article 595584. https://doi.org/10.3389/fpsyt.2020.595584

Ghaziri, J., Tucholka, A., Larue, V., Blanchette-Sylvestre, M., Reyburn, G., Gilbert, G., Lévesque, J., & Beauregard, M. (2013). Neurofeedback training induces changes in white and gray matter. Clinical EEG and Neuroscience, 44(4), 265–272. https://doi.org/10.1177/1550059413476031

Güneş, M., Bulut, M., Demir, S., İbiloğlu, A. O., Kaya, M. C., Atlı, A., Kaplan, İ., Camkurt, A., & Sir, A. (2016). Diagnostic performance of increased prolidase activity in schizophrenia. Neuroscience Letters, 613, 36–40. https://doi.org/10.1016/j.neulet.2015.12.036

Hammond, D. C. (2005). Neurofeedback with anxiety and affective disorders. Child and Adolescent Psychiatric Clinics of North America, 14(1), 105–123. https://doi.org/10.1016/j.chc.2004.07.008

Insolia, V., Priori, E. C., Gasperini, C., Coppa, F., Cocchia, M., Iervasi, E., Ferrari, B., Besio, R., Maruelli, S., Bernocchi, G., Forlino, A., & Bottone, M. G. (2020). Prolidase enzyme is required for extracellular matrix integrity and impacts on postnatal cerebellar cortex development. Journal of Comparative Neurology, 528(1), 65–84. https://doi.org/10.1002/cne.24735

Ishibashi, T., Dakin, K. A., Stevens, B., Lee, P. R., Kozlov, S. V., Stewart, C. L., & Fields, R. D. (2006). Astrocytes promote myelination in response to electrical impulses. Neuron, 49(6), 823–832. https://doi.org/10.1016/j.neuron.2006.02.006

Kokacya, H. M., Bahceci, B., Bahceci, I., Ramazan Dilek, A., & Dokuyucu, R. (2014). Prolidase activity and oxidative stress in patients with major depressive disorder. Psychiatria Danubina, 26(4), 314–318.

Krishna G., Sivakumar P. T., Dahale, A. B., Isaac T. G., Mukku, S. S. R., Prabha M. L., Unni, A. K. N., Sinha, P., Varghese, M., & Subramanian S. (2020). Increased prolidase activity in Alzheimer’s dementia: A case control study. Asian Journal of Psychiatry, 53, Article 102242. https://doi.org/10.1016/j.ajp.2020.102242

Lajtha, A., & Toth, J. (1974). Postmortem changes in the cerebral free amino acid pool. Brain Research, 76(3), 546–551. https://doi.org/10.1016/0006-8993(74)90833-6

Micoulaud-Franchi, J. A., Jeunet, C., Pelissolo, A., & Ros, T. (2021). EEG neurofeedback for anxiety disorders and post-traumatic stress disorders: A blueprint for a promising brain-based therapy. Current Psychiatry Reports, 23(12), 1–14. https://doi.org/10.1007/s11920-021-01299-9

Moore, N. C. (2000). A review of EEG biofeedback treatment of anxiety disorders. Clinical Electroencephalography, 31(1), 1–6. https://doi.org/10.1177/155005940003100105

Myara, I., Charpentier, C., & Lemonnier, A. (1982). Optimal conditions for prolidase assay by proline colorimetric determination: Application to iminodipeptiduria. Clinica Chimica Acta, 125(2), 193–205. https://doi.org/10.1016/0009-8981(82)90196-6

Nadler, J. V., Wang, A., Hakim, A. (1988). Toxicity of L-proline toward rat hippocampal neurons. Brain Research, 456(1), 168–172. https://doi.org/10.1016/0006-8993(88)90358-7

Namiduru, E. S. (2016). Prolidase. Bratislava Medical Journal, 117(8), 480–485. https://doi.org/10.4149/BLL_2016_093

Nasir, M., Trujillo, D., Levine, J., Dwyer, J. B., Rupp, Z. W., & Bloch, M. H. (2020). Glutamate systems in DSM-5 anxiety disorders: Their role and a review of glutamate and GABA psychopharmacology. Frontiers in Psychiatry, 11, Article 548505. https://doi.org/10.3389/fpsyt.2020.548505

Ramshaw, J. A. M., Shah, N. K., & Brodsky, B. (1998). Gly-XY tripeptide frequencies in collagen: A context for host–guest triple-helical peptides. Journal of Structural Biology, 122(1–2), 86–91. https://doi.org/10.1006/jsbi.1998.3977

Rao, S. L., Subbakrishna, D. K., & Gopukumar, K. (2004). NIMHANS neuropsychology battery-2004, manual. National Institute of Mental Health and Neurosciences.

Ros, T., Munneke, M. A. M., Ruge, D., Gruzelier, J. H., & Rothwell, J. C. (2010). Endogenous control of waking brain rhythms induces neuroplasticity in humans. European Journal of Neuroscience, 31(4), 770–778. https://doi.org/10.1111/j.1460-9568.2010.07100.x

Sagar, R., Dandona, R., Gururaj, G., Dhaliwal, R. S., Singh, A., Ferrari, A., Dua, T., Ganguli, A., Varghese, M., Chakma, J. K., Kumar, G. A., Shaji, K. S., Ambekar, A., Rangaswamy, T., Vijayakumar, L., Agarwal, V., Krishnankutty, R. P., Bhatia, R., Charlson, F., Chowdhary, F., … & Dandona, L. (2020). The burden of mental disorders across the states of India: The Global Burden of Disease Study 1990–2017. The Lancet Psychiatry, 7(2), 148–161. https://doi.org/10.1016/S2215-0366(19)30475-4

Scolari, M., Seidl-Rathkopf, K. N., & Kastner, S. (2015). Functions of the human frontoparietal attention network: Evidence from neuroimaging. Current Opinion in Behavioral Sciences, 1, 32–39. https://doi.org/10.1016/j.cobeha.2014.08.003

Selek, S., Altindag, A., Saracoglu, G., Celik, H., & Aksoy, N. (2011). Prolidase activity and its diagnostic performance in bipolar disorder. Journal of Affective Disorders, 129(1–3), 84–86. https://doi.org/10.1016/j.jad.2010.09.003

Stein, D. J., Scott, K. M., de Jonge, P., & Kessler, R. C. (2017). Epidemiology of anxiety disorders: From surveys to nosology and back. Dialogues in Clinical Neuroscience, 19(2), 127–136. https://doi.org/10.31887/DCNS.2017.19.2/dstein

Takeuchi, H., Sekiguchi, A., Taki, Y., Yokoyama, S., Yomogida, Y., Komuro, N., Yamanouchi, T., Suzuki, S., & Kawashima, R. (2010). Training of working memory impacts structural connectivity. The Journal of Neuroscience, 30(9), 3297–3303. https://doi.org/10.1523/JNEUROSCI.4611-09.2010

Verma, A. K., Bajpai, A., Keshari, A. K., Srivastava, M., Srivastava, S., & Srivastava, R. (2017). Association of major depression with serum prolidase activity and oxidative stress Journal of Advances in Medicine and Medical Research, 20(4), 1–8. https://doi.org/10.9734/BJMMR/2017/31446

Vismara, M., Girone, N., Cirnigliaro, G., Fasciana, F., Vanzetto, S., Ferrara, L., Priori, A., D’Addario, C., Viganò, C. & Dell’Osso, B. (2020). Peripheral biomarkers in DSM-5 anxiety disorders: An updated overview. Brain Sciences, 10(8), 564. https://doi.org/10.3390/brainsci10080564

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Published

2022-09-29

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Research Papers