Slow negative potentials associated with preparation period of memory-guided saccades and antisaccades in healthy individuals and subjects at clinical-high risk for schizophrenia

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Abstract

The concept of clinical-high risk (CHR) for schizophrenia implies the possibility of identifying a potential predisposition to future schizophrenia manifestation. An important goal of biological psychiatry is conducting research aimed at understanding the neurophysiological mechanisms of this condition. In this study, saccade characteristics of patients at CHR for schizophrenia (n = 15) and healthy participants (n = 15), as well as parameters of their slow negative potentials in the one-second interval preceding the signal to perform a saccade in a “memory-guided saccades/antisaccades” paradigm were analyzed. 12 participants from the CHR group also underwent magnetic resonance imaging (MRI) for subsequent comparison with the control group selected from the laboratory database. Saccade latencies and error rates were higher in the CHR group. There were also found lateral differences in CHR, but not in the control group. However, no between-group differences were observed in studied electrophysiological and MRI parameters. The obtained results may be interpreted as indirect signs of impairments in executive control, interhemispheric asymmetry and connectivity in the CHR group, although further studies are required to determine the possibility of using slow negative potentials parameters as clinical markers.

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About the authors

A. P. Dzhem

Mental Health Research Center

Author for correspondence.
Email: npjam@mail.ru
Russian Federation, Moscow

A. V. Pavlov

Moscow State University

Email: npjam@mail.ru
Russian Federation, Moscow

A. S. Tomyshev

Mental Health Research Center

Email: npjam@mail.ru
Russian Federation, Moscow

M. A. Omelchenko

Mental Health Research Center

Email: npjam@mail.ru
Russian Federation, Moscow

V. G. Kaleda

Mental Health Research Center

Email: npjam@mail.ru
Russian Federation, Moscow

M. V. Slavutskaya

Mental Health Research Center; Moscow State University

Email: npjam@mail.ru
Russian Federation, Moscow; Moscow

I. S. Lebedeva

Mental Health Research Center

Email: npjam@mail.ru
Russian Federation, Moscow

References

  1. Enderle J.D. Neural control of saccades // Prog. Brain Res. 2002. V. 140. P. 21.
  2. Herwig A., Beisert M., Schneider W.X. On the spatial interaction of visual working memory and attention: Evidence for a global effect from memory-guided saccades // J. Vis. 2010. V. 10. № 5. P. 8.
  3. Yung A.R., McGorry P.D., McFarlane C.A. et al. Monitoring and care of young people at incipient risk of psychosis // Schizophr. Bull. 1996. V. 22. № 2. P. 283.
  4. Kleineidam L., Frommann I., Ruhrmann S. et al. Antisaccade and prosaccade eye movements in individuals clinically at risk for psychosis: Comparison with first-episode schizophrenia and prediction of conversion // Eur. Arch. Psychiatry Clin. Neurosci. 2019. V. 269. № 8. P. 921.
  5. Obyedkov I., Skuhareuskaya M., Skugarevsky O. et al. Saccadic eye movements in different dimensions of schizophrenia and in clinical high-risk state for psychosis // BMC Psychiatry. 2019. V. 19. № 1. P. 110.
  6. Schurger A., Hu P. 'Ben', Pak J., Roskies A.L. What Is the Readiness Potential? // Trends Cogn. Sci. 2021. V. 25. № 7. P. 558.
  7. Van Der Stigchel S., Heslenfeld D.J., Theeuwes J. An ERP study of preparatory and inhibitory mechanisms in a cued saccade task // Brain Res. 2006. V. 1105. № 1. P. 32.
  8. Walter W.G., Cooper R., Aldridge V.J. et al. Contingent Negative Variation: An Electric Sign of Sensori-Motor Association and Expectancy in the Human Brain // Nature. 1964. V. 203. № 4943. P. 380.
  9. Klein C., Heinks T., Andresen B. et al. Impaired modulation of the saccadic contingent negative variation preceding antisaccades in schizophrenia // Biol. Psychiatry. 2000. V. 47. № 11. P. 978.
  10. Tomyshev A.S., Lebedeva I.S., Akhadov T.A. et al. Alterations in white matter microstructure and cortical thickness in individuals at ultra-high risk of psychosis: A multimodal tractography and surface-based morphometry study // Psychiatry Res. Neuroimaging. 2019. V. 289. P. 26.
  11. Liloia D., Brasso C., Cauda F. et al. Updating and characterizing neuroanatomical markers in high-risk subjects, recently diagnosed and chronic patients with schizophrenia: A revised coordinate-based meta-analysis // Neurosci. Biobehav. Rev. 2021. V. 123. P. 83.
  12. Dudina A.N., Tomyshev A.S., Omelchenko M.A. et al. [Structural features of the brain in individuals with youth depression at a clinical risk for psychosis] // Zh. Nevrol. Psikhiatr. Im. S.S. Korsakova. 2023. V. 123. № 6. P. 94.
  13. Mento G. The role of the P3 and CNV components in voluntary and automatic temporal orienting: A high spatial-resolution ERP study // Neuropsychologia. 2017. V. 107. P. 31.
  14. Duma G.M., Granziol U., Mento G. Should I stay or should I go? How local-global implicit temporal expectancy shapes proactive motor control: An hdEEG study // NeuroImage. 2020. V. 220. P. 117071.
  15. Omelchenko M.A. [Negative symptoms at the prodromal stage of schizophrenia at a young age (current problems of diagnostics and treatment)] // V.M. Bekhterev Review of Psychiatry and Medical Psychology. 2019. № 4–2. P. 41.
  16. Hikosaka O., Wurtz R.H. Visual and oculomotor functions of monkey substantia nigra pars reticulata. III. Memory-contingent visual and saccade responses // J. Neurophysiol. 1983. V. 49. № 5. P. 1268.
  17. Fischl B. FreeSurfer // NeuroImage. 2012. V. 62. № 2. P. 774.
  18. Desikan R.S., Ségonne F., Fischl B. et al. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest // NeuroImage. 2006. V. 31. № 3. P. 968.
  19. Gnezditsky V.V. [Evoked Brain Potentials in Clinical Practice]. Taganrog: TRTU Publishing House, 1997. 252 p.
  20. Ettinger U., Kumari V., Chitnis X.A. et al. Volumetric Neural Correlates of Antisaccade Eye Movements in First-Episode Psychosis // Am. J. Psychiatry. 2004. V. 161. № 10. P. 1918.
  21. Ekin M., Akdal G., Bora E. Antisaccade error rates in first-episode psychosis, ultra-high risk for psychosis and unaffected relatives of schizophrenia: A systematic review and meta-analysis // Schizophr. Res. 2024. V. 266. P. 41.
  22. Camchong J., Dyckman K.A., Austin B.P. et al. Common neural circuitry supporting volitional saccades and its disruption in schizophrenia patients and relatives // Biol. Psychiatry. 2008. V. 64. № 12. P. 1042.
  23. Liu W., Cai X., Chang Y. et al. Structural abnormalities in the Fronto-Parietal Network: Linking white matter integrity to sustained attention deficits in Schizophrenia // Brain Res. Bull. 2023. V. 205. P. 110818.
  24. Amador X.F., Malaspina D., Sackeim H.A. et al. Visual fixation and smooth pursuit eye movement abnormalities in patients with schizophrenia and their relatives // J. Neuropsychiatry Clin. Neurosci. 1995. V. 7. № 2. P. 197.
  25. Sklar A.L., Coffman B.A., Salisbury D.F. Localization of early-stage visual processing deficits at schizophrenia spectrum illness onset using magnetoencephalo-graphy // Schizophr. Bull. 2020. V. 46. № 4. P. 955.
  26. Gold J.M., Luck S.J. Working Memory in People with Schizophrenia // Curr. Top. Behav. Neurosci. 2022. V. 63. P. 137.
  27. Spagna A., Kim T.H., Wu T., Fan J. Right hemisphere superiority for executive control of attention // Cortex. 2020. V. 122. P. 263.
  28. Barrett G., Shibasaki H., Neshige R. Cortical potentials preceding voluntary movement: Evidence for three periods of preparation in man // Electroencephalogr. Clin. Neurophysiol. 1986. V. 63. № 4. P. 327.
  29. Kukleta M., Lamarche M. The early component of the premovement readiness potential and its behavioral determinants // Cogn. Brain Res. 1998. V. 6. № 4. P. 273.
  30. Kirenskaya A.V., Myamlin V.V., Novototsky-Vlasov V.Y. et al. The contingent negative variation laterality and dynamics in antisaccade task in normal and unmedicated schizophrenic subjects // Spanish J. Psychol. 2011. V. 14. № 2. P. 869.
  31. Tseng P., Chang C.F., Chiau H.Y. et al. The dorsal attentional system in oculomotor learning of predictive information // Front. Hum. Neurosci. 2013. V. 7. P. 404.
  32. Beck V.M., Vickery T.J. Oculomotor capture reveals trial-by-trial neural correlates of attentional guidance by contents of visual working memory // Cortex. 2020. V. 122. P. 159.
  33. Jonikaitis D., Noudoost B., Moore T. Dissociating the contributions of frontal eye field activity to spatial working memory and motor preparation // J. Neurosci. 2023. V. 43. № 50. P. 8681.
  34. Yokoyama O., Nishimura Y. Preselection of potential target spaces based on partial information by the supplementary eye field // Commun. Biol. 2024. V. 7. № 1. P. 1215.
  35. Jones D.T., Graff-Radford J. Executive Dysfunction and the Prefrontal Cortex // Continuum Lifelong Learning in Neurology. 2021. V. 27. № 6. P. 1586.
  36. Yang G., Wu H., Li Q. et al. Dorsolateral prefrontal activity supports a cognitive space organization of cognitive control // eLife. 2024. V. 12. P. RP87126.
  37. Numssen O., Bzdok D., Hartwigsen G. Functional specialization within the inferior parietal lobes across cognitive domains // eLife. 2021. V. 10. P. e63591.
  38. Andersen R.A., Cui H. Intention, action planning, and decision making in parietal-frontal circuits // Neuron. 2009. V. 63. № 5. P. 568.
  39. Talanow T., Kasparbauer A.M., Lippold J.V. et al. Neural correlates of proactive and reactive inhibition of saccadic eye movements // Brain Imaging Behav. 2020. V. 14. № 1. P. 72.
  40. Osborne K.J., Zhang W., Farrens J. et al. Neural mechanisms of motor dysfunction in individuals at clinical high-risk for psychosis: Evidence for impairments in motor activation. // J. Psychopathol. Clin. Sci. 2022. V. 131. № 4. P. 375.
  41. Di Russo F., Berchicci M., Bianco V. et al. Normative event-related potentials from sensory and cognitive tasks reveal occipital and frontal activities prior and following visual events // NeuroImage. 2019. V. 196. P. 173.
  42. Schneider D., Zickerick B., Thönes S., Wascher E. Encoding, storage, and response preparation — Distinct EEG correlates of stimulus and action representations in working memory // Psycho-physiology. 2020. V. 57. № 6. P. e13577.
  43. Reilly J.L., Lencer R., Bishop J.R. et al. Pharmacological treatment effects on eye movement control // Brain Cogn. 2008. V. 68. № 3. P. 415.
  44. Wen M., Dong Z., Zhang L. et al. Depression and Cognitive Impairment: Current Understanding of Its Neurobiology and Diagnosis // Neuropsychiatr. Dis. Treat. 2022. V. 18. P. 2783.

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2. Fig. 1. Stimulus presentation scheme. CFS — central fixation stimulus, PS — peripheral stimulus, CS — corrective stimulus. The scheme is presented for illustrative purposes, the proportions of the stimuli are not observed.

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3. Fig. 2. Average components of slow negative pre-stimulus potentials (SNP). A – average slow potentials of 15 healthy participants (solid line) and 15 patients with clinically high risk (CHR) of schizophrenia (dashed line) before saccades to the right. The moment of switching off the central fixation stimulus is indicated by an arrow. B – maps of the distribution of the peak amplitude of the components of SNP1, SNP2 and SNP3 in the groups of healthy participants (1) and patients with CHR of schizophrenia (2) before saccades to the right.

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