N.A. Karatygin¹, I.I. Korobeinikova², N.V. Karatygina³, Ya.A. Venerina4
1,2 P.K. Anokhin Research Institute of Normal Physiology (Moscow, Russia)
3 Research and clinical Center of Pediatric psychoneurology Moscow Healthcare Department, Russian Federation (Moscow Russia)
4 First Moscow State Medical University n.a. I.M. Sechenov (Moscow, Russia)
At present time conceptions of complex neurophysiological mechanisms underlying processes of attention are actively developing. In last few years, several researches revealed rhythmic character of processes of attention. Especially theta-rhythm is considered to be significant in organization of rhythmic interactions between brain zones, which take part in providing attention systems work. The aim of the work – to analyze and summarize modern date about role of theta-rhythm in providing basic processes of attention. The report presents modern data about role of theta-rhythm in processes of attention. Specific features of attention systems are discussed. Thrifold model of attention, developed by Steven E. Petersen and Michael I. Posner is reviewed in detail. Moreover, evidences of rhythmic character of processes of attention are summarized and leading part of theta-activity in providing these processes is demonstrated. We also discuss the investigations by Randolph F. Helfrich and Ian C. Fiebelkorn et al. which stated that the quantization of processes of attention with theta-frequency as a general principle of brain structures activity. Dependence of frequency characteristics of cortex zones of human brain from number of objects of attention is discussed. There is also an analysis of theta-band’s ability to modulate biopotentials of higher frequency. Special attention is paid to the researches focused on theta-gamma coupling. The influence of theta-rhythm phase on gamma-rhythm amplitude in phase-amplitude coupling of theta- and gamma-band is analyzed.
Theta-rhythm is considered to be one of the rhythmic components that regulate complex mental functions such as attention, memory and consciousness. Obviously, there is a lack of an exact understanding of the role for every band in mental functions regulation; therefore, more investigations in this field are required. However, several data about the role of theta-band in mental functions was collected. A complex of systems with different physiological and neurochemical basis provides attention. It was demonstrated that attention - is a rhythmical process in which theta-band is a crucial part. Theta-rhythm provides synchronization and joint activity of distant brain structures. Moreover, theta-rhythm modulates high-frequent bands. Theta- gamma-band coupling is supposed to be important for attention. Such cooperation is considered to be an evidence of cortical and subcortical zones and provides coordination of analyzing systems of different level. It is suggested that different phases of theta-band may provide retention/switching of attention or determine information flow. As a summary of review of literary sources, there is a conclusion about high significance of this frequency range in different attention systems functioning.
Karatygin N.A., Korobeinikova I.I., Karatygina N.V., Venerina Ya.A. Modern vision of relationship between theta rhythm and the processes of attention. Biomedicine Radioengineering. 2021. V. 24. № 1. P. 60–67. DOI:
10.18127/j15604136-202101-09 (In Russian).
- Buzsáki G. Theta oscillations in the hippocampus. Neuron. 2002. V. 33. № 3. P. 325–340.
- Korotkova T., Ponomarenko A., Monaghan C.K., Poulter S.L., Cacucci F., Wills T., Hasselmo M.E., Lever C. Reconciling the different faces of hippocampal theta: The role of theta oscillations in cognitive, emotional and innate behaviors. Neuroscience & Biobehavioral Reviews. 2018. V. 85. P. 65–80.
- Töllner T., Wang Y., Makeig S., Müller H.J., Jung T.P., Gramann K. Two independent frontal midline theta oscillations during conflict detection and adaptation in a Simon-type manual reaching task. Journal of Neuroscience. 2017. V. 37. № 9. P. 2504–2515.
- Machinskaya R.I. Nejrofiziologicheskie mekhanizmy proizvol'nogo vnimaniya (analiticheskij obzor) // Zhurnal vysshej nervnoj deyatel'nosti im. I.P. Pavlova. 2003. № 53(2). C. 133–150 (In Russian).
- Tsujimoto T., Shimazu H., Isomura Y., Sasaki K. Theta oscillations in primate prefrontal and anterior cingulate cortices in forewarned reaction time tasks. Journal of neurophysiology. 2009. V. 103. № 2. P. 827–843.
- Machinskaya R.I., Kurganskij A.V. Sravnitel'noe elektrofiziologicheskoe issledovanie regulyatornyh komponentov rabochej pamyati u vzroslyh i detej 7–8 let. Analiz kogerentnosti ritmov EEG // Fiziologiya cheloveka. 2012. T. 38(1). S. 5–19 (In Russian).
- Sellers K.K., Yu C., Zhou Z.C., Stitt I., Li Y., Radtke-Schuller S., Alagapan S., Fröhlich F. Oscillatory dynamics in the frontoparietal attention network during sustained attention in the ferret. Cell reports. 2016. V. 16. № 11. P. 2864–2874.
- Petersen S.E., Posner M.I. The attention system of the human brain: 20 years after. Annual review of neuroscience. 2012. V. 35. P. 73–89.
- Li S., Franken P., Vassalli A. Bidirectional and context-dependent changes in theta and gamma oscillatory brain activity in noradrenergic cell-specific Hypocretin/Orexin receptor 1-KO mice. Scientific reports. 2018. V. 8. № 1. P. 154–174.
- Buschman T.J., Kastner S. From behavior to neural dynamics: an integrated theory of attention. Neuron. 2015. V.88. № 1. P. 127–144.
- Rho H.J., Kim J.H., Lee S.H. Function of selective neuromodulatory projections in the mammalian cerebral cortex: Comparison between cholinergic and noradrenergic systems. Frontiers in neural circuits. 2018. V. 12(47) P. 1–13.
- Posner M.I., Rothbart M.K., Ghassemzadeh H. Focus: Attention Science: Restoring Attention Networks. The Yale journal of biology and medicine. 2019. V. 92. № 1. P. 139.
- Vossel S., Geng J.J., Fink G.R. Dorsal and ventral attention systems: distinct neural circuits but collaborative roles. The Neuroscientist. 2014. V. 20. № 2. P. 150–159.
- Fiebelkorn I.C., Kastner S. A Rhythmic Theory of Attention. Trends in Cognitive Sciences. 2019. V. 23. № 2. P. 87–101.
- Ridderinkhof K.R., Ullsperger M., Crone E.A., Nieuwenhuis S. The role of the medial frontal cortex in cognitive control. Science. 2004. V. 306. № 5695. P. 443–447.
- Van de Vijver I., Ridderinkhof K.R., Cohen M.X. Frontal oscillatory dynamics predict feedback learning and action adjustment. Journal of cognitive neuroscience. 2011. V. 23. № 12. P. 4106–4121.
- Thiele A., Bellgrove M.A. Neuromodulation of attention. Neuron. 2018. V. 97. № 4. P. 769–785.
- Posner M.I., Rothbart M.K., Sheese B.E., Voelker P. Developing attention: Behavioral and brain mechanisms. Advances in Neuroscience. 2014. Article ID 405094.
- Kichigina V.F. Dopaminergic regulation of theta activity of septohippocampal neuron in the awake rabbit. Zhurnal vysshei nervnoi deiatelnosti imeni I.P. Pavlova. 2004. V. 54. № 2. P. 210–215.
- Puig M.V., Gener T. Serotonin modulation of prefronto-hippocampal rhythms in health and disease. ACS chemical neuroscience. 2015. V. 6. № 7. P. 1017–1025.
- Clayton M.S., Yeung N., Kadosh R.C. The roles of cortical oscillations in sustained attention. Trends in cognitive sciences. 2015. V. 19. № 4. P. 188–195.
- Stitt I., Zhou Z.C., Radtke-Schuller S., Fröhlich F. Arousal dependent modulation of thalamo-cortical functional interaction. Nature communications. 2018. V. 9. № 1. P. 24–55.
- Yu C., Li Y., Stitt I.M., Zhou Z.C., Sellers K.K., Frohlich F. Theta oscillations organize spiking activity in higher-order visual thalamus during sustained attention. ENeuro. 2018. V. 5. № 1. P. 1–11.
- Nakajima M., Schmitt L.I., Halassa M.M. Prefrontal Cortex Regulates Sensory Filtering through a Basal Ganglia-to-Thalamus Pathway. Neuron. 2019. V. 103. № 1. P. 445–458.
- Helfrich R.F., Fiebelkorn I.C., Szczepanski S.M., Lin J.J., Parvizi J., Knight R.T., Kastner S. Neural mechanisms of sustained attention are rhythmic. Neuron. 2018. V. 99. № 4. P. 854–865.
- Fiebelkorn I.C., Pinsk M.A., Kastner S. A dynamic interplay within the frontoparietal network underlies rhythmic spatial attention. Neuron. 2018. V. 99. № 4. P. 842–853.
- Davidson M.J., Alais D., van Boxtel J.J., Tsuchiya N. Attention periodically samples competing stimuli during binocular rivalry. Elife. 2018. V. 7. P. 408–468.
- Jia J., Liu L., Fang F., Luo H. Sequential sampling of visual objects during sustained attention. PLoS biology. 2017. V. 15. № 6. P. e2001903.
- Holcombe A.O., Chen W.Y. Splitting attention reduces temporal resolution from 7 Hz for tracking one object to< 3 Hz when tracking three. Journal of vision. 2013. V. 13. № 11(12). P. 11–19.
- Womelsdorf T., Fries P. The role of neuronal synchronization in selective attention. Current opinion in neurobiology. 2007. V. 17. № 2. P. 154–160.
- Herrmann C.S., Strüber D., Helfrich R.F., Engel A.K. EEG oscillations: from correlation to causality. International Journal of Psychophysiology. 2016. V. 103. P. 12–21.
- Lisman J.E., Jensen O. The theta-gamma neural code. Neuron. 2013. V. 77. № 6. P. 1002–1016.
- Bagur S., Benchenane K. The Theta Rhythm Mixes and Matches Gamma Oscillations Cycle by Cycle. Neuron. 2018. V. 100. № 4. P. 768–771.
- Wolinski N., Cooper N.R., Sauseng P., Romei V. The speed of parietal theta frequency drives visuospatial working memory capacity. PLoS biology. 2018. V. 16. № 3. P. e2005348.
- Liesefeld H.R., Müller H.J. Current directions in visual working memory research: An introduction and emerging insights. British Journal of Psychology. 2019. V. 110. № 2. P.193–206.
- Sellers K.K., Yu C., Zhou Z.C., Stitt I., Li Y., Radtke-Schuller S., Alagapan S., Fröhlich F. Oscillatory dynamics in the frontoparietal attention network during sustained attention in the ferret. Cell reports. 2016. V. 16. № 11. P. 2864–2874.
- Gregoriou G.G., Rossi A.F., Ungerleider L.G., Desimone R. Lesions of prefrontal cortex reduce attentional modulation of neuronal responses and synchrony in V4. Nature neuroscience. 2014. V. 17. № 7. P. 1003–1011.
- Van de Vijver I., Ridderinkhof K.R., Cohen M.X. Frontal oscillatory dynamics predict feedback learning and action adjustment. Journal of cognitive neuroscience. 2011. V. 23. № 12. P. 4106–4121.
- Oehrn C.R., Hanslmayr S., Fell J., Deuker L., Kremers N.A., Do Lam A.T., Elger C.E., Axmacher N. Neural communication patterns underlying conflict detection, resolution, and adaptation. Journal of Neuroscience. 2014. V.34. № 31. P. 10438–10452.