• 1990 (Vol.4)
  • 1989 (Vol.3)
  • 1988 (Vol.2)
  • 1987 (Vol.1)

Multisensory information processing in visual, auditory and gustatory sensory systems with involvement of infraslow brain potential oscillations

© 2016 K. S. Pugachev, I. V. Filippov, A. A. Krebs, E.A. Zelentsov, E.V. Zyuzin, P. M. Maslyukov

Department of Physiology and Biophysics, Yaroslavl State Medical University (YSMU), 150000, Russia, Yaroslavl, Revolutsionnaya Street, 5

Received 03 Feb 2015

The aim of this work was to reveal and to analyze alterations of infraslow brain oscillations (ISO) in the range of seconds, dozens of seconds and minutes over projections of: the visual cortex (O1) under not only photic but also acoustic and taste stimulus exposure; the auditory cortex (T3) under not only acoustic but also visual and taste sensory stimulation; the frontal neocortex (Fp1) under application of not only gustatory but also visual and acoustic stimuli. We included 16 healthy human volunteers (8 men, 8 women) with the age of 24–41 (n = 48 repeated recordings). The recordings have been done by means of surface scalp Ag/AgCl electrodes, multichannel AC/DC amplifier and analog-to- digital converter. It was found the presence of continuous spontaneous dynamics of ISO in O1, T3 and Fp1 recordings under all experimental conditions that we used, these were ISO in the domain of seconds (frequencies of 0.1–0.5 Hz), dozens of seconds (0.0167–0.l Hz) and minutes (frequencies of less than 0.0167 Hz). We documented statistically significant different modifications of ISO in the domain of sends and dozens of seconds over projection of visual cortex (in O1 recordings) under conditions of not only photic but also acoustic and taste stimulus exposure. There were observed significant separate changes of ISO in the range of seconds and dozens of seconds over projections of auditory cortex (in T3 recordings) in response of not only to acoustic but to photic and gustatory sensory stimulation. Additionally, we determined statistically significant diverse alterations of ISO dynamics in the domain of sends and dozens of seconds over projection of frontal neocortex (in Fp1 recordings) under conditions of not only various testants application but also to visual and acoustic stimulus presentations. Obtained results indicate that ISO in the domain of seconds and multisecond fluctuations are involved in the multisensory afferent information processing by means of their spectral power shifts, moreover these ISO spectral pattern responses have both sensory modality-specific and sensory stimulus-specific properties.

Key words: infraslow brain potential oscillations, multisensory information processing, electrophysiology, sensory system physiology, visual cortex, auditory cortex, frontal neocortex

Cite: Pugachev K. S., Filippov I. V., Krebs A. A., Zelentsov E. A., Zyuzin E. V., Maslyukov P. M. Multisensornye protsessy pererabotki informatsii v korkovykh predstavitelstvakh zritelnoi, slukhovoi i vkusovoi sensornykh sistem cheloveka pri uchastii sverkhmedlennykh kolebanii potentsialov [Multisensory information processing in visual, auditory and gustatory sensory systems with involvement of infraslow brain potential oscillations]. Sensornye sistemy [Sensory systems]. 2016. V. 30(1). P. 79-95 (in Russian).

References:

  • Aladzhalova N.A. Slow electrical processes in the brain. Moscow. 1962. 240 p. [in Russian].
  • Aladzhalova N.A. Psychophysiological aspects of very slow rhythmic activity of the brain. Moscow. Nauka, 1979. 214 p. [in Russian].
  • Bibikov N.G., Dymov А.В. Fano’s and Allan’s factors describing the process of spontaneous impulse activity of auditory neurons of the medulla oblongata of the frog // Sensory systems. 2009. V. 23(3). P. 246–259 [in Russian].
  • Gnezdickij V.V. The inverse task of EEG and clinical electroencephalography. Taganrog. TRTU, 2000. 640 p. [in Russian].
  • Glanc S. Biomedical statistics. Moscow. Practika, 1999. 459 p. [in Russian].
  • Ilyuhina V.A. Very slow bioelectrical activity of the human brain. Leningrad. Nauka, 1977. 184 p. [in Russian].
  • Ilyuhina V.A. Neurophysiology of functional states of human. Leningrad. Nauka,1986. 173 p. [in Russian].
  • Ilyuhina V.A. The human brain in the mechanisms of information and control interactions of the organism and the environment. Saint Petersburg. Institute of Human Brain RAS, 2004. 321 p. [in Russian].
  • Krebs А.А., Pugachev K.S., Filippov I.V., Maslyukov P.M., Zyuzin E.V. Modulatory Influences of Amygdala on Dynamics of Infraslow Brain Potentials in Primary Cortical Sensory Areas of the Rat Brain // Yaroslavl Pedagogical Bulletin. 2013. V. 3 (2). P. 86– 92 [in Russian].
  • Krebs А.А., Filippov I.V., Pugachev K.S., Zyuzin E.V., Maslyukov P.M. The influences of neuromodulatory centers on very slow bioelectrical activity of primary cortical sensory areas of the brain // Sensory systems. 2015. V. 29 (2). P. 154– 169 [in Russian].
  • Pugachev K.S., Krebs А.А., Filippov I.V. Multisensory information processing in primary sensory cortical areas of brain sensory systems// Proceedings of the Komi Science Centre of the Ural Division of the Russian Academy of Sciences. 2012. No 4(12). P. 54–59 [in Russian].
  • Pugachev K.S., Krebs А.А., Filippov I.V., Zyuzin E.V. Infraslow brain potentials of neuromodulatory centers and highest cortical sensory areas // Proceedings of the Komi Science Centre of the Ural Division of the Russian Academy of Sciences. 2014. No 1(17). P. 51–56 [in Russian].
  • Urbah Y.V. Statistical analysis in biological and medical research. Moscow. Medicine, 1975. 295 p. [in Russian].
  • Filippov I.V., Krebs А.А., Pugachev K.S. Infraslow bioelectrical activity of the medial geniculate nucleus and primary auditory cortex after their successive electrical stimulation // Sensory systems. 2006. V. 20 (3). P. 245–252 [in Russian].
  • Filippov I.V. Infraslow bioelectrical activity in the lateral geniculate nucleus and primary visual cortex as a correlate of visual information neural processing // Sensory systems. 2007 a. V. 21 (3). P. 165–173 [in Russian].
  • Filippov I.V. Changes of infraslow brain potentials in the lateral geniculate nucleus and primary visual cortex after their one-by-one respective electrostimulation // Sensory systems. 2007 b. V. 21 (4). P. 339–348 [in Russian].
  • Filippov I.V., Krebs А.А., Pugachev K.S. Modulation effects of brainstem nuclei on infraslow bioelectrical activity in the primary auditory cortex // Sensory systems. 2007. V. 21 (3). P. 237–245 [in Russian].
  • Filippov I.V., Krebs А.А., Pugachev K.S. Infraslow brain potentials of the rat brain gustatory system sites under application of various taste stimuli // Sensory systems. 2008. V. 22 (2). P. 162–174 [in Russian].
  • Filippov I.V., Hudoerkov R.M., Krebs А.А., Pugachev K.S. Infraslow brain potentials of highest brain gustatory centers before and after their successive electrical stimulation // Sensory systems. 2012. V. 26 (1). P. 57-68 [in Russian].
  • Filippov I.V., Krebs А.А., Pugachev K.S., Maslyukov P.M., Zyuzin E.V. Infraslow bioelectrical activity of the human brain during exposure of different sensory stimuli // Sensory systems. 2013. V. 27 (3). P. 274–288 [in Russian].
  • Albrecht D., Royl G., Kaneoke Y. Very slow oscillatory activities in lateral geniculate neurons of freely moving and anaesthetized rats // Neurosci. Res. 1998. V. 32. P. 209–220.
  • Barone P. Is the primary visual cortex multisensory? Comment on “Crossmodal influences on visual perception” by Prof. Ladan Shams // Phys Life Rev. 2010. V. 7. No 3. P. 291–292.
  • Basura G.J., Koehler S.D., Shore S.E. Multi-sensory integration in brainstem and auditory cortex // Brain Res. 2012. V. 1485. P. 95–107.
  • Bizley J.K., Nodal F.R., Bajo V.M., Nelken I., King A.J.
  • Physiological and anatomical evidence for multisensory interactions in auditory cortex // Cereb Cortex. 2007. V. 17. No 9. P. 2172–2189.
  • Bizley J.K., King A.J. Visual-auditory spatial processing in auditory cortical neurons // Brain Res. 2008. V. 1242. P. 24–36.
  • Bonath B., Tyll S., Budinger E., Krauel K., Hopf J.M., Noesselt T. Task-demands and audio-visual stimulus configurations modulate neural activity in the human thalamus // Neuroimage. 2013. V. 66. P. 110–118.
  • Budinger E., Heil P., Hess A., Scheich H. Multisensory processing via early cortical stages: Connections of the primary auditory cortical field with other sensory systems // Neuroscience. 2006. V. 143. No 4. P. 1065– 1083.
  • Budinger E., Laszcz A., Lison H., Scheich H., Ohl F.W. Non-sensory cortical and subcortical connections of the primary auditory cortex in Mongolian gerbils: bottom-up and top-down rocessing of neuronal information via field AI // Brain Res. 2008. V. 1220. P. 2–32.
  • Campi K.L., Bales K.L., Grunewald R., Krubitzer L. Connections of auditory and visual cortex in the prairie vole (Microtus ochrogaster): evidence for multisensory processing in primary sensory areas // Cereb Cortex. 2010. V. 20. No 1. P. 89–108.
  • Collignon O., Voss P., Lassonde M. Cross-modal plasticity for the spatial processing of sounds in visually deprived subjects // Exp. Brain Res. 2009. V. 192. No 3. P. 343– 358.
  • Colonnese M., Khazipov R. Spontaneous activity in developing sensory circuits: Implications for resting state fMRI // Neuroimage. 2012. V. 62. No 4. P. 2212–2221.
  • Cuppini C., Ursino M., Magosso E., Rowland B.A., Stein B.E. An emergent model of multisensory integration in superior colliculus neurons // Front. Integr. Neurosci. 2010. V. 4. А. 6. Р. 1–15
  • Devrim M., Demiralp T., Kurt A., Yucesir I. Slow cortical potential shifts modulate the sensory threshold in human visual system // Neurosci. Lett. 1999. V. 270. No 1. P. 17–20.
  • Driver J., Noesselt T. Multisensory interplay reveals crossmodal influences on ‘sensory-specific’ brain regions, neural responses, and judgments // Neuron. 2008. V. 57. No 1. P. 11–23.
  • Filippov I.V. Power spectral analysis of very slow brain potential oscillations in primary visual cortex of freely moving rats during darkness and light // Neurocomputing. 2003. V. 52–54. P. 505–510.
  • Filippov I.V., Williams W.C., Frolov V.A. Very slow potential oscillations in locus coeruleus and dorsal raphe nucleus under different illumination in freely moving rats // Neurosci. Lett. 2004. V. 363. P. 89–93.
  • Filippov I.V., Frolov V.A. Very slow potentials in the lateral geniculate complex and primary visual cortex during different illumination changes in freely moving rats // Neurosci. Lett. 2005. V. 373. P. 51–56.
  • Filippov I.V. Very slow brain potential fluctuations (<0.5 Hz) in visual thalamus and striate cortex after their successive electrical stimulation in lightly anesthetized rats // Brain Res. 2005. V. 1066. P. 179–186.
  • Filippov I.V., Williams W.C., Krebs A.A., Pugachev K.S. Sound-induced changes of infraslow brain potential fluctuations in the medial geniculate nucleus and primary auditory cortex in anaesthetized rats // Brain Res. 2007. V. 1133. P. 78–86.
  • Filippov I.V., Williams W.C., Krebs A.A., Pugachev K.S. Dynamics of infraslow potentials in the primary auditory cortex: Component analysis and contribution of specific thalamic-cortical and non-specific brainstemcortical influences// Brain Res. 2008. V. 1219. P. 66–77.
  • Freudenburg Z.V., Gaona C.M., Sharma M., Bundy D.T., Breshears J.D., Pless R.B., Leuthardt E.C. Fast-scale network dynamics in human cortex have specific spectral covariance patterns // Proc Natl Acad Sci U S A. 2014. V. 111. No 12. P. 4602–4607.
  • Garcia-Lazaro J.A., Ahmed B., Schnupp J.W. Tuning to natural stimulus dynamics in primary auditory cortex // Curr. Biol. 2006. V. 16. P. 264–271.
  • Ghazanfar A.A., Lemus L. Multisensory integration: vision boosts information through suppression in auditory cortex // Curr Biol. 2010. V. 20. No 1. P. 22–23.
  • He J. Slow oscillations in non-lemniscal auditory thalamus // J. Neurosci. 2003. V. 23. P. 8281–8290.
  • Henschke J.U., Noesselt T., Scheich H., Budinger E. Possible anatomical pathways for short-latency multisensory integration processes in primary sensory cortices // Brain. Struct. Funct. 2015. V. 220. No 2. P. 955–977.
  • Hiltunen T., Kantola J., Abou Elseoud A., Lepola P., Suominen K., Starck T., Nikkinen J., Remes J., Tervonen O., Palva S., Kiviniemi V., Palva J.M. Infra-slow EEG fluctuations are correlated with resting-state network dynamics in fMRI // J. Neurosci. 2014. V. 34. No 2. P. 356–362.
  • Hishida R., Kudoh M., Shibuki K. Multimodal cortical sensory pathways revealed by sequential transcranial electrical stimulation in mice // Neurosci Res. 2014. V. 87. P. 49–55.
  • Kayser C., Petkov C.I., Augath M., Logothetis N.K. Functional imaging reveals visual modulation of specific fields in auditory cortex // J. Neurosci. 2007. V. 27. No 8. P. 1824–1835.
  • Kayser C., Petkov C.I., Logothetis N.K. Multisensory interactions in primate auditory cortex: fMRI and electrophysiology // Hear Res. 2009. V. 258. No 1–2. P. 80–88.
  • Kayser C., Petkov C.I., Logothetis N.K. Visual modulation of neurons in auditory cortex // Cereb Cortex. 2008. V. 18. No 7. P. 1560–1574.
  • King A.J., Walker K.M. Integrating information from different senses in the auditory cortex // Biol Cybern. 2012. V. 106. No 11–12. P. 617–625.
  • Lakatos P., Chen C.M., O’Connell M.N., Mills A., Schroeder C.E. Neuronal oscillations and multisensory interaction in primary auditory cortex // Neuron. 2007. V. 53. No 2. P. 279–292.
  • Leistner S., Sander T.H., Wuebbeler G., Link A., Elster C., Curio G., Trahms L., Mackert B.M. Magnitoencephalography discriminates modality-specific infraslow signals less than 0.1 Hz // Neuroreport. 2010. V. 21. No 3. P. 196–200.
  • Liang M., Mouraux A., Hu L., Iannetti G.D. Primary sensory cortices contain distinguishable spatial patterns of activity for each sense // Nat Commun. 2013. V. 4. А. 1979. Р. 1–10.
  • Martuzzi R., Murray M.M., Michel C.M., Thiran J.P., Maeder P.P., Clarke S., Meuli R.A. Multisensory interactions within human primary cortices revealed by BOLD dynamics // Cereb Cortex. 2007. V. 17. No 7. P. 1672–1679.
  • Mercier M.R., Foxe J.J., Fiebelkorn I.C., Butler J.S., Schwartz T.H., Molholm S. Auditory-driven phase reset in visual cortex: human electrocorticography reveals mechanisms of early multisensory integration // Neuroimage. 2013. V. 79. P. 19–29.
  • Monto S., Palva S., Voipio J., Palva J.M. Very slow EEG fluctuations predict the dynamics of stimulus detection and oscillation amplitudes in humans // J Neurosci. 2008. V. 28. No33. P. 8268–8272.
  • Naue N., Rach S., Strüber D., Huster R.J., Zaehle T., Körner U., Herrmann C.S. Auditory event-related response in visual cortex modulates subsequent visual responses in humans // J. Neurosci. 2011. V. 31. No 21. P. 7729–7736.
  • Ogawa Y. Firing properties of olfactory bulb neurons during sniffing in rats // Physiol. Behav. 1998. V. 64. P. 755–764.
  • Olcese U., Iurilli G., Medini P. Cellular and synaptic architecture of multisensory integration in the mouse neocortex // Neuron. 2013. V. 79. No 3. P. 579–593.
  • Pugachev K.S., Filippov I.V., Krebs A.A. Infraslow brain potential oscillations are implicated in multisensory mechanisms of information processing: evidence from intracortical field potential recordings // Abstract PCB117, Abstracts of International Union of Physiological Sciences IUPS 2013. P. 512.
  • Schroeder C.E., Foxe J. Multisensory contributions to low-level, ‘unisensory’ processing // Curr Opin Neurobiol. 2005. V. 15. No 4. P. 454–458.
  • Sieben K., Röder B., Hanganu-Opatz I.L. Oscillatory entrainment of primary somatosensory cortex encodes visual control of tactile processing // J. Neurosci. 2013. V. 33. No 13. P. 5736–5749.
  • Smiley J.F., Falchier A. Multisensory connections of monkey auditory cerebral cortex // Hear Res. 2009. V. 258. No 1–2. P. 37–46.
  • Stehberg J., Dang P.T., Frostig R.D. Unimodal primary sensory cortices are directly connected by longrange horizontal projections in the rat sensory cortex // Front Neuroanat. 2014. V. 8. 93. doi: 10.3389/ fnana.2014.00093. eCollection 2014.
  • Steriade M. Grouping of brain rhythms in corticothalamic systems // Neuroscience. 2006. V. 137. N. 4. P. 1087–1106.
  • Tallgren P., Vanhatalo S., Kaila K., Voipio J. Evaluation of commercially available electrodes and gels for recording of slow EEG potentials // Clin. Neurophysiol. 2005. V. 116. N. 4. P. 799–806.
  • Teich M.C., Heneghan C., Lowen S.B., Ozaki T., Kaplan E. Fractal character of the neural spike train in the visual system of the cat // J. Opt. Soc. Am. A. Opt. Image Sci. Vis. 1997. V. 14. N. 3. P. 529–546.
  • Thompson G.J., Pan W.J., Billings J.C., Grooms J.K., Shakil S., Jaeger D., Keilholz S.D. Phase-amplitude coupling and infraslow (<1 Hz) frequencies in the rat brain: relationship to resting state fMRI // Front Integr Neurosci. 2014 a. V.8. No 41. doi: 10.3389/fnint.2014.00041.
  • Thompson G.J., Pan W.J., Magnuson M.E., Jaeger D., Keilholz S.D. Quasi-periodic patterns (QPP): largescale dynamics in resting state fMRI that correlate with local infraslow electrical activity // Neuroimage. 2014б. V. 84. P. 1018–1031.
  • Thoss F., Bartsch B., Stebel J. Analysis of oscillation of the visual sensitivity // Vis. Res. 1998. V. 38. P. 139–142.
  • Tyll S., Budinger E., Noesselt T. Thalamic influences on multisensory integration // Commun Integr Biol. 2011. V. 4. No 4. P. 378–381.
  • Ursino M., Cuppini C., Magosso E. Neurocomputational approaches to modelling multisensory integration in the brain: A review // Neural Netw. 2014. V. 60. P. 141–165.
  • van den Brink R.L., Cohen M.X., van der Burg E., Talsma D., Vissers M.E., Slagter H.A. Subcortical, modality-specific pathways contribute to multisensory processing in Humans // Cereb Cortex. 2014. V. 24. No 8. P. 2169–2177.
  • Vanhatalo S., Voipio J., Kaila K. Full-band EEG (FbEEG): an emerging standard in electroencephalography // Clin. Neurophysiol. 2005. V. 116. P. 1–8.
  • Wallace M.T., Meredith M.A., Stein B.E. Integration of multiple sensory modalities in cat cortex // Exp Brain Res. 1992. V. 93. No 3. P. 484–488.
  • Wallace M.T., Ramachandran R., Stein B.E. A revised view of sensory cortical parcellation // Proc. Natl. Acad. Sci. USA. 2004. V. 101. No 7. P. 2167–2172.