• 1987 (Vol.1)

Influences of neuromodulatory centers on infraslow brain potential oscillations of primary cortical areas of sensory systems of the brain

© 2015 A .A. Krebs, I. V. Filippov, K. S. Pugachev, E. V. Zyuzin, P. M. Maslyukov

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

Received 16 Jan 2014

The aim of this work was to study influences of neuromodulatory centers (e.g., locus coeruleus, dorsal raphe nucleus, and basal magnocellular nucleus) on the dynamics of infraslow brain potential oscillations (ISO) in the primary visual, auditory and gustatory cortices of anesthetized rats in semi-chronic experiments. We used 60 rats (n = 180 experimental sessions) with chronic electrodes implanted to aforementioned sites of the brain. Recordings were done by means of multichannel universal AC/DC amplifier and analog-to-digital converter. It was shown that contact electrical stimulation of locus coeruleus, dorsal raphe nucleus, and basal magnocellular nucleus induced complex alterations of ISO and functional states of primary visual, auditory and gustatory cortical areas. These were manifested as statistically significant alterations of spectral patterns of oscillations in the domain of seconds (0.1–0.3 Hz) and multisecond waves (0.0167–0.05 Hz) in all primary sensory cortical sites of the brain (e.g., visual, auditory, gustatory cortices). Obtained data allow the conclusion about participation of locus coeruleus, dorsal raphe nucleus and basal magnocellular nucleus in the modulation of ongoing infraslow brain potential oscillations of primary sensory cortical areas of the brain. This may explain the contribution of these nuclei in neural processing of sensory information, taking into account the role if brain infraslow activity in such processes that was documented by us earlier.

Key words: infraslow brain potential oscillations, primary visual cortex, primary auditory cortex, gustatory cortex, locus coeruleus, dorsal raphe nucleus, basal magnocellular nucleus

Cite: Krebs A. A., Filippov I. V., Pugachev K. S., Zyuzin E. V., Maslyukov P. M. Vliyaniya neiromodulyatornykh tsentrov na sverkhmedlennuyu bioelektricheskuyu aktivnost pervichnykh korkovykh otdelov sensornykh sistem golovnogo mozga [Influences of neuromodulatory centers on infraslow brain potential oscillations of primary cortical areas of sensory systems of the brain]. Sensornye sistemy [Sensory systems]. 2015. V. 29(2). P. 163-178 (in Russian).

References:

  • Аладжалова Н.А. Медленные электрические процессы в головном мозге. М.: 1962. 240 с.
  • Аладжалова Н.А. Психофизиологические аспекты сверхмедленной ритмической активности головного мозга. М.: Наука, 1979. 214 с.
  • Бехтерева Н.П. Здоровый и больной мозг человека. Л.: Наука, 1988. 260 с.
  • Бехтерева Н.П. Нейрофизиологические аспекты психической деятельности человека. Л.: Медицина, 1971. 119 с.
  • Илюхина В.А. Нейрофизиология функциональных состояний человека. Л.: Наука, 1986. 173 с.
  • Илюхина В.А. Мозг человека в механизмах информационно-управляющих взаимодействий организма и среды обитания. СПб.: Ин-т мозга человека РАН, 2004. 321 с.
  • Кратин Ю.Г. Неспецифические системы головного мозга. Л.: Наука, 1987. 159 с.
  • Филиппов И.В., Кребс А.А., Пугачев К.С. Сверхмедленная биоэлектрическая активность структур слуховой системы головного мозга // Сенсорные системы. 2006 а. Т. 20. No 3. С. 238–244.
  • Филиппов И.В., Кребс А.А., Пугачев К.С. Сверхмедленная биоэлектрическая активность медиального коленчатого тела и первичной слуховой коры после их последовательной электростимуляции // Сенсорные системы. 2006 б. Т. 20. No 3. С. 245–252.
  • Филиппов И.В. Сверхмедленные колебания потенциалов латерального коленчатого тела и первичной зрительной коры как корреляты процессов переработки зрительной информации // Сенсорные системы. 2007 а. Т. 21. No 3. С. 165–173.
  • Филиппов И.В. Перестройки сверхмедленных колебаний потенциалов в латеральном коленчатом теле и в первичной зрительной коре после их соответствующей последовательной электростимуляции // Сенсорные системы. 2007 б. Т. 21. No 4. С. 339–348.
  • Филиппов И.В., Кребс А.А., Пугачев К.С. Модулирующие влияния стволовых ядер на сверхмедленную биоэлектрическую активность первичной слуховой коры головного мозга // Сенсорные системы. 2007 в. Т. 21. No 3. С. 237–245.
  • Филиппов И.В., Кребс А.А., Пугачев К.С. Сверхмедленные колебания потенциалов центральных представительств вкусовой системы головного мозга крыс при действии различных вкусовых стимулов // Сенсорные системы. 2008. Т. 22. No 2. С. 162–174.
  • Филиппов И.В., Кребс А.А., Пугачев К.С., Худоерков Р.М., Маслюков П.М., Коротаева М.С., Варенцов В.Е., Емельянов Д.М. Таламокортикальные и кортикоталамические взаимодействия с участием сверхмедленных биоэлектрических процессов ЦНС // Уч. зап. СПБ. гос. мед. ун-та (СПбГМУ). 2011. Т. 17. No 2. С. 72–73.
  • Филиппов И.В., Худоерков Р.М., Кребс А.А., Пугачев К.С. Сверхмедленные колебания потенциалов высших отделов вкусовой системы головного мозга до и после их последовательной электростимуляции // Сенсорные системы. 2012. Т. 26. No 1. С. 57–68.
  • Филиппов И.В., Кребс А.А., Пугачев К.С., Маслюков П.М., Зюзин Е.В. Сверхмедленная биоэлектрическая активность головного мозга человека при действии различных сенсорных стимулов // Сенсорные системы. 2013. Т. 27. No 3. С. 274–288.
  • Adams R.W., Lambert G.A., Lance J.W. Brain-stem facilitation of electrically evoked visual cortical response in the cat. Source, pathway and role of nicotinic receptors // Electroencephalogr Clin Neurophysiol. 1988. V. 69. No 1. P. 45–54.
  • Berridge C.W., Foote S.L. Enhancement of behavioral and electroencephalographic indices of waking following stimulation of noradrenergic beta-receptors within the medial septal region of the basal forebrain // J. Neurosci. 1996. V. 16. No 21. P. 6999–7009.
  • Blasiak T., Zawadzki A., Lewandowski M.H. Infra-slow oscillations (ISO) of the pupil size of urethane-anaesthetized rats // PLOS One. 2013. V. 8. I. 1. e62430.
  • 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: bottomup and top-down processing of neuronal information via field AI // Brain Res. 2008. V. 1220. P. 2–32.
  • Collier T.J., Greene J.G., Felten D.L., Stevens S.Y., Collier K.S. Reduced cortical noradrenergic neurotransmission is associated with increased neophobia and impaired spatial memory in aged rats // Neurobiol Aging. 2004. V. 25. No 2. P. 209–221.
  • Dafilis M.P., Frascoli F., Cadusch P.J., Liley D.T. Four dimensional chaos and intermittency in a mesoscopic model of the electroencephalogram // Chaos. 2013 V. 23. No 2. Р. 023111.
  • Detari L., Semba K., Rasmusson D.D. Responses of cortical EEG-related basal forebrain neurons to brainstem and sensory stimulation inurethane-anaesthetized rats // J. Neurosci. 1997. V. 9. No 6. P. 1153–1161.
  • Edeline J.M., Manunta Y., Hennevin E. Induction of selective plasticity in the frequency tuning of auditory cortex and auditory thalamus neurons by locus coeruleus stimulation // Hear Res. 2011. V. 274. No 1–2. P. 75–84.
  • Ego-Stengel V., Bringuier V., Shulz D.E. Noradrenergic modulation of functional selectivity in the cat visual cortex: an in vivo extracellular and intracellular study // Neuroscience. 2002. V. 111. No 2. P. 275–289.
  • Everitt B.J., Robbins T.W., Gaskin M., Fray P.J. The effects of lesions to ascending noradrenergic neurons on discrimination learning and performance in the rat // Neuroscience. 1983. V. 10. No 2. P. 397–410.
  • Filippov I.V., Williams W.C., Gladyshev A.V. Role of infraslow (0–0.5 Hz) potential oscillations in the regulation of brain stress response by the locus coeruleus system // Neurocomputing. 2002. V. 44–46. P. 795–798.
  • 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., 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.
  • Freeman W. J. Random activity at the microscopic neural level in cortex (“noise”) sustains and is regulated by low-dimensional dynamics of macroscopic cortical activity (“chaos”) // Int. J. Neural Syst. 1996. V. 7. No 4. Р. 473–480.
  • Freeman W. J. Mesoscopic neurodynamics: from neuron to brain // J. Physiol. 2000. V. 94. No 5–6. Р. 303–322.
  • Goard M., Dan Y. Basal forebrain activation enhances cortical coding of natural scenes // Nat. Neurosci. 2009. V. 12. No 11. P. 1444–1449.
  • Hansel D. Synchronized chaos in local cortical circuits // Int. J. Neural Syst. 1996. V. 7. No 4. Р. 403–415.
  • 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. P. 356–362.
  • Howard M.A., Simons D.J. Physiologic effects of nucleus basalis magnocellularis stimulation on rat barrel cort ex neurons // Exp. Brain Res. 1994. V. 102. No 1. P. 21–33.
  • Huang Y.A., Pereira E., Roper S.D. Acid stimulation (sour taste) elicits GABA and serotonin release from mouse taste cells // PloS One. 2011. V. 6. No 10. e25471.
  • Kaya N., Shen T., Lu S.G., Zhao F.L., Herness S. A paracrine signaling role for serotonin in rat taste buds: expression and localization of serotonin receptor subtypes // Am. J. Physiol. Regul. Integr. Comp. Physiol. 2004. V. 286. No 4. P. 649–658.
  • Kayama Y., Shimada S., Hishikawa Y., Ogawa T. Effects of stimulating the dorsal raphe nucleus of the rat on neuronal activity in the dorsal lateral geniculate nucleus // Brain Res. 1989. V. 489. No 1. P. 1–11.
  • Kisley M.A., Gerstein G.L. Trial-to-trial variability and state-dependent modulation of auditory-evoked responses in cortex // J. Neurosci. 1999. V. 19. No 23. P. 10451–10460.
  • Lee J., Kim H.R., Lee C. Trial-to-trial variability of spike response of V1 and saccadic response time // J. Neurophysiol. 2010. V. 104. No 5. P. 2556–2572.
  • Leopold D.A., Murayama Y., Logothetis N. Very slow activity fluctuations in monkey visual cortex: implications for functional imaging // Cereb. Cortex. 2003. V. 13. P. 422–433.
  • Lopez-Garcia J.C., Fernandez-Ruiz J., Escobar M.L., Bermudez-Rattoni F., Tapia R. Effects of excitotoxic lesions of the nucleus basalis magnocellularis on conditioned taste aversion and inhibitory avoidance in the rat // Pharmacol. Biochem. Behav. 1993. V. 45. No 1. P. 147–152.
  • McLean J., Waterhouse B.D. Noradrenergic modulation of cat area 17 neuronal responses to moving visual stimuli // Brain Res. 1994. V. 667. No 1. P. 83–97.
  • Metherate R., Cox C.L., Ashe J.H. Cellular bases of neocortical activation: modulation of neural oscillations by the nucleus basalisand endogenous acetylcholine // J. Neurosci. 1992. V. 12. No 12. P. 4701–4711.
  • Miranda M.I., Bermudez-Rattoni F. Reversible inactivation of the nucleus basalis magnocellularis induces disruption of cortical acetylcholine release and acquisition, but not retrieval, of aversive memories // Proc. Natl. Acad. Sci. U S A. 1999. V. 96. No 11. P. 6478–6482.
  • Miranda M.I., Ferreira G., Ramírez-Lugo L., BermudezRattoni F. Role of cholinergic system on the construction of memories: taste memory encoding // Neurobiol. Learn Mem. 2003. V. 80. No 3. P. 211–222.
  • Moyanova S., Dimov S. Modulation of visual excitability cycles in some brain structures by high-frequency stimulation of raphe dorsal nucleus in cats // Acta. Physiol. Pharmacol. Bulg. 1986. V. 12. No 1. P. 17–25.
  • Muir J.L., Page K.J., Sirinathsinghji D.J., Robbins T.W., Everitt B.J. Excitotoxic lesions of basal forebrain cholinergic neurons: effects on learning, memory and attention // Behav. Brain Res. 1993. V. 57. No 2. P. 123– 131.
  • Muir J.L., Everitt B.J., Robbins T.W. AMPA-induced excitotoxic lesions of the basal forebrain: a significant role for the cortical cholinergic system in attentional function // J. Neurosci. 1994. V. 14. No 4. P. 2313–2326.
  • Nakamura K., Yamamoto M., Takahashi K., Nakao M., Mizutani Y., Katayama N., Kodama T. State-dependency of neuronal slow dynamics during sleep observed in cat lateral geniculate nucleus // Sleep Res. Online. 2000. V. 3. P. 147–157.
  • Nowak L.G., Sanchez-Vives M.V., McCormick D.A. Influence of low and high frequency inputs on spike timing in visual cortical neurons // Cereb. Cortex. 1997. V. 7. No 6. P. 487–501.
  • Novak P., Lepicovska V. Slow modulation of EEG // Neuroreport. 1992. V. 3. P. 189–192.
  • Olpe H.R., Glatt A., Laszlo J., Schellenberg A. Some electrophysiological and pharmacological properties of the cortical, noradrenergic projection of the locus coeruleus in the rat // Brain Res. 1980. V. 186. No 1. P. 9–19.
  • Pan Wen-Ju, Thompson G.J., Magnuson M.E., Jaeger D., Keilholz S. Infraslow LFP correlates to resting-state fMRI BOLD signal // NeuroImage. 2013. 74. P. 288– 297.
  • Robbins T.W., Everitt B.J., Ryan C.N., Marston H.M., Jones G.H., Page K.J. Comparative effects of quisqualic and ibotenic acid-induced lesions of the substantia innominata and globus pallidus on the acquisition of a conditional visual discrimination: differential effects on cholinergic mechanisms // Neuroscience. 1989. V. 28. No 2. P. 337–352.
  • Salgado H., Garcia-Oscos F., Martinolich L., Hall S., Restom R., Tseng K.Y., Atzori M. Preand postsynaptic effects of norepinephrine on γ-aminobutyric acid-mediated synaptic transmission in layer 2/3 of the rat auditory cortex // Synapse. 2012. V. 66. No 1. P. 20–28.
  • Santiago A.C., Shammah-Lagnado S.J. Afferent connections of the amygdalopiriform transition area in the rat // J. Comp. Neurol. 2005. V. 489. No 3. P. 349–371.
  • Steele G.E., Weller R.E. Subcortical connections of subdivisions of inferior temporal cortex in squirrel monkeys // Vis. Neurosci. 1993. V. 10. No 3. P. 563–583.
  • Scaglione A., Moxon K.A., Aguilar J., Foffani G. Trialto-trial variability in the responses of neurons carries information about stimulus location in the rat whisker thalamus // Proc. Natl. Acad. Sci. U S A. 2011. V. 108. No 36. P. 14956–14961.
  • Steriade M., Amzica F., Nunez A. Cholinergic and noradrenergic modulation of the slow (approximately 0.3 Hz) oscillation in neocortical cells // J. Neurophysiol. 1993. V. 70. No 4. P. 1385–1400.
  • Swanson L.W. Brain Maps: Structure of the Rat Brain. Amsterdam. Elsevier, 1998. 267 р.
  • Tan A.Y., Chen Y., Scholl B., Seidemann E., Priebe N.J. Sensory stimulation shifts visual cortex from synchronous to asynchronous states // Nature. 2014. V. 509. No 7499. P. 226–229.
  • Thompson G.J., Merritt M.D., Pan Wen-Ju, Magnuson M.E., Grooms J.K., Jaeger D., Keilholz S.D. Neural correlates of time-varying functional connectivity in the rat // NeuroImage. 2013. 83. P. 826–836.
  • Thompson G.J., Pan Wen-Ju, Magnuson M.E., Jaeger D., Keilholz S.D. Quasi-periodic patterns (QPP): Largescale dynamics in resting state fMRI that correlate with local infraslow activity //NeuroImage. 2014. V. 84. P. 1018–1031.
  • Tremere L.A. Noradrenergic Modulation of Light-Driven Egr-1 Expression in the Adult Visual Cortex // J. Exp. Neurosci. 2011. V. 5. P. 13–19.
  • VanhataloS.,VoipioJ.,KailaK.Full-bandEEG(FbEEG): an emerging standard in electroencephalography // Clin. Neurophysiol. 2005. V. 116. P. 1–8.
  • Xiang Z., Prince D.A. Heterogeneous actions of serotonin on interneurons in rat visual cortex // J. Neurophysiol. 2003. V. 89. No 3. P. 1278–1287.
  • Zaborszky L., Hoemke L., Mohlberg H., Schleicher A., Amunts K., Zilles K. Stereotaxic probabilistic maps of the magnocellular cell groups in human basal forebrain // Neuroimage. 2008. V. 42. No 3. P. 1127–1241.