Beta activity: a carrier for visual attention

• Autorzy: Wrobel A
• Języki publikacji: EN

Abstrakty

EN

The alpha (8-13 Hz), beta (15-25 Hz) and gamma (30-60 Hz) bands of the EEG have been long studied clinically because of their putative functional importance. Old experimental results indicate that repetitive stimulation of the visual pathway evokes synchronous responses at the cortical level with a gain that depends on frequency; oscillations within relevant bands are less damped at subsequent processing levels than others. Our current results show in the cat that cortico-geniculate feedback has a build-in potentiation mechanism that operates at around the beta frequency and activates thalamic cells thus lowering the threshold for visual information transmission. We have also shown that enhanced beta activity is propagated along this feedback pathway solely during attentive visual behavior. This activity consists of 300-1,000 ms bursts that correlate in time with gamma oscillatory events. Beta-bursting activity spreads to all investigated visual centers, including the lateral posterior and pulvinar complex and higher cortical areas. Other supporting data are discussed that are concerned with the enhanced beta activity during attentive-like behavior of various species, including humans. Finally, we put forward a general hypothesis which attributes the appearance of oscillations within the alpha, beta and gamma bands to different activation states of the visual system. According to this hypothesis, alpha activity characterizes idle arousal of the system, while beta bursts shift the system to an attention state that consequently allows for gamma synchronization and perception.

Słowa kluczowe

EN

cortico-thalamic loop; directed transfer function; mammal; brain; neuronal mechanism; electroencephalogram; organization; cortical activity; gain; thalamic transmission; oscillation; visual system; visual information flow; lateral geniculate nucleus; pyramidal cell; resonance frequency

• Wydawca: -
• Czasopismo: Acta Neurobiologiae Experimentalis
• Rocznik: 2000
• Tom: 60
• Numer: 2
• Opis fizyczny: p247-260,fig.

Twórcy

autor

Wrobel A

• Nencki Institute of Experimental Biology, 3 Pasteur St., 02-093 Warsaw, Poland

Bibliografia

• Adrian E.D. (1953) The physiological basis of perception. In: Brain mechanisms and consciousness (Eds. E.D. Adrian, F. Bremer and H.H. Jasper). Blackwell, Oxford, p. 237-248.
• Ahissar E., Vaadia E., Ahissar M., Bergman H., Arieli A., Abeles M. (1992) Dependence of cortical plasticity on correlated activity of single neurons and on behavioral con­text. Science 257: 412-1415.
• Ahlsen G., Lindstrom S., Lo F.S. (1985) Interaction between inhibitory pathways to principal cells in the lateral genicu­late nucleus of the cat. Exp. Brain Res. 58: 134-143.
• Arieli A., Shoham D., Hildesheim R., Grinvald A. (1995) Coherent spatiotemporal patterns of ongoing activity re­vealed by real-time optical imaging coupled with single unit recording in cat visual cortex. J. Neurosci. 73: 2072­2093.
• Basar E. (1980) EEG brain dynamics. Relation between EEG and brain evoked potentials. Elsevier, Amsterdam.
• Bekisz M., Wrobel A. (1993) 20 Hz rhythm of activity in visual system of perceiving cat. Acta Neurobiol. Exp. 53: 175-182.
• Bekisz M., Wrobel A. (1999) Coupling of beta and gamma ac­tivity in cortico-thalamic system of cats attending to visual stimuli. NeroReport 10: 3589-3594.
• Berger H. (1930) Uber das elektroenkephalogram des Men­schen: Zweite Mittelung. J. Psychol. Neurol. (Lpz), 40: 160-179. (English translation in Electroencephalogr. Clin. Neurophysiol. (Suppl.), 1969, 28: 75-93).
• Bressler S.L. (1990) The gamma wave: a cortical information carrier? TINS. 13: 161-162.
• Cardenas V.A., Gill P., Fein G. (1997) Human p50 suppress­ion is not affected by variations in wakeful alertness. Biol. Psychiatry 41: 891-901.
• Castro-Alamancos M.A., Connors B.W. (1997) Thalamocor­tical synapses. Progr. Neurobiol. 51: 581-606.
• Chalupa L.M. (1991) Visual function of the pulvinar. In: Vi­sion and visual dysfunction (Ed. A.G. Leventhal). Vol 4. The Macmillian Press, Houndmills, p. 140-159.
• Childers D.G., Perry N.W. (1970) Alpha-like activity in vi­sion. Brain Res. 25: 1-20.
• Coenen A.M., Vendrik A .J. (1972) Determination of the trans­fer ratio of cat's geniculate neurons through quasi-intracellular recordings and the relation with level of alertness. Exp. Brain Res. 14: 227-242.
• Crick F. (1994) The astonishing hypothesis. The scientific search for the soul. Charles Scribner's Sons, New York.
• Eckhorn R. Bauer R., Jordan W., Brosch M., Kruse W., Munk M., Reitboeck H.J. (1988) Coherent oscillations: a mech­anism for feature linking in the visual cortex? Biol. Cybern. 60: 121-130.
• Felleman D.J., Van Essen D.C. (1991) Distributed hierarchi­cal processing in the primate cerebral cortex. Cerebral Cor­tex 1: 1-47.
• Frien A., Eckhorn R., Bauer R. Woelbern T., Kehr H. (1994) Stimulus-specific fast oscillations at zero phase between visual areas VI and V2 of awake monkey. NeuroReport 5: 2273-2277.
• Garey L.J., Dreher B., Robinson S.R. (1991) The organization of visual thalamus. In: Vision and visual dusfunction (Ed. B. Dreher and S.R. Robinson). Vol. 3. The Macmillian Press, Houndmills, p. 176-234.
• Geisert E.E., Langsetmo A., Spear P.D. (1981) Influence of the cortico-geniculate pathway on response properties of cat lateral geniculate neurons. Brain Res. 208: 409-415.
• Giannitrapani D. Scanning mechanisms and the EEG (1971) Electroencephalogr. Clin. Neurophysiol. 30: 139-146.
• Gomez C.M., Vazquez M. Vaquero E., Lopez-Mendoza D., Cardoso M.J. (1998) Frequency analysis of the EEG during spatial selective attention. Int. J. Neurosci. 95: 17-32.
• Graille C., Rougel-Buser A. (1996) Posterior parietal electro- cortical (ECoG) "attention rhythms" in macaque during a visually guided manual task. Eur. J. Neurosci. (Suppl.) 9: 122.
• Gray C.M., Di Prisco G.V. (1997) Stimulus dependent neur­onal oscillations and local synchronization in striate cortex of the alert cat. J. Neurosci. 17: 3239-3253.
• Gray C.M., Konig P., Engel A.K., Singer W. (1989) Oscilla­tory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 338: 334-337.
• Guillery R.W. (1995) Anatomical evidence concerning the role of the thalamus in cortico-cortical communication. A brief review. J. Anat. 187: 585-592.
• Hernandez-Peon R. (1966) Physiological mechanisms in at­tention. In: Frontiers in physiological psychology (Ed. R.W. Russel). Academic Press, New York, p. 121-147
• Herculano-Houzel S., Munk M.H.J., Neunschwander S., Singer W. (1999) Precisely synchronized oscillatory firing patterns require electrophysiological activation. J. Neuro­sci. 19: 3992-4010.
• Hughes G. W., Maffei L. (1966) Retinal ganglion cell response to sinusoidal light stimulation. J. Neurophysiol. 29: 333­352.
• Kaas J.H. (1993) The organization of visual cortex in pri­mates: problems, conclusions, and the use of comparative studies in understanding the human brain. In: The func­tional organization of the human visual cortex (Eds. B. Gu- lyas, D. Ottoson and P. Roland). Pergamon Press, Oxford, p. 1-11.
• Kalil R.E., Chase R. (1970) Corticofugal influence on activity of lateral geniculate neurons in the cat. J. Neurophysiol. 33: 459- 474.
• Kaminski M.J., Blinowska K.J. (1991) A new method of the description of the information flow in the brain structures. Biol. Cybern. 65:203-210.
• Krakowska D., Waleszczyk W., Bekisz M., Wrobel A. (1995) General 20 Hz synchronization within cortico­thalamic division of the cat's visual system shifts to spe­cific pattern during visual attention. Eur. J. Neurosci. (Suppl.) 8: 38.
• Lindstrom S., Wrobel A. (1990) Frequency dependent corti­cofugal excitation of principal cells in the cat's dorsal lat­eral geniculate nucleus. Exp. Brain Res. 79: 313-318.
• Livingstone M.S., Hubel D.H. (1981) Effects of sleep and arousal on the processing of visual information in the cat. Nature (Lond.) 291: 554-561.
• Llinas R. (1994) Unpublished results, cited in: T.M. Mc Kenna, T.A. Mc Mullen, M.F. Shlesinger: The brain as a dynamic physical system. Neuroscience 60: 587-605.
• Lopes da Silva F. (1991) Neural mechanisms underlying brain waves: from neural membranes to networks. Electronence- phalogr. Clin. Neurophysiol. 79: 81-93.
• Lopes da Silva F., Van Rotterdam A., Storm van Leeuwen W., Tielen A.M. (1970a) Dynamic characteristics of visual evoked potentials in the dog. I. Cortical and subcortical potentials evoked by sine wave modulated light. Electro- nencephalogr. Clin. Neurophysiol. 29: 246-259.
• Lopes da Silva F., Van Rotterdam A., Storm van Leeuwen W., Tielen A.M. (1970b) Dynamic characteristics of visual evoked potentials in the dog. II. Beta frequency selectivity in evoked potentials and background activity. Electro- nencephalogr. Clin. Neurophysiol. 29: 260-268.
• Lutzenberger W., Pulvermuller F., Elbert T., Birbaumer N. (1995) Visual stimulation alters local 40 Hz responses in humans: an EEG-study. Neurosci. Lett. 183: 39-42.
• McCormick D.A., von Krosigk M. (1992) Corticothalamic ac­tivation modulates thalamic firing through glutamate "metabotropic" receptors. Proc. Natl. Acad. Sci. USA. 89: 2774-2778.
• Menon V., Freeman W.J., Cutillo B.A., Desmond J.E., Ward M.F. Bressler S.L., Laxer K.D., Barbaro N., Gevins A.S. (1996) Spatio-temporal correlations in human gamma band electrocorticograms. Electrencephalogr. Clin. Neurophysi­ol. 98: 89-102.
• Montagu J.D. (1966) The relationship between the intensity of repetitive photic stimulation and the cerebral response. Electronencephalogr. Clin. Neurophysiol. 23: 152-161.
• Montero V.M. (1991) A quantitative study of synaptic con­tacts on interneurons and relay cells of the cat lateral ge­niculate nucleus. Exp. Brain Res. 86: 257-270.
• Motokawa K., Ebe M. (1953) Selective stimulation of color receptors with alternating currents. Science 116: 92-94.
• Mundy-Castle A.C. (1951) Theta and beta rhythm in the elec­troencephalograms of normal adults. EEG Clin. Neurophy­siol. 3: 477-486.
• Murthy V.N., Fetz E.E. (1996) Oscillatory activity in sensori­motor cortex of awake monkeys: synchronization of local field potentials and relation to behavior. J. Neurophysiol. 76: 3949-3967.
• Musiał P., Bekisz M., Wrobel A. (1997) Spectral charac­teristics of lateral geniculate and cortical responses evoked by electrical stimulation of chiasma change with atten- tional mode in behaving cats. Proc. 2nd ENA Meeting. Strassbourg, p. 102.
• Niebur E., Koch C., Rosin C. (1993) An oscillation-based model for the neuronal basis of attention. Vision Res. 18: 2789-2802.
• Olshausen B.A., Anderson C.H., Van Essen D.C. (1993) A neurobiological model of visual attention and invariant pat­tern recognition based on dynamic routing of information. J. Neurosci. 13:4700-4719.
• Ray W.J., Cole H.W. (1985) EEG alpha activity reflects atten- tional demands, and beta activity reflects emotional and cognitive processes. Science 228: 750-752.
• Robinson D.L., Peterson S.E. (1992) The pulvinar and visual salience. TINS 15: 127-132.
• Roelfsema P.R., Engel A.K., Konig P., Singer W. (1997) Vi- suomotor integration is associated with zero time-lag syn­chronization among cortical areas. Nature 385: 157-161.
• Roskies A.L. (ed.) (1999) Reviews on the binding problem. Neuron 24: 7-110.
• Schanze T., Eckhorn R. (1997) Phase correlation of cortical rhythms at different frequencies: higher order spectral ana­lysis of multiple-microelectrode recordings from cat and monkey visual cortex. Int. J. Psychophysiol. 26: 171-189.
• Schwartz F. (1947). Uber die Reizumg des Seheorgans durch doppelphasige und gleichgerichtete elektrische Schwin­gungen. Z. Sinnesphys. 69: 158-172.
• Singer W. (1977) Control of thalamic transmission by corti- cofugal and ascending reticular pathways in the visual sys­tem. Physiol. Rev. 57: 386-420.
• Spekreijse H., van Norren D., van den Berg T.J.T.P. (1971) Flicker responses in monkey lateral geniculate nucleus and human perception of flicker. Proc. Natl. Acad. Sci. USA 68:2802-2805.
• Steriade M. (1993) Cellular substrates of brain rhythms. In: Elec­troencephalography: basic principles, clinical application and related fields (Eds. E. Niedermeyer and F. Lopes da Silva). Ill ed. Williams and Wilkins, Baltimore, p. 27-62.
• Steriade M., AmzicaF., Contreras D. (1996) Synchronization of fast (30-40 Hz) spontaneous cortical rhythms during brain activation. J. Neurosci. 16: 392-417.
• Steriade M., Gloor P., Llinas R.R., Lopes da Silva F.H., Me- sulam M.M. (1990) Basic mechanisms of cerebral rhyth­mic activities. Electroencephalogr. Clin. Neurophysiol. 76: 481-508.
• Tallon-Baudry C., Bertrand O. (1999) Oscillatory gamma ac­tivity in humans and its role in object representation. TICS 3: 1-18.
• Takigawa M., Kidiyoor R.G. (1991) Analysis of high fre­quency and in human EEG by differentiation and directed coherence. Neurosciences 17: 289-295.
• Thatcher R.W., Krause P.J., Hrybak M. (1986) Cortico-corti- cal associations and EEG coherence: a two-compartmental model. Electroencephalogr. Clin. Neurophysiol. 64: 123­143.
• Treisman A., Gelade G. (1980) A feature-integration theory of attention. Cogn. Psychol. 12: 97-136.
• Utlett G.A., Johnson L.C. (1958) Pattern, stability and corre­lates of photic-electraencephalographic activation. J. Nerv. Ment. Dis. 126: 153-168.
• Vanni S., Revonsuo A., Hari R. (1997) Modulation of the pa- rieto-occipital alpha rhythm during object detection. J. Neurosci. 17:7141-7147.
• von Stein A., Rappelsberger P., Filz O., Petsche H. (1993) EEG-Korrelate bildlicher Vorstellung; eine Amplituden- und Koharenzuntersuchung. Z. EEG-EMG 24: 217-224.
• Whittington M.A., Traub R.D., Faulkner H.J., Stanford I.M., Jefferys G.R. (1997) Recurrent excitatory postsynaptic potentials induced by synchronized fast cortical oscilla­tions. Proc. Natl. Acad. Sci. USA 94: 12198-12203.
• Wilson J.R., Friedlander M.J., Sherman S.M. (1984) Fine structural morphology of identified X- and Y-cells in the cat's lateral geniculate nucleus. Proc. R. Soc. Lond. B 221: 411-436.
• Wróbel A. (1997a) Attention related oscillatory activity with­in sensory systems. Acta Neurobiol. Exp. 57: 38.
• Wróbel A. (1997b) In search for integrative mechanisms of the brain activity (in Polish). In: Mózg a zachowanie (Eds.T. Górska, A. Grabowska and J. Zagrodzka). PWN, Warszawa, p. 460-486.
• Wróbel A. (1998) Beta frequency burst - elementary event of attention span. In: Time and timing in neural systems. Abstr. Satellite Symp. FENS in Strzękocino. p. 42-44.
• Wróbel A., Bekisz M., Kublik E., Waleszczyk W. (1994a) 20 Hz bursting beta activity in cortico-thalamic system of visually attending cats. Acta Neurobiol. Exp. 54: 95-107.
• Wróbel A., Bekisz, M., Waleszczyk W. (1994b) 20 Hz bursts of activity in the cortico-thalamic pathway during attentive perception. In: Oscillatory event related brain dynamics (Eds. C. Pantev, Th. Elbert and B. Lutken- honer). Vol. 271. Plenum Press, London. NATO A/Life Sciences.
• Wróbel A., Hedstrom A., Lindstróm S. (1998) Synaptic ex­citation of principal cells in the cat's lateral geniculate nucleus during focal epileptic seizures in the visual cor­tex. Acta Neurobiol. Exp. 58: 271-276.
• Zeki S. (1993) A vision of the brain. Blackwell Scientific Pub­lications, Oxford, 366 p.