Abstract
We conducted a cued spatial attention experiment to investigate the time–frequency structure of human EEG induced by attentional orientation of an observer in external auditory space. Seven subjects participated in a task in which attention was cued to one of two spatial locations at left and right. Subjects were instructed to report the speech stimulus at the cued location and to ignore a simultaneous speech stream originating from the uncued location. EEG was recorded from the onset of the directional cue through the offset of the inter-stimulus interval (ISI), during which attention was directed toward the cued location. Using a wavelet spectrum, each frequency band was then normalized by the mean level of power observed in the early part of the cue interval to obtain a measure of induced power related to the deployment of attention. Topographies of band specific induced power during the cue and inter-stimulus intervals showed peaks over symmetric bilateral scalp areas. We used a bootstrap analysis of a lateralization measure defined for symmetric groups of channels in each band to identify specific lateralization events throughout the ISI. Our results suggest that the deployment and maintenance of spatially oriented attention throughout a period of 1,100 ms is marked by distinct episodes of reliable hemispheric lateralization ipsilateral to the direction in which attention is oriented. An early theta lateralization was evident over posterior parietal electrodes and was sustained throughout the ISI. In the alpha and mu bands punctuated episodes of parietal power lateralization were observed roughly 500 ms after attentional deployment, consistent with previous studies of visual attention. In the beta band these episodes show similar patterns of lateralization over frontal motor areas. These results indicate that spatial attention involves similar mechanisms in the auditory and visual modalities.
Similar content being viewed by others
References
Alho K, Connolly JF, Cheour M, Lehtokoski A, Huotilainen M, Virtanen J, Aulanko R, Ilmoniemi RJ (1998) Hemispheric lateralization in preattentive processing of speech sounds. Neurosci Lett 258:9–12
Arrington CM, Carr TH, Mayer AR, Rao SM (2000) Neural mechanisms of visual attention: object-based selection of a region in space. J Cogn Neurosci 12(Supplement 2):106–117
Bahramisharif A, van Gerven M, Heskes T, Jensen O (2010) Covert attention allows for continuous control of brain-computer interfaces. Eur J Neurosci 31(8):1501–1508
Bauer M, Oostenveld R, Peeters M, Fries P (2006) Tactile spatial attention enhances gamma-band activity in somatosensory cortex and reduces low-frequency activity in parieto-occipital areas. J Neurosci 26(2):490–501
Blauert J (2001) Spatial hearing. The psychophysics of human sound localization, Rev. Ed edn. MIT, Cambridge
Buser P, Rougeul-Buser A (2005) Visual attention in behaving cats: attention shifts and sustained attention episodes are accompanied by distinct electrocortical activities. Behav Brain Res 164(1):42–51
Canolty RT, Edwards E, Dalal SS, Soltani M, Nagarjan SS, Kirsch HE, Berger MS, Barbaro NM, Knight RT (2006) High gamma power is phase-locked to theta oscillations in human neocortex. Science 313:1626–1628
Corbetta M, Shulman GL (2002) Control of goal- and stimulus-driven attention in the brain. Nat Rev Neurosci 31:201–215
Corbetta M, Akbudak E, Conturo TE, Synder AZ, Ollinger JM, Drury HA, Linenweber HR, Petersen SE, Raichle ME, Van Essen DC, Shulman GL (1998) A common network of functional areas for attention and eye movements. Neuron 21(4):761–773
Corbetta M, Kinkade JM, Ollinger JM, McAvoy MP, Shulman GL (2000) Voluntary orienting is dissociated from target detection in human posterior parietal cortex. Nat Neurosci 3(3):292–297
Desimone R, Duncan J (1995) Neural mechanisms of selective visual attention. Annu Rev Neurosci 18:193–222
Doesburg SM, Roggeveen AB, Kitajo K, Ward LM (2008) Large scale gamma band phase synchronization and selective attention. Cereb Cortex 18:386–396
Efron B, Tibshirani R (1993) An introduction to the bootstrap. Chapman & Hall/CRC, Boca Raton
Egeth HE, Yantis S (1997) Visual attention: control, representation, and time course. Annu Rev Psychol 48:269–297
Engel AK, Fries P, Singer W (2001) Dynamic predictions: oscillations and synchrony in top-down processing. Nat Rev Neurosci 2(10):704–716
Fabiani GE, McFarland DJ, Wolpaw JR, Pfurtscheller G (2004) Conversion of EEG activity into cursor movement by a brain-computer interface (BCI). IEEE Trans Neural Syst Rehabil Eng 12(3):331–338
Fink GR, Halligan PW, Marshall JC, Firth CD, Frackowiak RSJ, Dolan RJ (1996) Where in the brain does visual attention select the forest and the trees? Nature 382:626–628
Fox MD, Corbetta M, Snyder AZ, Vincent JL, Raichle ME (2006) Spontaneous neuronal activity distinguishes human dorsal and ventral attention systems. Proc Natl Acad Sci USA 103(26):10046–10051
Foxe J, Simpson G, Ahlfors S (1998) Parieto-occipital ~10 Hz activity reflects anticipatory state of visual attention mechanisms. NeuroReport 9:3929–3933
Fries P, Reynolds JH, Rorie AE, Desimone R (2001) Modulation of oscillatory neuronal synchronization by selective visual attention. Science 291(5508):1560–1563
Fu K, Foxe J, Murray M, Higgins B, Javitt D, Schroeder C (2001) Attention-dependent suppression of distracter visual input can be cross-modally cued as indexed by anticipatory parieto-occipital alpha-band oscillations. Cogn Brain Res 12:145–152
Gitelman D, Nobre A, Parrish T, LaBar K, Kim Y, Meyer M, Mesulam M (1999) A large-scale distributed network for covert spatial attention. Further anatomical delineation based on stringent behavioral and cognitive controls. Brain 122(6):1093–1106
Hillyard SA, Anllo-Vento L (1998) Event-related brain potentials in the study of visual selective attention. Proc Natl Acad Sci USA 95:781–787
Hopfinger JB, Buonocore MH, Mangun GR (2000) The neural mechanisms of top-down attentional control. Nat Neurosci 3(3):284–291
Kastner S, Ungerleider LG (2000) Mechanisms of visual attention in the human cortex. Annu Rev Neurosci 23:315–341
Kastner S, Pinsk M, De Weerd P, Desimone R, Ungerleider L (1999) Increased activity in human visual cortex during directed attention in the absence of visual stimulation. Neuron 22:751–761
Krumbholz K, Nobis EA, Weatheritt RJ, Fink GR (2009) Executive control of spatial attention shifts in the auditory as opposed to the visual modality. Hum Brain Mapp 30:1457–1469
Kwak H, DagenBach D, Egeth H (1991) Further evidence for a time-independent shift of the focus of attention. Percept Psychophys 49(5):473–480
Martinez A, Moses P, Frank L, Buxton R, Wong E, Stiles J (1997) Hemispheric asymmetries in global and local processing: evidence from fMRI. NeuroReport 8:1685–1689
Mesulam MM (1981) A cortical network for directed attention and unilateral neglect. Ann Neurol 10(4):309–325
Moore TJ (1981) Voice communication jamming research. AGARD conference proceedings 331: Aural Commun Aviat 2:1–6
Moore T, Armstrong KM, Fallah M (2003) Visuomotor origins of covert spatial attention. Neuron 40:671–683
Müller HJ, Rabbitt PM (1989) Reflexive and voluntary orienting of visual attention: time course of activation and resistance to interruption. J Exp Psychol Hum Percept Perform 15(2):315–330
Nakayama K, Mackeben M (1989) Sustained and transient components of focal visual attention. Vis Res 29(11):1631–1647
Nunez PL, Srinivasan R (2006) Electric fields of the brain: the neurophysics of EEG, 2nd edn. Oxford University Press, New York
Nunez PL, Srinivasan R (2010) Scale and frequency chauvinism in brain dynamics: too much emphasis on gamma band oscillations. Brain Struct Funct 215:67–71
Pardo JV, Fox PT, Raichle ME (1991) Localization of a human system for sustained attention by positron emission tomography. Nature 349:61–64
Pfurtscheller G, Brunner C, Schlogl A, Lopes da Silva FH (2006) Mu rhythm (de) synchronization and EEG single-trial classification of different motor imagery tasks. NeuroImage 31(1):153–159
Pineda JA (2005) The functional significance of mu rhythms: translating. Brain Res Rev 50(1):57–68
Poeppel D (2003) The analysis of speech in different temporal integration windows: cerebral lateralization as ‘asymmetric sampling in time’. Speech Commun 41:245–255
Posner M, Petersen S (1990) The attention system of the human brain. Annu Rev Neurosci 13:25–42
Reeves A, Sperling G (1986) Attention gating in short-term visual memory. Psychol Rev 93(2):180–206
Rihs TA, Michel CM, Thut G (2007) Mechanisms of selective inhibition in visual spatial attention are indexed by α–band EEG synchronization. Eur J Neurosci 23:603–610
Rougeul-Buser A, Buser P (1997) Rhythms in the alpha band in cats and their behavioural correlates. Int J Psychophysiol 26(1–3):191–203
Sagi D, Julez B (1985) Fast noninertial shifts of attention. Spat Vis 1(2):141–149
Salmi J, Rinne T, Koistinen S, Salonen O, Alho K (2009) Brain networks of bottom-up triggered and top-down controlled shifting of auditory attention. Brain Res 1286:155–164
Sauseng P, Klimesch W, Gruber WR, Birbaumer N (2008) Cross frequency phase synchronization: a brain mechanism of memory matching and attention. NeuroImage 40:308–317
Schack B, Vath N, Petsche H, Geissler HG, Moller E (2002) Phase-coupling of theta-gamma EEG rhythms during short-term memory processing. Int J Psychophysiol 44:143–163
Sheliga BM, Riggio L, Rizzolatti G (1994) Orienting of attention and eye movements. Exp Brain Res 98:507–522
Smith DV, Davis B, Niu K, Healy EW, Bonilha L, Fridriksson J, Morgan PS, Rorden C (2009) Spatial attention evokes similar activation patterns for visual and auditory stimuli. J Cogn Neurosci 22(2):347–361
Spence C, Driver J (1998) Crossmodal attention. Curr Opin Neurobiol 8:245–253
Spence C, Pavani F, Driver J (2000) Crossmodal links between vision and touch in covert endogeneous spatial attention. J Exp Psychol Hum Percept Peform 26:1298–1319
Srinivasan R, Thorpe S, Deng S, Lappas T, Dzmura M (2009) Decoding attentional orientation from EEG spectra. Hum Comput Interact New Trends 5610:176–183
Thorpe S, Srinivasan R, Deng S, Lappas T, D’Zmura M (2009) Decoding attentional orientation from EEG spectra. Poster presented at the annual meeting of the Society for Neuroscience, Chicago
Thut G, Nietzel A, Brandt SA, Pascual-Leone A (2006) Alpha-band electroencephalographic activity over occipital cortex indexes visuospatial attention bias and predicts visual target detection. J Neurosci 26(37):9494–9950
Tiitinen HT, Sinkkonen J, Reinikainen K, Alho H, Lavikainen J, Naatanen B (1993) Selective attention enhances the auditory 40-Hz transient response in humans. Nature 364(6432):59–60
van Gerven M, Jensen O (2009) Attention modulations of posterior alpha as a control signal for two-dimensional brain-computer interfaces. J Neurosci Methods 179(1):78–84
Wang Y, Makeig S (2009) Predicting intended movement direction using EEG from human posterior parietal cortex. Found Augment Cogn Neuroergon Oper Neurosci 5638:437–446
Weichselgartner E, Sperling G (1987) Dynamics of automatic and controlled visual attention. Science 238:778–780
Wolpaw JR, McFarland DJ (2004) Control of a two-dimensional movement signal by a noninvasive brain-computer interface in humans. Proc Natl Acad Sci USA 101(51):17849–17854
Wolpaw JR, McFarland DJ, Vaughan TM, Schalk G (2003) The Wadsworth Center brain-computer interface (BCI) research and development program. IEEE Trans Neural Syst Rehabil Eng 11(2):204–207
Worden M, Foxe J, Wang N, Simpson G (2000) Anticipatory biasing of visuospatial attention indexed by retinotopically specific alpha band electroencephalography increases over occipital cortex. J Neurosci 20(63):1–6
Wu CT, Weissman DH, Roberts KC, Woldorff MG (2007) The neural circuitry underlying the executive control of auditory spatial attention. Brain Res 1134:187–198
Acknowledgments
We thank Tom Lappas, Siyi Deng, Cort Horton, and Bill Winter for their contributions to this work. This work was supported by ARO 54228-LS-MUR, and R01-MH68004.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Thorpe, S., D’Zmura, M. & Srinivasan, R. Lateralization of Frequency-Specific Networks for Covert Spatial Attention to Auditory Stimuli. Brain Topogr 25, 39–54 (2012). https://doi.org/10.1007/s10548-011-0186-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10548-011-0186-x