Top

Published in:

01-09-2007 | Original Article

Orienting and maintenance of spatial attention in audition and vision: multimodal and modality-specific brain activations

Authors: Juha Salmi, Teemu Rinne, Alexander Degerman, Oili Salonen, Kimmo Alho

Published in: Brain Structure and Function | Issue 2/2007

Abstract

We studied orienting and maintenance of spatial attention in audition and vision. Functional magnetic resonance imaging (fMRI) in nine healthy subjects revealed activations in the same superior and inferior parietal, and posterior prefrontal areas in the auditory and visual orienting tasks when these tasks were compared with the corresponding maintenance tasks. Attention-related activations in the thalamus and cerebellum were observed during the auditory orienting and maintenance tasks and during the visual orienting task. In addition to the supratemporal auditory cortices, auditory orienting, and maintenance produced stronger activity than the respective visual tasks in the inferior parietal and prefrontal cortices, whereas only the occipital visual cortex and the superior parietal cortex showed stronger activity during the visual tasks than during the auditory tasks. Differences between the brain networks involved in auditory and visual spatial attention could be, for example, due to different encoding of auditory and visual spatial information or differences in stimulus-driven (bottom-up triggered) and voluntary (top-down controlled) attention between the auditory and visual modalities, or both.

Akshoomoff NA, Courchesne E, Townsend J (1997) Attention coordination and anticipatory control. Int Rev Neurobiol 41:575–598PubMed

Alho K, Medvedev SV, Pakhomov SV, Roudas MS, Tervaniemi M, Reinikainen K, Zeffiro T, Näätänen R (1999) Selective tuning of the left and right auditory cortices during spatially directed attention. Cogn Brain Res 7:335–341CrossRef

Alho K, Woods DL, Algazi A (1994) Processing of auditory stimuli during auditory and visual attention as revealed by event-related potentials. Psychophysiology 31:469–479PubMedCrossRef

Allen G, Buxton RB, Wong EC, Courchesne E (1997) Attentional activation of the cerebellum independent of motor involvement. Science 275:1940–1943PubMedCrossRef

Allen GI, Gilbert PF, Yin TC (1978) Convergence of cerebral inputs onto dentate neurons in monkey. Exp Brain Res 32:151–170PubMedCrossRef

Aron AR, Robbins TW, Poldrack RA (2004) Inhibition and the right inferior frontal cortex. Trends Cogn Sci 8:170–177PubMedCrossRef

Beckmann CF, Jenkinson M, Smith SM (2003) General multilevel linear modeling for group analysis in FMRI. Neuroimage 20:1052–1063PubMedCrossRef

Bos J, Benevento LA (1975) Projections of the medial pulvinar to orbital cortex and frontal eye fields in the rhesus monkey (Macaca mulatta). Exp Neurol 49:487–496PubMedCrossRef

Brodal P (1978) The corticopontine projection in the rhesus monkey. Origin and principles of organization. Brain 101:251–283PubMedCrossRef

Brugge JF, Reale RA, Jenison RL, Schnupp J (2001) Auditory cortical spatial receptive fields. Audiol Neurootol 6:173–177PubMedCrossRef

Corbetta M, Miezin FM, Shulman GE, Petersen SE (1993) A PET study of visuospatial attention. J Neurosci 13:1202–1226PubMed

Corbetta M, Kincade JM, Ollinger JM, McAvoy MP, Shulman GL (2000) Voluntary orienting is dissociated from target detection in human posterior parietal cortex. Nat Neurosci 3:292–297PubMedCrossRef

Corbetta M, Shulman GL (2002) Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3:201–215PubMedCrossRef

Corbetta M, Kincade JM, Shulman GL (2002) Neural systems for visual orienting and their relationships to spatial working memory. J Cogn Neurosci 14:508–523PubMedCrossRef

Coull JT, Nobre AC (1998) Where and when to pay attention: the neural systems for directing attention to spatial locations and to time intervals as revealed by both PET and fMRI. J Neurosci 18:7426–7435PubMed

Downar J, Crawley AP, Mikulis DJ, Davis KD (2000) A multimodal cortical network for the detection of changes in the sensory environment. Nat Neurosci 3:277–283PubMedCrossRef

Degerman A, Rinne T, Salmi J, Salonen O, Alho K (2006) Selective attention to sound location or pitch studied with fMRI. Brain Res 1077:123–134PubMedCrossRef

Farah MJ, Wong AB, Monheit MA, Morrow LA (1989) Parietal lobe mechanisms of spatial attention: modality specific or multimodal? Brain Res 27:461–470

Fiez JA, Petersen SE, Cheney MK, Raichle ME (1992) Impaired non-motor learning and error detection associated with cerebellar damage. A single case study. Brain 115:155–178PubMedCrossRef

Furukawa S, Xu L, Middlebrooks JC (2000) Coding of sound-source location by ensembles of cortical neurons. J Neurosci 20:1216–1228PubMed

Gaab N, Gaser C, Zaehle T, Jäncke L, Schlaug G (2003) Functional anatomy of pitch memory-an fMRI study with sparse temporal sampling. Neuroimage 19:1417–1426PubMedCrossRef

Gemba H, Sasaki K (1989) Potential related to no-go reaction of go/no-go hand movement task with color discrimination in human. Neurosci Lett 101:263–268PubMedCrossRef

Giesbrecht B, Woldorff MG, Song AW, Mangun GR (2003) Neural mechanisms of top-down control during spatial and feature attention. Neuroimage 19:496–512PubMedCrossRef

Gitelman DR, Nobre AC, Parrish TB, LaBar KS, Kim YH, Meyer JR, Mesulam MM (1999) A large-scale distributed network for covert spatial attention: further anatomical deliation based on stringent behavioural and cognitive controls. Brain 122:1093–1106PubMedCrossRef

Gottwald B, Mihajlovic Z, Wilde B, Mehdorn HM (2003) Does the cerebellum contribute to specific aspects of attention? Neuropsychologia 41:1452–1460PubMedCrossRef

Heinze HJ, Mangun GR, Burchert W, Hinrichs H, Scholz M, Münte TF, Gos A, Scherg M, Johannes S, Hundeshagen H (1994) Combined spatial and temporal imaging of brain activity during visual selective attention in humans. Nature 372:543–546PubMedCrossRef

Hopfinger JB, Buonocore MH, Mangun GR (2000) The neural mechanisms of top-down attentional control. Nat Neurosci 3:284–291PubMedCrossRef

Hugdahl K, Wester K, Asbjornsen A (1991) Auditory neglect after right frontal lobe and right pulvinar thalamic lesions. Brain Lang 41:465–473PubMedCrossRef

Hyvärinen J (1982) Posterior parietal lobe of the primate brain. Physiol Rev 62:1060–1129PubMed

Ito M (1990) A new physiological concept on cerebellum. Rev Neurol 146:564–569PubMed

Kirschen MP, Chen SH, Schraedley-Desmond P, Desmond JE (2005) Load- and practice-dependent increases in cerebro-cerebellar activation in verbal working memory: an fMRI study. Neuroimage 24:462–472PubMedCrossRef

Knight RT, Scabini D, Woods DL, Clayworth CC (1989) Contributions of temporal-parietal junction to the human auditory P3. Brain Res 502:109–116PubMedCrossRef

Konishi S, Nakajima K, Uchida I, Kikyo H, Kameyama M, Miyashita Y (1999) Common inhibitory mechanism in human inferior prefrontal cortex revealed by event-related functional MRI. Brain 122:981–991PubMedCrossRef

LaBerge D (1995) Attentional processing: the brain’s art of mindfulness. Harvard University Press, Cambridge

LaBerge D, Buchsbaum MS (1990) Positron emission tomographic measurements of pulvinar activity during an attention task. J Neurosci 10:613–619PubMed

Le TH, Pardo JV, Hu X (1998) 4 T-fMRI study of nonspatial shifting of selective attention: cerebellar and parietal contributions. J Neurophysiol 79:1535–1548PubMed

Leiner HC, Leiner AL, Dow RS (1991) The human cerebro-cerebellar system: its computing, cognitive, and language skills. Behav Brain Res 44:113–128PubMedCrossRef

Mangun GR, Buonocore MH, Girelli M, Jha AP (1998) ERP and fMRI measures of visual spatial selective attention. Hum Brain Mapp 6:383–389PubMedCrossRef

Martinkauppi S, Rämä P, Aronen HJ, Korvenoja A, Carlson S (2000) Working memory of auditory localization. Cereb Cortex 10:889–898PubMedCrossRef

Menon V, Adleman NE, White CD, Glover GH, Reiss AL (2001) Error-related brain activation during a Go/NoGo response inhibition task. Hum Brain Mapp 12:131–143PubMedCrossRef

Mesulam MM (1999) Spatial attention and neglect: parietal, frontal and cingulate contributions to the mental representation and attentional targeting of salient extrapersonal events. Philos Trans R Soc Lond B Biol Sci 354:1325–1346PubMedCrossRef

Mesulam MM (1981) A cortical network for directed attention and unilateral neglect. Ann Neurol 10:309–325PubMedCrossRef

Mesulam MM, Van Hoesen GW, Pandya DN, Geschwind N (1977) Limbic and sensory connections of the inferior parietal lobule (area PG) in the rhesus monkey: a study with a new method for horseradish peroxidase histochemistry. Brain Res 136:393–414PubMedCrossRef

Middleton FA, Strick PL (1997) Cerebellar output channels. Int Rev Neurobiol 41:61–82PubMedCrossRef

Molholm S, Martinez A, Ritter W, Javitt DC, Foxe JJ (2005) The neural circuitry of pre-attentive auditory change-detection: an fMRI study of pitch and duration mismatch negativity generators. Cereb Cortex 15:545–551PubMedCrossRef

Näätänen R (1990) The role of attention in auditory information processing as revealed by event-related potentials and other brain measures of cognitive function. Behav Brain Sci 13:201–233

Nitschke MF, Binkofski F, Buccino G, Posse S, Erdmann C, Kompf D, Seitz RJ, Heide W (2004) Activation of cerebellar hemispheres in spatial memorization of saccadic eye movements: an fMRI study. Hum Brain Mapp 22:155–164PubMedCrossRef

Noesselt T, Hillyard SA, Woldorff MG, Schoenfeld A, Hagner T, Jäncke L, Tempelmann C, Hinrichs H, Heinze HJ (2002) Delayed striate cortical activation during spatial attention. Neuron 35:575–587PubMedCrossRef

Petkov CI, Kang X, Alho K, Bertrand O, Yund EW, Woods DL (2004) Attentional modulation of human auditory cortex. Nat Neurosci 7:658–663PubMedCrossRef

Posner MI, Rothbart MK (2007) Research on attention networks as a model for the integration of psychological science. Annu Rev Psychol 10:1–23CrossRef

Price CJ, Veltman DJ, Ashburner J, Josephs O, Friston KJ (1999) The critical relationship between the timing of stimulus presentation and data acquisition in blocked designs with fMRI. Neuroimage 10:36–44PubMedCrossRef

Ramnani N, Behrens TE, Johansen-Berg H, Richter MC, Pinsk MA, Andersson JL, Rudebeck P, Ciccarelli O, Richter W, Thompson AJ, Gross CG, Robson MD, Kastner S, Matthews PM (2006) The evolution of prefrontal inputs to the cortico-pontine system: diffusion imaging evidence from Macaque monkeys and humans. Cereb Cortex 16:811–818PubMedCrossRef

Rinne T, Degerman A, Alho K (2005) Superior temporal and inferior frontal cortices are activated by infrequent sound duration decrements: an fMRI study. Neuroimage 26:66–72PubMedCrossRef

Schall JD (2002) The neural selection and control of saccades by the frontal eye field. Philos Trans R Soc Lond B Biol Sci 29:1073–1082

Schmahmann JD (1996) From movement to thought: anatomic substrates of cerebellar contribution to cognitive processing. Hum Brain Mapp 4:174–198CrossRef

Schmahmann JD (1997) The cerebellum and cognition. Int Rev Neurobiol 41:475–630CrossRef

Schmahmann JD, Doyon J, Toga AW, Petrides M, Evans AC (2000) MRI atlas of the human cerebellum. Academic, London

Shomstein S, Yantis S (2006) Parietal cortex mediates voluntary control of spatial and nonspatial auditory attention. J Neurosci 26:435–439PubMedCrossRef

Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TE, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, Niazy RK, Saunders J, Vickers J, Zhang Y, De Stefano N, Brady JM, Matthews PM (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23(Suppl 1):S208–S219PubMedCrossRef

Stecker GC, Middlebrooks JC (2003) Distributed coding of sound locations in the auditory cortex. Biol Cybern 89:341–349PubMedCrossRef

Thoenissen D, Zilles K, Toni I (2002) Differential involvement of parietal and precentral regions in movement preparation and motor intention. J Neurosci 15:9024–9034

Toni I, Shah NJ, Fink GR, Thoenissen D, Passingham RE, Zilles K (2002) Multiple movement representations in the human brain: an event-related fMRI study. J Cogn Neurosci 14:769–784PubMedCrossRef

Tootell RB, Hadjikhani N, Hall EK, Marrett S, Vanduffel W, Vaughan JT, Dale AM (1998) The retinotopy of visual spatial attention. Neuron 21:1409–1422PubMedCrossRef

Townsend J, Courchesne E, Covington J, Westerfield M, Harris NS, Lyden P, Lowry TP, Press GA (1999) Spatial attention deficits in patients with acquired or developmental cerebellar abnormality. J Neurosci 19:5632–5643PubMed

Vandenberghe R, Gitelman DR, Parrish TB, Mesulam MM (2001) Functional specificity of superior parietal mediation of spatial shifting. Neuroimage 14:661–673PubMedCrossRef

Winkowski DE, Knudsen EI (2006) Top-down gain control of the auditory space map by gaze control circuitry in the barn owl. Nature 439:336–339PubMedCrossRef

Weissmann DH, Warner LM, Woldorff MG (2004) The neural mechanisms for minimizing cross-modal distraction. J Neurosci 24:10941–10949CrossRef

Woldorff MG, Hillyard SA (1991) Modulation of early auditory processing during selective listening to rapidly presented tones. Electroencephalogr Clin Neurophysiol 79:170–191PubMedCrossRef

Woods DL, Alho K, Algazi A (1992) Intermodal selective attention I: effects on event-related potentials to lateralized auditory and visual stimuli. Electroencephalogr Clin Neurophysiol 82:341–355PubMedCrossRef

Woods DL, Knight RT, Scabini D (1993) Anatomical substrates of auditory selective attention: behavioral and electrophysiological effects of posterior association cortex lesions. Cogn Brain Res 1:227–240CrossRef

Woolrich MW, Ripley BD, Brady M, Smith SM (2001) Temporal autocorrelation in univariate linear modeling of FMRI data. Neuroimage 14:1370–1386PubMedCrossRef

Wu CT, Weissman DH, Roberts KC, Woldorff MG (2007) The neural circuitry underlying the executive control of auditory spatial attention. Brain Res 23:187–198CrossRef

Yantis S, Schwarzbach J, Serences JT, Carlson RL, Steinmetz MA, Pekar JJ, Courtney SM (2002) Transient neural activity in human parietal cortex during spatial attention shifts. Nat Neurosci 5:995–1002PubMedCrossRef

Zatorre RJ, Bouffard M, Ahad P, Belin P (2002) Where is ‘where’ in the human auditory cortex? Nat Neurosci 5:905–909PubMedCrossRef

Zatorre RJ, Mondor TA, Evans AC (1999) Auditory attention to space and frequency activates similar cerebral systems. Neuroimage 10:544–554PubMedCrossRef

Title: Orienting and maintenance of spatial attention in audition and vision: multimodal and modality-specific brain activations
Authors: Juha Salmi
Teemu Rinne
Alexander Degerman
Oili Salonen
Kimmo Alho
Publication date: 01-09-2007
Publisher: Springer-Verlag
Published in: Brain Structure and Function / Issue 2/2007
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-007-0152-2

At a glance: The STEP trials

Springer Medicine

Orienting and maintenance of spatial attention in audition and vision: multimodal and modality-specific brain activations

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 2/2007

Origin, migration and fate of newly generated neurons in the adult rodent piriform cortex

A detailed 3D model of the guinea pig cochlea

Anatomical analysis of afferent projections to the medial prefrontal cortex in the rat

Mapping functional connectivity in barrel-related columns reveals layer- and cell type-specific microcircuits

Do early sensory cortices integrate cross-modal information?

Precerebellar and vestibular nuclei of the short-beaked echidna (Tachyglossus aculeatus)