Do early sensory cortices integrate cross-modal information?

Brain Structure and Function - Tập 212 Số 2 - Trang 121-132 - 2007
Christoph Kayser1, Nikos K. Logothetis2,1
1Max Planck Institute for Biological Cybernetics, Tübingen, Germany
2Division of Imaging Science and Biomedical Engineering, University of Manchester, Manchester, UK

Tóm tắt

Từ khóa


Tài liệu tham khảo

Adrian ED (1949) The Sherrington lectures: 1. Sensory integration: University of Liverpool Press

Alvarado JC, Vaughan JW, Stanford TR, Stein BE (2007) Multisensory versus unisensory integration: contrasting modes in the superior colliculus. J Neurophysiol 97:3193–3205

Avillac M, Ben Hamed S, Duhamel JR (2007) Multisensory integration in the ventral intraparietal area of the macaque monkey. J Neurosci 27:1922–1932

Banati RB, Goerres GW, Tjoa C, Aggleton JP, Grasby P (2000) The functional anatomy of visual-tactile integration in man: a study using positron emission tomography. Neuropsychologia 38:115–124

Barnes CL, Pandya DN (1992) Efferent cortical connections of multimodal cortex of the superior temporal sulcus in the rhesus monkey. J Comp Neurol 318:222–244

Barraclough NE, Xiao D, Baker CI, Oram MW, Perrett DI (2005) Integration of visual and auditory information by superior temporal sulcus neurons responsive to the sight of actions. J Cogn Neurosci 17:377–391

Beauchamp MS (2005) Statistical criteria in FMRI studies of multisensory integration. Neuroinformatics 3:93–114

Beauchamp MS, Lee KE, Argall BD, Martin A (2004) Integration of auditory and visual information about objects in superior temporal sulcus. Neuron 41:809–823

Benevento LA, Fallon J, Davis BJ, Rezak M (1977) Auditory–visual interaction in single cells in the cortex of the superior temporal sulcus and the orbital frontal cortex of the macaque monkey. Exp Neurol 57:849–872

Bental E, Dafny N, Feldman S (1968) Convergence of auditory and visual stimuli on single cells in the primary visual cortex of unanesthetized unrestrained cats. Exp Neurol 20:341–351

Bernstein LE, Auer ET Jr, Moore JK, Ponton CW, Don M, Singh M (2002) Visual speech perception without primary auditory cortex activation. Neuroreport 13:311–315

Bizley JK, Nodal FR, Bajo VM, Nelken I, King AJ (2006) Physiological and anatomical evidence for multisensory interactions in auditory cortex. Cereb Cortex Epub doi:10.1093/cercor/bhl128

Bremmer F, Klam F, Duhamel JR, Ben Hamed S, Graf W (2002) Visual-vestibular interactive responses in the macaque ventral intraparietal area (VIP). Eur J Neurosci 16:1569–1586

Bruce C, Desimone R, Gross CG (1981) Visual properties of neurons in a polysensory area in superior temporal sulcus of the macaque. J Neurophysiol 46:369–384

Budinger E, Heil P, Hess A, Scheich H (2006) Multisensory processing via early cortical stages: connections of the primary auditory cortical field with other sensory systems. Neuroscience 143:1065–1083

Bullier J (2001) Integrated model of visual processing. Brain Res Brain Res Rev 36:96–107

Calvert GA (2001) Crossmodal processing in the human brain: insights from functional neuroimaging studies. Cereb Cortex 11:1110–1123

Calvert GA, Bullmore ET, Brammer MJ, Campbell R, Williams SC, McGuire PK, Woodruff PW, Iversen SD, David AS (1997) Activation of auditory cortex during silent lipreading. Science 276:593–596

Calvert GA, Brammer MJ, Bullmore ET, Campbell R, Iversen SD, David AS (1999) Response amplification in sensory-specific cortices during crossmodal binding. Neuroreport 10:2619–2623

Calvert GA, Campbell R, Brammer MJ (2000) Evidence from functional magnetic resonance imaging of crossmodal binding in the human heteromodal cortex. Curr Biol 10:649–657

Cappe C, Barone P (2005) Heteromodal connections supporting multisensory integration at low levels of cortical processing in the monkey. Eur J Neurosci 22:2886–2902

Colin C, Radeau M, Soquet A, Demolin D, Colin F, Deltenre P (2002) Mismatch negativity evoked by the McGurk-MacDonald effect: a phonetic representation within short-term memory. Clin Neurophysiol 113:495–506

Crabtree JW, Isaac JT (2002) New intrathalamic pathways allowing modality-related and cross-modality switching in the dorsal thalamus. J Neurosci 22:8754–8761

Crabtree JW, Collingridge GL, Isaac JT (1998) A new intrathalamic pathway linking modality-related nuclei in the dorsal thalamus. Nat Neurosci 1:389–394

Crivello F, Schormann T, Tzourio-Mazoyer N, Roland PE, Zilles K, Mazoyer BM (2002) Comparison of spatial normalization procedures and their impact on functional maps. Hum Brain Mapp 16:228–250

Cusick CG, Seltzer B, Cola M, Griggs E (1995) Chemoarchitectonics and corticocortical terminations within the superior temporal sulcus of the rhesus monkey: evidence for subdivisions of superior temporal polysensory cortex. J Comp Neurol 360:513–535

de la Mothe LA, Blumell S, Kajikawa Y, Hackett TA (2006) Thalamic connections of the auditory cortex in marmoset monkeys: core and medial belt regions. J Comp Neurol 496:72–96

Dehner LR, Keniston LP, Clemo HR, Meredith MA (2004) Cross-modal circuitry between auditory and somatosensory areas of the cat anterior ectosylvian sulcal cortex: a ‘new’ inhibitory form of multisensory convergence. Cereb Cortex 14:387–403

Desai R, Liebenthal E, Possing ET, Waldron E, Binder JR (2005) Volumetric vs. surface-based alignment for localization of auditory cortex activation. Neuroimage 26:1019–1029

Driver J, Spence C (1998) Crossmodal attention. Curr Opin Neurobiol 8:245–253

Duhamel JR, Colby CL, Goldberg ME (1998) Ventral intraparietal area of the macaque: congruent visual and somatic response properties. J Neurophysiol 79:126–136

Engel SA, Rumelhart DE, Wandell BA, Lee AT, Glover GH, Chichilnisky EJ, Shadlen MN (1994) fMRI of human visual cortex. Nature 369:525

Ernst MO, Bulthoff HH (2004) Merging the senses into a robust percept. Trends Cogn Sci 8:162–169

Falchier A, Clavagnier S, Barone P, Kennedy H (2002) Anatomical evidence of multimodal integration in primate striate cortex. J Neurosci 22:5749–5759

Felleman DJ, Van Essen DC (1991) Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex 1:1–47

Fishman MC, Michael P (1973) Integration of auditory information in the cat’s visual cortex. Vision Res 13:1415–1419

Fogassi L, Gallese V, Fadiga L, Luppino G, Matelli M, Rizzolatti G (1996) Coding of peripersonal space in inferior premotor cortex (area F4). J Neurophysiol 76:141–157

Fort A, Delpuech C, Pernier J, Giard MH (2002a) Dynamics of cortico-subcortical cross-modal operations involved in audio–visual object detection in humans. Cereb Cortex 12:1031–1039

Fort A, Delpuech C, Pernier J, Giard MH (2002b) Early auditory-visual interactions in human cortex during nonredundant target identification. Brain Res Cogn Brain Res 14:20–30

Foxe JJ, Schroeder CE (2005) The case for feedforward multisensory convergence during early cortical processing. Neuroreport 16:419–423

Foxe JJ, Wylie GR, Martinez A, Schroeder CE, Javitt DC, Guilfoyle D, Ritter W, Murray MM (2002) Auditory-somatosensory multisensory processing in auditory association cortex: an fMRI study. J Neurophysiol 88:540–543

Frens MA, Van Opstal AJ (1995) A quantitative study of auditory-evoked saccadic eye movements in two dimensions. Exp Brain Res 107:103–117

Fu KM, Johnston TA, Shah AS, Arnold L, Smiley J, Hackett TA, Garraghty PE, Schroeder CE (2003) Auditory cortical neurons respond to somatosensory stimulation. J Neurosci 23:7510–7515

Fuster JM, Bodner M, Kroger JK (2000) Cross-modal and cross-temporal association in neurons of frontal cortex. Nature 405:347–351

Ghazanfar AA, Schroeder CE (2006) Is neocortex essentially multisensory? Trends Cogn Sci 10:278–285

Ghazanfar AA, Maier JX, Hoffman KL, Logothetis NK (2005) Multisensory integration of dynamic faces and voices in rhesus monkey auditory cortex. J Neurosci 25:5004–5012

Giard MH, Peronnet F (1999) Auditory-visual integration during multimodal object recognition in humans: a behavioral and electrophysiological study. J Cogn Neurosci 11:473–490

Gielen SC, Schmidt RA, Van den Heuvel PJ (1983) On the nature of intersensory facilitation of reaction time. Percept Psychophys 34:161–168

Graziano MS, Yap GS, Gross CG (1994) Coding of visual space by premotor neurons. Science 266:1054–1057

Graziano MS, Reiss LA, Gross CG (1999) A neuronal representation of the location of nearby sounds. Nature 397:428–430

Guest S, Catmur C, Lloyd D, Spence C (2002) Audiotactile interactions in roughness perception. Exp Brain Res 146:161–171

Hackett TA, Stepniewska I, Kaas JH (1998) Subdivisions of auditory cortex and ipsilateral cortical connections of the parabelt auditory cortex in macaque monkeys. J Comp Neurol 394:475–495

Hackett TA, De La Mothe LA, Ulbert I, Karmos G, Smiley J, Schroeder CE (2007) Multisensory convergence in auditory cortex, II. Thalamocortical connections of the caudal superior temporal plane. J Comp Neurol 502:924–952

Hershenson M (1962) Reaction time as a measure of intersensory facilitation. J Exp Psychol 63:289–293

Hikosaka K, Iwai E, Saito H, Tanaka K (1988) Polysensory properties of neurons in the anterior bank of the caudal superior temporal sulcus of the macaque monkey. J Neurophysiol 60:1615–1637

Howard IP, Templeton WB (1966) Human spatial orientation. Wiley, London

Hyvarinen J, Shelepin Y (1979) Distribution of visual and somatic functions in the parietal associative area 7 of the monkey. Brain Res 169:561–564

Jones EG (1998) Viewpoint: the core and matrix of thalamic organization. Neuroscience 85:331–345

Jones EG, Powell TP (1970) An anatomical study of converging sensory pathways within the cerebral cortex of the monkey. Brain 93:793–820

Jousmaki V, Hari R (1998) Parchment-skin illusion: sound-biased touch. Curr Biol 8:R190

Kaas JH, Hackett TA (2000) Subdivisions of auditory cortex and processing streams in primates. Proc Natl Acad Sci USA 97:11793–11799

Kayser C, Petkov CI, Augath M, Logothetis NK (2005) Integration of touch and sound in auditory cortex. Neuron 48:373–384

Kayser C, Petkov CI, Augath M, Logothetis NK (2007) Functional imaging reveals visual modulation of specific fields in auditory cortex. J Neurosci 27:1824–1835

Krauzlis RJ, Liston D, Carello CD (2004) Target selection and the superior colliculus: goals, choices and hypotheses. Vision Res 44:1445–1451

Lakatos P, Chen CM, O’Connell MN, Mills A, Schroeder CE (2007) Neuronal oscillations and multisensory interaction in primary auditory cortex. Neuron 53:279–292

Lamme VA, Roelfsema PR (2000) The distinct modes of vision offered by feedforward and recurrent processing. Trends Neurosci 23:571–579

Lauritzen M (2005) Reading vascular changes in brain imaging: is dendritic calcium the key? Nat Rev Neurosci 6:77–85

Laurienti PJ, Perrault TJ, Stanford TR, Wallace MT, Stein BE (2005) On the use of superadditivity as a metric for characterizing multisensory integration in functional neuroimaging studies. Exp Brain Res 166:298–297

Lehmann C, Herdener M, Esposito F, Hubl D, di Salle F, Scheffler K, Bach DR, Federspiel A, Kretz R, Dierks T, Seifritz E (2006) Differential patterns of multisensory interactions in core and belt areas of human auditory cortex. Neuroimage 31:294–300

Levitt JB, Lund JS (1997) Contrast dependence of contextual effects in primate visual cortex. Nature 387:73–76

Logothetis NK, Wandell BA (2004) Interpreting the BOLD Signal. Annu Rev Physiol 66:735–769

Logothetis NK, Guggenberger H, Peled S, Pauls J (1999) Functional imaging of the monkey brain. Nat Neurosci 2:555–562

Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A (2001) Neurophysiological investigation of the basis of the fMRI signal. Nature 412:150–157

Lomo T, Mollica A (1959) Activity of single units of the primary optic cortex during stimulation by light, sound, smell and pain, in unanesthetized rabbits. Boll Soc Ital Biol Sper 35:1879–1882

Macaluso E, Frith CD, Driver J (2000) Modulation of human visual cortex by crossmodal spatial attention. Science 289:1206–1208

Martin KA (2002) Microcircuits in visual cortex. Curr Opin Neurobiol 12:418–425

McDonald JJ, Teder-Salejarvi WA, Hillyard SA (2000) Involuntary orienting to sound improves visual perception. Nature 407:906–908

McGurk H, MacDonald J (1976) Hearing lips and seeing voices. Nature 264:746–748

Meredith MA, Keniston LR, Dehner LR, Clemo HR (2006) Crossmodal projections from somatosensory area SIV to the auditory field of the anterior ectosylvian sulcus (FAES) in Cat: further evidence for subthreshold forms of multisensory processing. Exp Brain Res Epub (ahead of publication)

Molholm S, Ritter W, Murray MM, Javitt DC, Schroeder CE, Foxe JJ (2002) Multisensory auditory-visual interactions during early sensory processing in humans: a high-density electrical mapping study. Brain Res Cogn Brain Res 14:115–128

Moore CI, Nelson SB, Sur M (1999) Dynamics of neuronal processing in rat somatosensory cortex. Trends Neurosci 22:513–520

Morel A, Kaas JH (1992) Subdivisions and connections of auditory cortex in owl monkeys. J Comp Neurol 318:27–63

Morrell F (1972) Visual system’s view of acoustic space. Nature 238:44–46

Mottonen R, Krause CM, Tiippana K, Sams M (2002) Processing of changes in visual speech in the human auditory cortex. Brain Res Cogn Brain Res 13:417–425

Murata K, Cramer H, Bach-y-Rita P (1965) Neuronal convergence of noxious, acoustic, and visual stimuli in the visual cortex of the cat. J Neurophysiol 28:1223–1239

Murray MM, Molholm S, Michel CM, Heslenfeld DJ, Ritter W, Javitt DC, Schroeder CE, Foxe JJ (2005) Grabbing your ear: rapid auditory-somatosensory multisensory interactions in low-level sensory cortices are not constrained by stimulus alignment. Cereb Cortex 15:963–974

Pandya DN, Rosene DL, Doolittle AM (1994) Corticothalamic connections of auditory-related areas of the temporal lobe in the rhesus monkey. J Comp Neurol 345:447–471

Pekkola J, Ojanen V, Autti T, Jaaskelainen IP, Mottonen R, Sams M (2005a) Attention to visual speech gestures enhances hemodynamic activity in the left planum temporale. Hum Brain Mapp 27:471–477

Pekkola J, Ojanen V, Autti T, Jaaskelainen IP, Mottonen R, Tarkiainen A, Sams M (2005b) Primary auditory cortex activation by visual speech: an fMRI study at 3 T. Neuroreport 16:125–128

Perrault TJ Jr, Vaughan JW, Stein BE, Wallace MT (2003) Neuron-specific response characteristics predict the magnitude of multisensory integration. J Neurophysiol 90:4022–4026

Petkov CI, Kayser C, Augath M, Logothetis NK (2006) Functional imaging reveals numerous fields in the monkey auditory cortex. PLOS Biology 4:e215

Rademacher J, Caviness VS Jr, Steinmetz H, Galaburda AM (1993) Topographical variation of the human primary cortices: implications for neuroimaging, brain mapping, and neurobiology. Cereb Cortex 3:313–329

Rao RP, Ballard DH (1999) Predictive coding in the visual cortex: a functional interpretation of some extra-classical receptive-field effects. Nat Neurosci 2:79–87

Riesenhuber M, Poggio T (2000) Models of object recognition. Nat Neurosci 3(Suppl):1199–1204

Rizzolatti G, Scandolara C, Gentilucci M, Camarda R (1981) Response properties and behavioral modulation of “mouth” neurons of the postarcuate cortex (area 6) in macaque monkeys. Brain Res 225:421–424

Rockland KS, Ojima H (2003) Multisensory convergence in calcarine visual areas in macaque monkey. Int J Psychophysiol 50:19–26

Romanski LM, Bates JF, Goldman-Rakic PS (1999) Auditory belt and parabelt projections to the prefrontal cortex in the rhesus monkey. J Comp Neurol 403:141–157

Saito DN, Yoshimura K, Kochiyama T, Okada T, Honda M, Sadato N (2005) Cross-modal binding and activated attentional networks during audio–visual speech integration: a functional MRI study. Cereb Cortex 15:1750–1760

Schlack A, Sterbing-D’Angelo SJ, Hartung K, Hoffmann KP, Bremmer F (2005) Multisensory space representations in the macaque ventral intraparietal area. J Neurosci 25:4616–4625

Schroeder CE, Foxe JJ (2002) The timing and laminar profile of converging inputs to multisensory areas of the macaque neocortex. Brain Res Cogn Brain Res 14:187–198

Schroeder CE, Lindsley RW, Specht C, Marcovici A, Smiley JF, Javitt DC (2001) Somatosensory input to auditory association cortex in the macaque monkey. J Neurophysiol 85:1322–1327

Schroeder CE, Smiley J, Fu KG, McGinnis T, O’Connell MN, Hackett TA (2003) Anatomical mechanisms and functional implications of multisensory convergence in early cortical processing. Int J Psychophysiol 50:5–17

Schroeder CE, Molholm S, Lakatos P, Ritter W, Foxe JJ (2004) Human–simian correspondence in the early cortical processing of multisensory cues. Cogn Process 5:140–151

Schurmann M, Caetano G, Hlushchuk Y, Jousmaki V, Hari R (2006) Touch activates human auditory cortex. Neuroimage 30:1325–1331

Seltzer B, Cola MG, Gutierrez C, Massee M, Weldon C, Cusick CG (1996) Overlapping and nonoverlapping cortical projections to cortex of the superior temporal sulcus in the rhesus monkey: double anterograde tracer studies. J Comp Neurol 370:173–190

Shams L, Kamitani Y, Shimojo S (2000) Illusions. What you see is what you hear. Nature 408:788

Sillito AM, Cudeiro J, Jones HE (2006) Always returning: feedback and sensory processing in visual cortex and thalamus. Trends Neurosci 29:307–316

Smiley JF, Hackett TA, Ulbert I, Karmas G, Lakatos P, Javitt DC, Schroeder CE (2007) Multisensory convergence in auditory cortex, I. Cortical connections of the caudal superior temporal plane in macaque monkeys. J Comp Neurol 502:894–923

Somers DC, Todorov EV, Siapas AG, Toth LJ, Kim DS, Sur M (1998) A local circuit approach to understanding integration of long-range inputs in primary visual cortex. Cereb Cortex 8:204–217

Spinelli DN, Starr A, Barrett TW (1968) Auditory specificity in unit recordings from cat’s visual cortex. Exp Neurol 22:75–84

Stanford TR, Stein BE (2007) Superadditivity in multisensory integration: putting the computation in context. Neuroreport 18:787–792

Stanford TR, Quessy S, Stein BE (2005) Evaluating the operations underlying multisensory integration in the cat superior colliculus. J Neurosci 25:6499–6508

Stein BE (1998) Neural mechanisms for synthesizing sensory information and producing adaptive behaviors. Exp Brain Res 123:124–135

Stein BE, Meredith MA (1993) Merging of the Senses. MIT Press, Cambridge

Stein BE, Wallace MT (1996) Comparisons of cross-modality integration in midbrain and cortex. Prog Brain Res 112:289–299

Sugihara T, Diltz MD, Averbeck BB, Romanski LM (2006) Integration of auditory and visual communication information in the primate ventrolateral prefrontal cortex. J Neurosci 26:11138–11147

Sumby WH, Polack I (1954) Visual contribution to speech intelligibility in noise. J Acoust Soc Am 26:212–215

Towe AL, Harding GW (1970) Extracellular microelectrode sampling bias. Exp Neurol 29:366–381

Ullman S (1995) Sequence seeking and counter streams: a computational model for bidirectional information flow in the visual cortex. Cereb Cortex 5:1–11

van Atteveldt N, Formisano E, Goebel R, Blomert L (2004) Integration of letters and speech sounds in the human brain. Neuron 43:271–282

Vaudano E, Legg CR, Glickstein M (1991) Afferent and efferent connections of temporal association cortex in the rat: a horseradish peroxidase study. Eur J Neurosci 3:317–330

Vroomen J, de Gelder B (2000) Sound enhances visual perception: cross-modal effects of auditory organization on vision. J Exp Psychol Hum Percept Perform 26:1583–1590

Zaborszky L (2002) The modular organization of brain systems. Basal forebrain: the last frontier. Prog Brain Res 136:359–372

Zaborszky L, Duque A (2000) Local synaptic connections of basal forebrain neurons. Behav Brain Res 115:143–158

Zikopoulos B, Barbas H (2006) Prefrontal projections to the thalamic reticular nucleus form a unique circuit for attentional mechanisms. J Neurosci 26:7348–7361