Anatomical evidence of multimodal integration in primate striate cortex

Falchier, Arnaud; Clavagnier, Simon; Barone, Pascal; Kennedy, Henry

doi:10.1523/jneurosci.22-13-05749.2002

Cited by 892Multisensory perception and integrationVisual perception and processing mechanismsTactile and Sensory Interactions

Anatomical evidence of multimodal integration in primate striate cortex

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Falchier, Arnaud, Clavagnier, Simon, Barone, Pascal, Kennedy, Henry·2002·The Journal of Neuroscience

DOI 10.1523/jneurosci.22-13-05749.2002PMC PMC6758216

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Abstract

The primary visual cortex (area 17 or V1) is not thought to receive input from nonvisual extrastriate cortical areas. However, this has yet to be shown to be the case using sensitive tracers in the part of area 17 subserving the peripheral visual field. Here we show using retrograde tracers that peripheral area 17 subserving the visual field at an eccentricity of 10-20 degrees receives projections from the core and parabelt areas of the auditory cortex as well as from the polysensory area of the temporal lobe (STP). The relative strength of these projections was calculated for each injection by computing the proportions of retrogradely labeled neurons located in the auditory and STP areas with respect to number of labeled neurons constituting the established projection from the superior temporal sulci (STS) motion complex (middle temporal area, medial superior temporal, fundus of the superior temporal area). In peripheral area V1 the projection from auditory cortex corresponds to 9.5% of that of the STS motion complex and STP to 35% of that from the STS motion complex. Compared to peripheral area 17, central and paracentral area 17 showed considerably weaker inputs from auditory cortex (0.2-0.8%) but slightly more from STP cortex (3.5-6.1%). The present results show that the connectivity of area 17 is eccentricity dependent. Direct projections from auditory and STP cortex to peripheral area 17 have important consequences for higher visual functions of area 17, including multimodal integration at early stages of the visual cortical pathway.

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Internal heterogeneity in connectivity patterns is well documented for the peripheral versus central representations of V1, V2, and V4 and for the body representation of F2.
“This is well documented for the peripheral versus central representations of V1, V2, and V4 (Falchier et al. 2002) and the body representation of F2 (Johnson et al. 1996; Matelli et al. 1998; Tanne-Gariepy et al. 2002; Luppino et al. 2003).”
From A Weighted and Directed Interareal Connectivity Matrix for Macaque Cerebral Cortex (2014) · cites this paper as Falchier et al. 2002
Many cortical areas show major internal heterogeneity in their connectivity patterns that exceeds the variability reported here for repeat injections localized to a particular areal subregion.
“Many cortical areas show major internal heterogeneity in their connectivity patterns that exceeds the variability reported here for repeat injections that were localized to a particular areal subregion.”
From A Weighted and Directed Interareal Connectivity Matrix for Macaque Cerebral Cortex (2014) · cites this paper as Falchier et al. 2002
Subsequent studies have revealed numerous connections between functional systems, for example, between early auditory and visual areas.
“However, subsequent studies have revealed numerous connections between functional systems, for example, between early auditory and visual areas (Falchier et al. 2002).”
From A Weighted and Directed Interareal Connectivity Matrix for Macaque Cerebral Cortex (2014) · cites this paper as Falchier et al. 2002

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Anatomy of hierarchy: Feedforward and feedback pathways in macaque visual cortex
Markov, N. T., Vezoli, J., Chameau, P., Falchier, A., Quilodran, R., Huissoud, C., Lamy, C., Misery, P., Giroud, P., Ullman, S., et al. (2014) · Journal of Comparative Neurology · doi:10.1002/cne.23458 · Cited by 759 · see citing works
“…V2 V6A 38.10 22.7 V2 STPi 7.41 27 V2 STPc 0.00 28.2 V2 TPt 0.00 25.2 V2 PGa 2.33 24.6 V2 IPa 37.04 24.2 V2 FST 7.05 16.2 The Journal of Comparative Neurology |Research in Systems Neuroscience 233 1998; Barone et al., 2000; Falchier et al., 2002; Clavagnier et al., 2004; Markov et al., 2011, 2012).”
InfluentialSelf-citation
Visual speech speeds up the neural processing of auditory speech
van Wassenhove, V., Grant, K. W., & Poeppel, D. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0408949102 · Cited by 843 · see citing works
Multisensory interplay reveals crossmodal influences on ‘sensory-specific’ brain regions, neural responses, and judgments
Driver, J., & Noesselt, T. (2008) · Neuron · doi:10.1016/j.neuron.2007.12.013 · Cited by 940 · see citing works
“Current data from macaques suggest fewer direct connections between sensory-specific cortices than for feedback connections (see later section) to those from conventional multisensory areas, such as STS (Falchier et al., 2002).”
Influential
Neural reorganization following sensory loss: the opportunity of change
Merabet, L. B., & Pascual-Leone, A. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2758 · Cited by 751 · see citing works
“and non-human adult primates have demonstrated direct connections between auditory and visual cortical area”
Background
Extrastriate body area in human occipital cortex responds to the performance of motor actions
Astafiev, S. V., Stanley, C. M., Shulman, G. L., & Corbetta, M. (2004) · Nature Neuroscience · doi:10.1038/nn1241 · Cited by 629 · see citing works
“Additional multimodal input into peripheral V1 might come from auditory cortex as well as from the superior temporal polysensory area (area STP), which contains visual, auditory and tactile unimodal and multimodal neuron”
Background
Multisensory convergence in calcarine visual areas in macaque monkey
Rockland, K. S., & Ojima, H. (2003) · International Journal of Psychophysiology · doi:10.1016/s0167-8760(03)00121-1 · Cited by 564 · see citing works
“Moreover, as these originate from neurons in layer 6 (Falchier et al., 2002) and terminate in layers 1 andyor 6 (present study), the projections have the laminar profile of classical feedback or top–down connections (but see cautionary discussion in Rockland, 1997, 2002).”
BackgroundResult
The shape of boubas: sound–shape correspondences in toddlers and adults
Maurer, D. M., Pathman, T., & Mondloch, C. J. (2006) · Developmental Science · doi:10.1111/j.1467-7687.2006.00495.x · Cited by 553 · see citing works
Environmental enrichment strengthens corticocortical interactions and reduces amyloid-β oligomers in aged mice
Mainardi, M., Garbo, A. D., Caleo, M., Berardi, N., Sale, A., & Maffei, L. (2013) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2014.00001 · Cited by 438 · see citing works
“Connections between V1 and A1 have been described in the cat, in the primate and in the prairie vole (Innocenti and Clarke, 1984; Falchier et al., 2002; Campi et al., 2009).”
Background
Cognitive neuroscience: Primary visual cortex and visual awareness
Tong, F. (2003) · Nature Reviews Neuroscience · doi:10.1038/nrn1055 · Cited by 507 · see citing works
Architectonic Mapping of the Human Brain beyond Brodmann
Amunts, K., & Zilles, K. (2015) · Neuron · doi:10.1016/j.neuron.2015.12.001 · Cited by 534 · see citing works
Integrating face and voice in person perception
Campanella, S., & Belin, P. (2007) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2007.10.001 · Cited by 522 · see citing works
“Whether these low-level effects are mediated by feedback projection from the multimodal cortex or by direct interactions between the ‘unimodal’ auditory and visual regions through coupled synchronized oscillations via direct anatomical projections [ 16 ], or both, remains a matter for investigation.”
Multimodal interaction: A review
Turk, M. (2013) · Pattern Recognition Letters · doi:10.1016/j.patrec.2013.07.003 · Cited by 519 · see citing works
“, area V1 in the visual cortex) where connections are made and outputs influenced by crossmodal sources – combining auditory and visual stimuli (Falchier et al., 2002; Arnal et al., 2009; Campi et al., 2010; Werner and Noppeney, 2011; Leitão et al., 2012), visual and tactile stimuli (Vasconcelos et al.”
Background
Multisensory contributions to low-level, ‘unisensory’ processing
Schroeder, C. E., & Foxe, J. J. (2005) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2005.06.008 · Cited by 506 · see citing works
“Most dramatically, two laboratories [15,16] have shown anatomical interconnections between low-level visual and low-level auditory areas, which include the primary cortices (V1 and A1), and two others have shown that eye position can affect the gain of auditory responses in A1 [17,18].”
Background
Do deaf individuals see better?
Bavelier, D., Dye, M., & Hauser, P. C. (2006) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2006.09.006 · Cited by 507 · see citing works
Tactile Spatial Attention Enhances Gamma-Band Activity in Somatosensory Cortex and Reduces Low-Frequency Activity in Parieto-Occipital Areas
Bauer, M., Oostenveld, R., Peeters, M., & Fries, P. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.5228-04.2006 · Cited by 470 · see citing works
“In principle, this might be related to direct input from heteromodal areas (Falchier et al., 2002; Schroeder and Foxe, 2002) or to mechanisms underlying visual imagery that are not yet fully understood (Zhang et al., 2004).”
Background
Multisensory spatial interactions: a window onto functional integration in the human brain
Macaluso, E., & Driver, J. (2005) · Trends in Neurosciences · doi:10.1016/j.tins.2005.03.008 · Cited by 428 · see citing works
“Using retrograde tracing in monkeys, Falchier et al. [ 24 ] found direct connections from primary auditory cortex (A1) to regions in primary visual cortex (V1).”
Weight consistency specifies regularities of macaque cortical networks
Markov, N. T., Misery, P., Falchier, A., Lamy, C., Vezoli, J., Quilodran, R., Gariel, M. A., Giroud, P., Ercsey-Ravasz, M., Pilaz, L. J., et al. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhq201 · Cited by 386 · see citing works
Self-citation
Language processing in the occipital cortex of congenitally blind adults
Bedny, M., Pascual‐Leone, Á., Dodell‐Feder, D., Fedorenko, E. G., & Saxe, R. R. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1014818108 · Cited by 424 · see citing works
“In nonhuman primates, there are very few projections from early auditory to early visual cortices, and cross-modal bottom-up input from thalamic relays has not been shown (53, 54).”
Background
Grabbing Your Ear: Rapid Auditory–Somatosensory Multisensory Interactions in Low-level Sensory Cortices Are Not Constrained by Stimulus Alignment
Murray, M. M., Molholm, S., Michel, C. M., Heslenfeld, D. J., Ritter, W., Javitt, D. C., Schroeder, C. E., & Foxe, J. J. (2004) · Cerebral Cortex · doi:10.1093/cercor/bhh197 · Cited by 404 · see citing works
“Anatomical tracing studies have revealed direct projections to visual areas V1 and V2 from primary (Falchier et al., 2002) as well as association areas (Falchier et al., 2002; Rockland and Ojima, 2003) of macaque auditory cortex.”
Background
Real-time classification and sensor fusion with a spiking deep belief network
O'Connor, P., Neil, D., Liu, S., Delbrück, T., & Pfeiffer, M. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00178 · Cited by 409 · see citing works
“Recent studies have revealed the existence of anatomical connections that would enable cross-modal interactions also at lower levels (Falchier et al., 2002; Markov et al., 2012), and functional studies have provided some (but not conclusive) evidence of co-activations of early sensory areas by…”
Background
Integration of touch and sound in auditory cortex.
Kayser, C., Petkov, C., Augath, M., & Logothetis, N. (2005) · Neuron · doi:10.1016/j.neuron.2005.09.018 · Cited by 404 · see citing works
“This suggestion is further corroborated by the discovery of direct anatomical projections between (primary) auditory and visual cortices (Falchier et al., 2002; Rockland and Ojima, 2003).”
The Basic-Systems Model of Episodic Memory
Rubin, D. C. (2006) · Perspectives on Psychological Science · doi:10.1111/j.1745-6916.2006.00017.x · Cited by 374 · see citing works
Heteromodal connections supporting multisensory integration at low levels of cortical processing in the monkey
Cappe, C., & Barone, P. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04462.x · Cited by 353 · see citing works
“However, the notion that multisensory integration is restricted to high order areas has recently been challenged by anatomical (Falchier et al., 2002; Rockland & Ojima, 2003) imaging (Sathian et al., 1997; Calvert et al., 2000; Laurienti et al., 2002) and electrophysiological data (Giard &…”
BackgroundResultInfluential
Preserved Functional Specialization for Spatial Processing in the Middle Occipital Gyrus of the Early Blind
Renier, L. A., Anurova, I., Volder, A. D., Carlson, S., VanMeter, J. W., & Rauschecker, J. P. (2010) · Neuron · doi:10.1016/j.neuron.2010.09.021 · Cited by 355 · see citing works
“Other possible mechanisms include a strengthening of corticocortical input from other sensory modalities (Falchier et al., 2002; Rockland and Ojima, 2003) or of nonvisual thalamocortical connections (Hackett and Schroeder, 2009).”
Background
Functional imaging of human crossmodal identification and object recognition
Amedi, A., von Kriegstein, K., van Atteveldt, N., Beauchamp, M. S., & Naumer, M. J. (2005) · Experimental Brain Research · doi:10.1007/s00221-005-2396-5 · Cited by 351 · see citing works
“It has recently been shown (Falchier et al. 2002; Rockland and Ojima 2003) that in the macaque areas V1 and V2 receive direct input from core and parabelt auditory areas.”
Background
Physiological and Anatomical Evidence for Multisensory Interactions in Auditory Cortex
Bizley, J. K., Nodal, F. R., Bajo, V. M., Nelken, I., & King, A. J. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhl128 · Cited by 341 · see citing works
“Anatomical studies in primates have shown that different regions of auditory cortex, including A1, project to V1 and V2 (Falchier et al. 2002; Rockland and Ojima 2003).”
Pip and pop: Nonspatial auditory signals improve spatial visual search.
Van der Burg, E., Olivers, C. N. L., Bronkhorst, A. W., & Theeuwes, J. (2008) · Journal of Experimental Psychology: Human Perception and Performance · doi:10.1037/0096-1523.34.5.1053 · Cited by 485 · see citing works
“They are also consistent with neurological evidence that such integration occurs relatively early ( Falchier, Clavagnier, Barone, & Kennedy, 2002; Giard & Peronnet, 1999; Molholm et al., 2002; Talsma, Doty, & Woldorff, 2007) and effortlessly (Vroomen & De Gelder, 2000).”
Background
Information flow in the auditory cortical network
Hackett, T. A. (2010) · Hearing Research · doi:10.1016/j.heares.2010.01.011 · Cited by 349 · see citing works
“4a) (Barbas, 2007;Cavada et al., 2000;Falchier et al., 2002;Falchier et al., 2009;Ghashghaei et al., 2002;Hackett et al., 1999;Kosmal et al., 1997;Lavenex et al., 2002;Lewis et al., 2000;Petrides et al., 2002;Rockland et al., 2003;Romanski et al., 1999a;Romanski et al., 1999b;Saleem et al.,…”
Sound alters activity in human V1 in association with illusory visual perception
Watkins, S., Shams, L. B., Tanaka, S., Haynes, J., & Rees, G. E. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.01.016 · Cited by 336 · see citing works
A revised view of sensory cortical parcellation
Wallace, M. T., Ramachandran, R., & Stein, B. E. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0305697101 · Cited by 329 · see citing works
A Dual Role for Prediction Error in Associative Learning
den Ouden, H. E. M., Friston, K. J., Daw, N. D., McIntosh, A. R., & Stephan, K. E. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhn161 · Cited by 306 · see citing works
“3A), and anatomical connections from primary auditory cortex to peripheral visual cortex have been demonstrated in recent monkey studies (Falchier et al. 2002; Rockland and Ojima 2003).”
Auditory Cortical Neurons Respond to Somatosensory Stimulation
Fu, K., Johnston, T. A., Shah, A., Arnold, L. L., Smiley, J., Hackett, T., Garraghty, P., & Schroeder, C. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-20-07510.2003 · Cited by 348 · see citing works
“, 2001; Schroeder and Foxe, 2002), and cross connections between low-level cortices, including A1, V1, and S1 (Zhou and Fuster, 1996; Falchier et al., 2002; Rockland and Ojima, 2003), suggests that multisensory convergence may occur at early, putatively unisensory, cortical processing stages.”
Background
Multisensory Processing in Review: from Physiology to Behaviour
Alais, D., Newell, F. N., & Mamassian, P. (2010) · Seeing and Perceiving · doi:10.1163/187847510x488603 · Cited by 325 · see citing works
Bimodal speech: early suppressive visual effects in human auditory cortex
Besle, J., Fort, A., Delpuech, C., & Giard, M. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03670.x · Cited by 319 · see citing works
Functional specialization for auditory–spatial processing in the occipital cortex of congenitally blind humans
Collignon, O., Vandewalle, G., Voss, P., Albouy, G., Charbonneau, G., Lassonde, M. C., & Leporé, F. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1013928108 · Cited by 322 · see citing works
“Because both activations and deactivations by nonvisual tasks indicate the presence of nonvisual input in the occipital cortex of sighted individuals (22), these observations suggest that connections between auditory and visual cortices (48) may subserve cross-modal inhibition and/or multisensory integration in the ea…”
Background
The case for feedforward multisensory convergence during early cortical processing
Foxe, J. J., & Schroeder, C. E. (2005) · Neuroreport · doi:10.1097/00001756-200504040-00001 · Cited by 311 · see citing works
“[37] reported direct inputs to peripheral V1 from the auditory cortex, inputs that included the core primary auditory area (A1)”
Background
Multisensory integration: methodological approaches and emerging principles in the human brain.
Calvert, G. A., & Thesen, T. (2004) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2004.03.018 · Cited by 425 · see citing works
“[26] identified projections from core and parabelt auditory cortex into parts of V1 corresponding to the representation of the peripheral visual field.”
Background
Implicit multisensory associations influence voice recognition
von Kriegstein, K., & Giraud, A.-L. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0040326 · Cited by 309 · see citing works
“Early crossmodal effects are also backed-up by anatomical studies that used retrograde labelling of monkey visual cortex to show the presence of projections arising from auditory cortex in several cortical layers [41–44].”
Background
Primary auditory cortex activation by visual speech: an fMRI study at 3???T
Pekkola, J., Ojanen, V., Autti, T. H., Jääskeläinen, I. P., Möttönen, R., Tarkiainen, A., & Sams, M. E. (2005) · Neuroreport · doi:10.1097/00001756-200502080-00010 · Cited by 306 · see citing works
Early- and Late-Onset Blind Individuals Show Supra-Normal Auditory Abilities in Far-Space
Voss, P., Lassonde, M. C., Gougoux, F., Fortin, M., Guillemot, J., & Leporé, F. (2004) · Current Biology · doi:10.1016/j.cub.2004.09.051 · Cited by 305 · see citing works
Evidence that cochlear-implanted deaf patients are better multisensory integrators
Rouger, J., Lagleyre, S., Fraysse, B., Denève, S., Déguine, O., & Barone, P. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0609419104 · Cited by 300 · see citing works
Compensatory plasticity and cross-modal reorganization following early visual deprivation
Kupers, R., & Ptito, M. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.08.001 · Cited by 293 · see citing works
Cross-Modality Sharpening of Visual Cortical Processing through Layer-1-Mediated Inhibition and Disinhibition
Ibrahim, L. A., Mesik, L., Ji, X., Fang, Q., Li, H.-F., Li, Y.-T., Zingg, B., Zhang, L. I., & Tao, H. W. (2016) · Neuron · doi:10.1016/j.neuron.2016.01.027 · Cited by 287 · see citing works
Do early sensory cortices integrate cross-modal information?
Kayser, C., & Logothetis, N. (2007) · Brain Structure and Function · doi:10.1007/s00429-007-0154-0 · Cited by 319 · see citing works
“…from classical association areas, which reach down to primary and secondary auditory cortex (Barnes and Pandya 1992; Hackett et al. 1998; Romanski et al. 1999; Smiley et al. 2007), to primary and secondary visual areas (Falchier et al. 2002) and to somatosensory cortex (Cappe and Barone 2005).”
Background
Audiovisual Temporal Correspondence Modulates Human Multisensory Superior Temporal Sulcus Plus Primary Sensory Cortices
Noesselt, T., Rieger, J. W., Schoenfeld, M. A., Kanowski, M., Hinrichs, H., Heinze, H., & Driver, J. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.2252-07.2007 · Cited by 282 · see citing works
“Visual stimuli were presented peripherally, which may maximize the opportunity for interplay between auditory and visual cortex (Falchier et al., 2002), and also allowed us to test for any contralaterality in effects for one visual field or the other.”
BackgroundResultInfluential
The newly sighted fail to match seen with felt
Held, R., Ostrovsky, Y., de Gelder, B., Gandhi, T., Ganesh, S., Mathur, U., & Sinha, P. (2011) · Nature Neuroscience · doi:10.1038/nn.2795 · Cited by 284 · see citing works
Cross-modal plasticity for the spatial processing of sounds in visually deprived subjects
Collignon, O., Voss, P., Lassonde, M. C., & Leporé, F. (2008) · Experimental Brain Research · doi:10.1007/s00221-008-1553-z · Cited by 286 · see citing works
“ies showing direct connections between auditory and visual cortical regions in adult sighted monkeys (Cappe and Barone 2005; Clavagnier et al. 2004; Falchier et al. 2002; Rockland and Ojima 2003), suggesting that some exuberant intermodal connections might not be pruned in early infancy, even if their functional purpo…”
BackgroundInfluential
Multisensory Interactions within Human Primary Cortices Revealed by BOLD Dynamics
Martuzzi, R., Murray, M. M., Michel, C. M., Thiran, J., Maeder, P. P., Clarke, S., & Meuli, R. A. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhl077 · Cited by 279 · see citing works
“Multisensory Interactions within Human”
Method
Visual cortex activity in early and late blind people
Burton, H. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-10-04005.2003 · Cited by 270 · see citing works
“Multimodal regions with cortical connections to lower tier somatosensory, auditory, and visual representations occur in posterior parietal, superior and middle temporal, and several extrastriate regions (Andersen et al., 1990; Felleman and Van Essen, 1991; Lewis and Van Essen, 2000; Falchier et al., 2002).”
Background
Multisensory processing via early cortical stages: Connections of the primary auditory cortical field with other sensory systems
Budinger, E., Heil, P. F., Hess, A., & Scheich, H. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.08.035 · Cited by 272 · see citing works
Nonauditory Events of a Behavioral Procedure Activate Auditory Cortex of Highly Trained Monkeys
Brosch, M., Selezneva, E., & Scheich, H. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1571-05.2005 · Cited by 279 · see citing works
“These findings are in line with recent demonstrations of anatomical connections between early auditory and visual cortical areas (Falchier et al., 2002; Rockland and Ojima, 2003) and complement reports of acoustic responses in visual cortical areas 17–19 (Morrell, 1972; Fishman and Michael , 1973;…”
Rapid and Reversible Recruitment of Early Visual Cortex for Touch
Merabet, L. B., Hamilton, R. H., Gottfried Schlaug, A., Swisher, J. D., Kiriakopoulos, E. T., Pitskel, N. B., Kauffman, T., & Pascual‐Leone, Á. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003046 · Cited by 278 · see citing works
“Anatomical support demonstrating the existence of longrange cortico-cortical connections between early sensory cortices in non-human primates has been reported [30–33].”
Background
Multisensory Integration: Flexible Use of General Operations
van Atteveldt, N., Murray, M. M., Thut, G., & Schroeder, C. E. (2014) · Neuron · doi:10.1016/j.neuron.2014.02.044 · Cited by 269 · see citing works
“For example, sensory cortices can influence each other through direct (lateral) anatomical connections (e.g., Falchier et al., 2002), or through feedforward projections from nonspecific (Hackett et al., 2007; Lakatos et al., 2007) or higher-order (Cappe et al., 2007) thalamic nuclei.”
Severe multisensory speech integration deficits in high-functioning school-aged children with autism spectrum disorder (ASD) and their resolution during early adolescence
Foxe, J. J., Molholm, S., Del Bene, V. A., Frey, H.-P., Russo, N. N., Blanco, D., Saint-Amour, D., & Ross, L. A. (2015) · Cerebral Cortex · doi:10.1093/cercor/bht213 · Cited by 263 · see citing works
“…and anatomical studies in nonhuman primates has shown a high degree of direct connectivity between early auditory and visual sensory regions (Falchier et al. 2002, 2010; Molholm et al. 2002; Foxe and Schroeder 2005; Schroeder and Foxe 2005; Smiley and Falchier 2009), and one could certainly…”
Background
Thalamic connections of the auditory cortex in marmoset monkeys: Core and medial belt regions
de la Mothe, L. A., Blumell, S., Kajikawa, Y., & Hackett, T. A. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.20924 · Cited by 270 · see citing works
Sound-induced flash illusion as an optimal percept
Shams, L. B., Ma, W. J., & Beierholm, U. (2005) · Neuroreport · doi:10.1097/01.wnr.0000187634.68504.bb · Cited by 267 · see citing works
Early Cross-Modal Interactions in Auditory and Visual Cortex Underlie a Sound-Induced Visual Illusion
Mishra, J., Martı́nez, A., B, T. J. S. A., & Hillyard, S. A. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.4912-06.2007 · Cited by 255 · see citing works
“Recent anatomical labeling studies in macaques (Falchier et al., 2002; Rockland and Ojima, 2003; Clavagnier et al., 2004) have identified projections from primary auditory (AI) or auditory association cortices to the visual cortex (areas V1 and V2), which could mediate the cross-modal interaction responsible for produ…”
Background
Impairment of auditory spatial localization in congenitally blind human subjects
Gori, M., Sandini, G., Martinoli, C., & Burr, D. C. (2014) · Brain · doi:10.1093/brain/awt311 · Cited by 252 · see citing works
“but not central visual field has strong auditory projections (Falchier et al., 2002), possibly facilitating colonization.”
Background
Visual activation of auditory cortex reflects maladaptive plasticity in cochlear implant users
Sandmann, P., Dillier, N., Eichele, T., Meyer, M. E., Kegel, A., Pascual-Marqui, R. D., Marcar, V. L., Jäncke, L., & Debener, S. (2012) · Brain · doi:10.1093/brain/awr329 · Cited by 259 · see citing works
“connections (Falchier et al., 2002; Rockland and Ojima, 2003; Cappe and Barone, 2005; Hall and Lomber, 2008).”
Comparing the Effects of Auditory Deprivation and Sign Language within the Auditory and Visual Cortex
Fine, I., Finney, E. M., Boynton, G. M., & Dobkins, K. R. (2005) · Journal of Cognitive Neuroscience · doi:10.1162/089892905774597173 · Cited by 256 · see citing works
“Analogously, projections from A1 to V1 have been demonstrated in both kittens (Dehay, Kennedy, & Bullier, 1988; Innocenti, Berbel, & Clarke, 1988; Clarke & Innocenti, 1986) and adult monkeys ( Falchier, Clavagnier, Barone, & Kennedy, 2002 ).”
Long-distance feedback projections to area V1: Implications for multisensory integration, spatial awareness, and visual consciousness
Clavagnier, S., Falchier, A., & Kennedy, H. (2004) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/cabn.4.2.117 · Cited by 249 · see citing works
“A detailed explanation of the histological procedures has been reported elsewhere (Falchier et al., 2002).”
BackgroundResultInfluential
Dual Neural Routing of Visual Facilitation in Speech Processing
Arnal, L. H., Morillon, B., Kell, C. A., & Giraud, A.-L. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.3194-09.2009 · Cited by 241 · see citing works
“1A), a direct corticocortical input to auditory cortex from visual cortex (Falchier et al., 2002; Rockland and Ojima, 2003; Cappe and Barone, 2005).”
Rapid discrimination of visual and multisensory memories revealed by electrical neuroimaging
Murray, M. M., Michel, C. M., de Peralta, R. G., Ortigue, S., Brunet, D., Andino, S. L. G., & Schnider, A. (2003) · NeuroImage · doi:10.1016/j.neuroimage.2003.09.035 · Cited by 244 · see citing works
“At an anatomical level, studies using tracer injections have revealed direct projections to visual areas V1 and V2 from both primary as well as association areas of auditory cortex (Falchier et al., 2002; Rockland and Ojima, 2003).”
Background
Sound Facilitates Visual Learning
Seitz, A. R., Kim, R., & Shams, L. (2006) · Current Biology · doi:10.1016/j.cub.2006.05.048 · Cited by 243 · see citing works
“We chose an auditory-visual task because visual motion stimuli are typically accompanied by sounds and because there exists anatomical evidence in animals [32, 33] and a wealth of human psychophysical [11, 13, 34] and neurophysiological [18, 19, 21, 22, 35] evidence indicating vigorous auditory-visual interactions tha…”
Background
Functional Imaging Reveals Visual Modulation of Specific Fields in Auditory Cortex
Kayser, C., Petkov, C., Augath, M., & Logothetis, N. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.4737-06.2007 · Cited by 280 · see citing works
“Projections from auditory to visual cortex have been demonstrated in the macaque monkey (Falchier et al., 2002; Rockland and Ojima, 2003).”
Multisensory Processes: A Balancing Act across the Lifespan
Murray, M. M., Lewkowicz, D. J., Amedi, A., & Wallace, M. T. (2016) · Trends in Neurosciences · doi:10.1016/j.tins.2016.05.003 · Cited by 242 · see citing works
Diffusion Tensor Imaging Reveals White Matter Reorganization in Early Blind Humans
Shimony, J. S., Burton, H., Epstein, A. A., McLaren, D. G., Sun, S.-W., & Snyder, A. Z. (2005) · Cerebral Cortex · doi:10.1093/cercor/bhj102 · Cited by 233 · see citing works
Neural substrates for dividing and focusing attention between simultaneous auditory and visual events
Johnson, J. A., & Zatorre, R. J. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.02.026 · Cited by 236 · see citing works
Auditory Cortex Tracks Both Auditory and Visual Stimulus Dynamics Using Low-Frequency Neuronal Phase Modulation
Luo, H., Liu, Z., & Poeppel, D. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000445 · Cited by 224 · see citing works
“Importantly, independent anatomical evidence also reveals direct connections among early sensory areas [26,27].”
Attention to Simultaneous Unrelated Auditory and Visual Events: Behavioral and Neural Correlates
Johnson, J. A., & Zatorre, R. J. (2005) · Cerebral Cortex · doi:10.1093/cercor/bhi039 · Cited by 230 · see citing works
“Recent research using retrograde tracers in monkeys showed the existence of projections between peripheral primary visual cortices and auditory primary and secondary areas (Falchier et al., 2002).”
Background
Crossmodal influences on visual perception
Shams, L. B., & Kim, R. S. (2010) · Physics of Life Reviews · doi:10.1016/j.plrev.2010.04.006 · Cited by 229 · see citing works
“Retrograde tracers injected in peripheral V1 and V2 in monkeys indicated input from both the superior temporal polysensory area and the auditory core and belt and caudal parabelt areas [24] (see Fig.”
Statistical Criteria in fMRI Studies of Multisensory Integration
Beauchamp, M. S. (2005) · Neuroinformatics · doi:10.1385/ni:3:2:093 · Cited by 227 · see citing works
“Even areas that are unisensory by definition, such as primary visual cortex, may receive multisensory input (Falchier et al., 2002; Foxe et al., 2002; Schroeder et al., 2003).”
Background
The Thalamocortical Projection Systems in Primate: An Anatomical Support for Multisensory and Sensorimotor Interplay
Cappe, C., Morel, A., Barone, P., & Rouiller, E. M. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhn228 · Cited by 222 · see citing works
“In the monkey, only a sparse direct projection had been reported from AI to V1 (Falchier et al 2002), although such pathway represents probably the anatomical support of the decrease in visual latency of V1 neurons in visuoauditory conditions (Wang et al 2008).”
BackgroundInfluential
Predictive coding and multisensory integration: an attentional account of the multisensory mind
Talsma, D. (2015) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2015.00019 · Cited by 219 · see citing works
“These pathways are thought to connect the sensory cortices, either directly to each other (Falchier et al., 2002), or through cortico-thalamic-cortical pathways (Hackett et al., 2007; Lakatos et al., 2007; van den Brink et al., 2014), suggesting that information can be transferred relatively…”
Background
The multisensory function of the human primary visual cortex
Murray, M. M., Thelen, A., Thut, G., Romei, V., Martuzzi, R., & Matusz, P. J. (2016) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2015.08.011 · Cited by 219 · see citing works
“…processes is based on anatomical evidence for monosynaptic afferents from primary and/or low-level auditory association cortices in monkeys (Falchier et al., 2002, 2009; Rockland and Ojima, 2003; Cappe and Barone, 2005; see also Clarke and Innocenti (1990), Clemo et al. (2008) for evidence…”
Background
Alterations of the visual pathways in congenital blindness
Ptito, M., Schneider, F., Paulson, O. B., & Kupers, R. C. (2008) · Experimental Brain Research · doi:10.1007/s00221-008-1273-4 · Cited by 219 · see citing works
“Cross-connections between low-level cortical areas, including V1, A1 and S1, have been described in the normal brain (Zhou and Fuster 1996; Falchier et al. 2002; Rockland and Ojima 2003) and neuronal activity was recorded in the monkey auditory cortex in response to somatic stimuli in monkeys…”
Background
The development of cortical connections
Price, D. J., Kennedy, H., Dehay, C., Zhou, L., Mercier, M., Jossin, Y., Goffinet, A. M., Tissir, F., Blakey, D., & Molnár, Z. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04620.x · Cited by 215 · see citing works
“…can be defined: (i) those that feed information forward from the cortical inputs to higher levels; and (ii) those that feed information back the other way (Lund et al., 1975; Rockland & Pandya, 1979; Maunsell & van Essen, 1983; Kennedy & Bullier, 1985; Barone et al., 2000; Falchier et al., 2002).”
Background
Impact of blindness onset on the functional organization and the connectivity of the occipital cortex
Collignon, O., Dormal, G., Albouy, G., Vandewalle, G., Voss, P., Phillips, C. L. M., & Leporé, F. (2013) · Brain · doi:10.1093/brain/awt176 · Cited by 218 · see citing works
“…blind suggest that these changes are more ‘epiphenomenal’ in nature in the latter group, and therefore might present less of a hindrance to sight restoration procedures compared to when vision is reacquired after early visual deprivation (Fine et al., 2003; Levin et al., 2010; Dormal et al., 2012).”
Background
A morphometric analysis of auditory brain regions in congenitally deaf adults
Emmorey, K. D., Allen, J. S., Bruss, J., Schenker-Ahmed, N. M., & Damásio, H. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1730169100 · Cited by 215 · see citing works
Multisensory anatomical pathways
Cappe, C., Rouiller, E. M., & Barone, P. (2009) · Hearing Research · doi:10.1016/j.heares.2009.04.017 · Cited by 207 · see citing works
“…anterograde and retrograde tracers in the monkey made it possible to highlight direct projections of the auditory cortex to the primary visual cortex V1 (Falchier et al., 2002), as well as of the associative auditory cortex to the primary and secondary visual areas (Rockland and Ojima, 2003) (Fig.”
BackgroundInfluential
Resolving multisensory conflict: a strategy for balancing the costs and benefits of audio-visual integration
Roach, N. W., Heron, J., & McGraw, P. V. (2006) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2006.3578 · Cited by 210 · see citing works
“Modulation of unimodal signals could be mediated by feedback projections from multimodal regions (Driver & Spence 2000; Meredith 2002), or alternatively, by direct interconnections between primary sensory areas (Falchier et al. 2002; Rockland & Ojima 2003).”
Background
Evidence from Blindness for a Cognitively Pluripotent Cortex
Bedny, M. (2017) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2017.06.003 · Cited by 207 · see citing works
“Such connections outnumber direct projections from other sensory systems, such as primary auditory and somatosensory cortices [66,67].”
Background
Distinct Functional Contributions of Primary Sensory and Association Areas to Audiovisual Integration in Object Categorization
Werner, S., & Noppeney, U. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.5091-09.2010 · Cited by 197 · see citing works
“Indeed, their extensive bidirectional anatomical connectivity to visual and auditory areas renders them ideal for integrating inputs from multiple senses (Neal et al., 1990; Seltzer and Pandya, 1994; Falchier et al., 2002; Rockland and Ojima, 2003).”
Background
Emotional Voice Areas: Anatomic Location, Functional Properties, and Structural Connections Revealed by Combined fMRI/DTI
Ethofer, T., Bretscher, J., Gschwind, M., Kreifelts, B., Wildgruber, D., & Vuilleumier, P. O. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr113 · Cited by 201 · see citing works
“These findings might reflect the observation made in anatomical studies of nonhuman primates that both PAC and higher order auditory cortex are reciprocally connected with early visual areas (Falchier et al. 2002; Rockland and Ojima 2003) and thus represent a possible neural substrate for crossmodal integration in ear…”
Background
Interactions between the Superior Temporal Sulcus and Auditory Cortex Mediate Dynamic Face/Voice Integration in Rhesus Monkeys
Ghazanfar, A. A., Chandrasekaran, C., & Logothetis, N. K. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0541-08.2008 · Cited by 195 · see citing works
“…sulcus (Lewis and Van Essen, 2000), prefrontal cortex (Hackett et al., 1999; Romanski et al., 1999), and even primary and secondary visual cortex (Falchier et al., 2002; Rockland and Ojima, 2003), we, along with Calvert (2001), hypothesized that for face/voice integration, the relevant source of…”
Background
The Mouse Cortical Connectome, Characterized by an Ultra-Dense Cortical Graph, Maintains Specificity by Distinct Connectivity Profiles
Gămănuț, R., Kennedy, H., Toroczkai, Z., Ercsey-Ravasz, M., Essen, D. C. V., Knoblauch, K., & Burkhalter, A. (2018) · Neuron · doi:10.1016/j.neuron.2017.12.037 · Cited by 202 · see citing works
The role of visual experience for the neural basis of spatial cognition
Pasqualotto, A., & Proulx, M. J. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2012.01.008 · Cited by 192 · see citing works
“Studies on primates have reported evidence for primary sensory cortices receiving multisensory afferents (Falchier et al., 2002; Murata et al., 1965; Rockland and Ojima, 2003).”
Background
Cortical connections of the auditory cortex in marmoset monkeys: Core and medial belt regions
de la Mothe, L. A., Blumell, S., Kajikawa, Y., & Hackett, T. A. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.20923 · Cited by 188 · see citing works
Assessing the Role of the ‘Unity Assumption’ on Multisensory Integration: A Review
Chen, Y., & Spence, C. J. (2017) · Frontiers in Psychology · doi:10.3389/fpsyg.2017.00445 · Cited by 191 · see citing works
“…compared to central visual field (e.g., Charbonneau et al., 2013; Gleiss and Kayser, 2013; Chen et al., submitted), which is thought to be partly attributable to the more extensive neural connectivity across sensory-dominant areas in the periphery (Falchier et al., 2002; Rockland and Ojima, 2003).”
Background
The representation of space near the body through touch and vision
Macaluso, E., & Maravita, A. (2010) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2009.10.010 · Cited by 181 · see citing works
Multisensory processing in children with autism: high-density electrical mapping of auditory-somatosensory integration
Russo, N., Foxe, J. J., Brandwein, A. B., Altschuler, T., Gomes, H., & Molholm, S. (2010) · Autism Research · doi:10.1002/aur.152 · Cited by 180 · see citing works
“Crucially, evidence from anatomical studies have shown that there are direct long range connections between the various sensory cortical areas [Falchier et al., 2002; Rockland & Ojima, 2003] and it may be the disruption of this form of connectivity that leads to impairment of early MSI in ASD.”
Background
Multisensory convergence in auditory cortex, I. Cortical connections of the caudal superior temporal plane in macaque monkeys
Smiley, J. F., Hackett, T. A., Ulbert, I., Karmas, G., Lakatos, P., Javitt, D. C., & Schroeder, C. E. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21325 · Cited by 181 · see citing works
“There was also some evidence that the connection between the auditory belt and V2 is reciprocal, in that small numbers of retrogradely labeled cells were found in V2 in layers III and V after belt injections (Falchier et al., 2002; Rockland and Ojima, 2003).”
Background
Improvement of visual contrast detection by a simultaneous sound
Lippert, M., Logothetis, N. K., & Kayser, C. (2007) · Brain Research · doi:10.1016/j.brainres.2007.07.050 · Cited by 180 · see citing works
Anatomical mechanisms and functional implications of multisensory convergence in early cortical processing.
Schroeder, C., Smiley, J., Fu, K., McGinnis, T., O'Connell, M. N., & Hackett, T. (2003) · International Journal of Psychophysiology · doi:10.1016/s0167-8760(03)00120-x · Cited by 193 · see citing works

Projection from Visual Areas V2 and Prostriata to Caudal Auditory Cortex in the Monkey
Falchier, A., Schroeder, C. E., Hackett, T. A., Lakatos, P., Nascimento‐Silva, S., Ulbert, I., Karmos, G., & Smiley, J. F. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp213 · Cited by 130 · see citing works
Auditory cortex projections target the peripheral field representation of primary visual cortex
Hall, A. J., & Lomber, S. (2008) · Experimental Brain Research · doi:10.1007/s00221-008-1485-7 · Cited by 69 · see citing works
Functional organisation of auditory inputs to visual cortex
Egea-Weiss, A. (2025) · UCL Discovery (University College London)
Audiovisual interactions in the Cat: Direct cortical projections from the posterior auditory field to primary visual cortex
Hall, A. J., Mellott, J. G., & Lomber, S. G. (2010) · Journal of Vision · doi:10.1167/7.9.867
Connections of Auditory and Visual Cortex in the Prairie Vole (Microtus ochrogaster): Evidence for Multisensory Processing in Primary Sensory Areas
Campi, K. L., Bales, K. L., Grunewald, R., & Krubitzer, L. A. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp082 · Cited by 90 · see citing works

Authors: Falchier, A., Clavagnier, S., Barone, P., & Kennedy, H.
Affiliations: Inserm (FR)
ORCID: Falchier, Arnaud
Clavagnier, Simon
Barone, Pascal
Kennedy, Henry
Venue: The Journal of Neuroscience
Publisher: Society for Neuroscience
Published: 2002-07-01
Volume: 22
Issue: 13
Pages: 5749-5759
ISSN: 0270-6474 (ISSN-L)
1529-2401
DOI: 10.1523/jneurosci.22-13-05749.2002
PMC: PMC6758216
OpenAlex: W2134188685
Cited by: 892
References: 82
Citations by year: 2026: 13 · 2025: 20 · 2024: 32 · 2023: 25 · 2022: 33 · 2021: 28 · 2020: 24 · 2019: 30 · 2018: 37 · 2017: 32 · 2016: 34 · 2015: 44 · 2014: 43 · 2013: 68 · 2012: 53
FWCI: 34.18
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Journal of Neuroscience (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Topics: Social Sciences › Psychology › Experimental and Cognitive Psychology › Multisensory perception and integration
Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
Life Sciences › Neuroscience › Cognitive Neuroscience › Tactile and Sensory Interactions
Keywords: primary visual cortex, area 17, multimodal integration, extrastriate cortex, retrograde tracing, primate visual cortex, auditory-visual interaction
MeSH terms: Animals, Auditory Cortex, Coloring Agents, Injections, Macaca fascicularis, Neurons, Species Specificity, Temporal Lobe, Visual Cortex, Visual Fields, Visual Pathways

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