Anatomical Evidence of Multimodal Integration in Primate Striate Cortex

“There are numerous brain areas and pathways for multisensory interactions, ranging from the brain stem [14] to early sensory cortical areas [13,15], to association and other cortical areas [12], including feedforward [16] and feedback pathways [ 17 ,18].”

“, 1998b; Jones, 1998), (2) direct lateral projections from low-level nonauditory cortices (Falchier et al., 2002; Rockland and Ojima, 2003; Cappe and Barone, 2005), and (3) feedback projections from higher-order multisensory regions of neocortex (Hackett et al.”

“The G29 × 29 subgraph suggests an unexpectedly high incidence of unidirectional links.”

“…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).”

“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).”

“and non-human adult primates have demonstrated direct connections between auditory and visual cortical area”

“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”

“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).”

“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).”

“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.”

“, 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.”

“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].”

“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).”

“Using retrograde tracing in monkeys, Falchier et al. [ 24 ] found direct connections from primary auditory cortex (A1) to regions in primary visual cortex (V1).”

“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).”

“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.”

“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…”

“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).”

“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 &…”

“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).”

“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.”

“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).”

“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).”

“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.,…”

“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).”

“, 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.”

“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…”

“[37] reported direct inputs to peripheral V1 from the auditory cortex, inputs that included the core primary auditory area (A1)”

“[26] identified projections from core and parabelt auditory cortex into parts of V1 corresponding to the representation of the peripheral visual field.”

“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].”

“…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).”

“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.”

“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…”

“Multisensory Interactions within Human”

“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).”

“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;…”

“Anatomical support demonstrating the existence of longrange cortico-cortical connections between early sensory cortices in non-human primates has been reported [30–33].”

“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.”

“…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…”

“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…”

“but not central visual field has strong auditory projections (Falchier et al., 2002), possibly facilitating colonization.”

“connections (Falchier et al., 2002; Rockland and Ojima, 2003; Cappe and Barone, 2005; Hall and Lomber, 2008).”

“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 ).”

“A detailed explanation of the histological procedures has been reported elsewhere (Falchier et al., 2002).”

“1A), a direct corticocortical input to auditory cortex from visual cortex (Falchier et al., 2002; Rockland and Ojima, 2003; Cappe and Barone, 2005).”

“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).”

“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…”

“Projections from auditory to visual cortex have been demonstrated in the macaque monkey (Falchier et al., 2002; Rockland and Ojima, 2003).”

“Importantly, independent anatomical evidence also reveals direct connections among early sensory areas [26,27].”

“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).”

“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.”

“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).”

“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).”

“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…”

“…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…”

“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…”

“…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).”

“…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).”

“…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.”

“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).”

“Such connections outnumber direct projections from other sensory systems, such as primary auditory and somatosensory cortices [66,67].”

“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).”

“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…”

“…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…”

“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).”

“…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).”

“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.”

“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).”