Anatomical Evidence of Multimodal Integration in Primate Striate Cortex

“Several laboratories have now independently identified monosynaptic projections between these cortices in nonhuman primates (Falchier et al., 2002; Rockland and Ojima, 2003; Cappe and Barone, 2005).”

“This may be achieved through awakening of dormant horizontal connections between these cortices, as recently demonstrated in adult primates (Falchier et al., 2002).”

“Tracer studies revealed direct connections from auditory cortices to primary and secondary visual areas, with stronger projections from higher auditory areas (Falchier et al., 2002, 2010; Rockland and Ojima, 2003).”

“, 2007) and neuroanatomical (Barnes and Pandya, 1992; Hackett et al., 1998; Falchier et al., 2002; Cappe and Barone, 2005) studies.”

“Furthermore, they tend to have anatomical characteristics of “backward” or modulatory projections.(36,37) From the vantage point of neuronal physiology, an area could therefore display unimodal features in the forward or dominant mode of neurotransmission but not necessarily in the physiologically more latent backward…”

“512 Current Biology 26, 509–514, February 22, 2016 a2016 Elsevier ity between sensory areas [29], or top-down influences from higher-order association cortices [30].”

“…the source of these direct inputs, but candidate sources include long-range corticocortical connections from multimodal parietal areas (Rockland and Ojima 2003), somatosensory processing areas, or other primary sensory cortices (Cappe and Barone 2005; Clavagnier et al. 2004; Falchier et al. 2002).”

“…by neuroanatomical and neurophysiological studies, which have revealed that the striate cortex receives neuronal projections from auditory cortices, whichmay facilitate multimodal integration (Clavagnier et al., 2004; Falchier et al., 2002; Rockland and Ojima, 2003; Schroeder and Foxe, 2005).”

“…modulations in LGB and its condition-dependent coupling with other areas might in principle potentially involve early visual cortex, which is anatomically linked with posterior STS (Falchier et al., 2002; Ghazanfar et al., 2005; Kayser and Logothetis, 2009) and reciprocally connected with LGB.”

“Even early cortical areas, such as V1 and A1, that have been considered exclusively involved with one sense, have been shown to have multisensory influences (Falchier et al., 2002; Ghazanfar & Schroeder, 2006; Stein & Meredith, 1993).”

“…and considering the absence of rIPS contribution to this function in the blind, we suggested that sounds may reach the OC in blind subjects either via subcortical connections (Piche et al., 2007) or direct “feedforward” afferent projections arising from the auditory cortex (Falchier et al., 2002).”

“While these results cannot speak to the exact mechanism by which multisensory training mediates visual learning, anatomical studies have found evidence for input to lower level visual areas both directly from primary and parabelt auditory cortex [25,26], and also from the superior temporal polysensory area [25].”

“Recently, tracer studies in primates (Falchier et al., 2002; Rockland and Ojima, 2003) have revealed direct anatomical connections between early auditory and primary visual areas.”

“More recent findings in the macaque suggest a lifelong presence of connections from primary auditory cortex to peripheral area V1, as well as from a polysensory temporal region to peripheral V1 (Falchier et al., 2002).”

“Furthermore, the discovery of heteromodal connections directly linking areas involved in different sensory modalities could be the anatomical support of such interactions [19-21].”

“…higher-order multisensory regions (Molholm et al., 2006) and the presence of extensive bidirectional anatomical connectivity with early sensory cortices (Falchier et al., 2002; Neal et al., 1990; Rockland and Ojima, 2003; Seltzer and Pandya, 1994), are clearly consistent with this possibility.”

“However, auditory projections to visual cortex were later demonstrated in very young kittens (Innocenti and Clarke, 1984), and more recent anatomical data with more sensitive tracers showed that a direct projection from auditory to visual cortex also exists in adult rhesus monkeys (Falchier et al., 2002; Rockland and…”

“At the time, theorizing about speech perception was unrelated to evidence about visual speech perception (lipreading1), even though there were reports available in the literature showing that speech can be perceived visually.”

“We now know that, not only higher cortex, but also probably most of the primary sensory cortex, is polysensory (Falchier et al., 2002; Rockland and Ojima, 2003; Clavagnier et al., 2004; Budinger et al., 2006; Driver and Noesselt, 2008; Ptito et al., 2008; Collignon et al., 2009).”

“The requisite anatomy for such interactions has been well documented (Falchier et al., 2002, 2010; Rockland and Ojima, 2003; Cappe and Barone, 2005) and may even include a corticothalamocortical loop (Cappe et al., 2007a, 2009c; Hackett et al., 2007).”

“Anatomical tracer studies of nonhuman primates demonstrate the existence of direct pathways between primary sensory areas [Cappe and Barone, 2005; Clavagnier et al., 2004; Falchier et al., 2002; Rockland and Ojima, 2003; Rockland and Van Hoesen, 1994].”

“…V1 has been demonstrated to have connections with area prostriata (marmoset monkeys; Yu et al. 2012), and with auditory areas (cynomolgus monkeys; Falchier et al. 2002), the great majority of connections are restricted to unimodal extrastriate visual areas (reviewed in: Felleman and Van Essen…”

“Tracing studies provide structural evidence for all of these routes [(a) Karlen et al., 2006; (b1) Falchier et al., 2002; (b2) Rockland and Ojima, 2003] but do not allow to determine their functional relevance.”

“…to demonstrate projections from primary auditory cortex, auditory association areas and the superior temporal polysensory area (STP) to the area of primary visual cortex representing the peripheral visual field (Clavagnier et al., 2004; Falchier et al., 2002; Rockland and Van Hoesen, 1994).”

“V1 has been shown to have direct connections with auditory regions in the monkey (Falchier et al., 2002) and it is possible that direct collateral connections drive this effect.”

“More surprisingly, the early onset of th nteractions suggests a fairly direct pathway mediating nteractions, as opposed to a second-order effect due m o feedback modulations from higher-order cortical ar ecent neuroanatomical studies in monkey have rep irect projections from primary and parabelt auditory co nd STP to…”

“Projections from auditory cortex to primary visual cortex have been reported in the adult primate (Falchier et al., 2002; Clavagnier et al., 2004), but there have been no reports yet of direct projections between auditory cortex and MT.”

“, superior colliculus and the pulvinar nucleus of the thalamus) [10–12], and possibly direct lateral connections between unimodal cortices [13].”

“However, anatomical studies have shown that areas in the calcarine fissure representing peripheral vision may be more strongly connected with the auditory cortex than areas representing the fovea (Falchier et al., 2002; Wang et al., 2008).”

“They found direct axonal connections between auditory cortex and the primary and secondary visual cortex (Falchier et al. 2002; Rockland and Ojima 2003).”

“For example, the visual perception pathway is connected to the auditory cortex [73], [74].”

“Visual and auditory cortices directly interact both anatomically and functionally (Bizley et al., 2007; Clavagnier et al., 2004; Falchier et al., 2002; Morrell, 1972; Shams et al., 2002; Zangenehpour and Zatorre, 2010) resulting in responses to visual and auditory stimuli in both regions…”

“A testable hypothesis is that this kind of recruitment could bemost pronounced in peripheral parts of early visual cortex of blind individuals, as peripheral areas are primary receivers of auditory and, potentially, high-level information [15, 16].”

“, 2016) that relay external (Falchier et al., 2002; Fishman and Michael, 1973; Iurilli et al., 2012) and internal signals (Fu et al.”

“know that the representation of the near-periphery (10–20 eccentricity) in the primary visual area (V1) receives projections from the auditory cortex, and that these same areas have limited or no projections to the central representation in V1 (Falchier et al., 2002; Rockland & Ojima, 2003).”

“Although several studies have argued that sensory integration occurs in secondary sensory or association cortex (Jones & Powell, 1970; Bavelier & Neville, 2002) or in frontal cortex (Rizzolatti, Riggio, Dascola & Umilta, 1980), recent evidence has pointed to the presence of top-down inputs from these association regio…”

“Subcortically, the SC and the basal ganglia as well as association and other cortical regions including the superior temporal sulcus, the parietal, premotor and prefrontal cortex [79–82] are also implicated in MSI, including feedback as well as feedforward anatomical projections [83,84].”

“…projections between sensory cortices have been identified and possibly have a behavioral function regarding stimuli in the periphery of the visual field (Falchier et al., 2002, 2010), we assume that they are too sparse to specify the contentspecific patterns of activity that we have observed.”

“These cortices share both structural and functional connections as demonstrated in both primates (Falchier et al., 2002; Rockland and Ojima, 2003) and humans (Beer et al., 2011; Eckert et al., 2008) which provides an underlying network substrate to facilitate this neuronal communication.”

“Our results are in line with recent evidence that sensory cortical areas receive input from multiple sensory modalities early in development (Wallace et al. 2004; Falchier et al. 2002; Rockland and Ojima 2003).”

“Such earlyMSI processes putatively rely on long-range connections implicating primary sensory cortical areas (Falchier et al., 2002).”

“in the macaque, with the majority of connections terminating in regions that respond to visual stimuli in the peripheral field [10].”

“For example, within-area heterogeneity has been reported for V1 and V2 in the macaque, where central vs peripheral parts of the visual field representation differ in their connectivity with parietal and temporal cortex (Baizer et al., 1991; Falchier et al., 2002); in primary motor cortex, the head and leg regions are…”

“…audio-visual pathways have been identified (for a review, see Cappe et al., 2012), including direct pathways between lower-level unimodal regions (Falchier et al., 2002; Rockland and Ojima, 2003) and indirect hierarchical feedback connections from higher-level multisensory regions to the…”

“…monosynaptic projections identified between unisensory (including primary) cortices raise the possibility of interactions during early stimulus processing stages (Falchier et al., 2002, 2010; Rockland and Ojima, 2003; Cappe and Barone, 2005; Cappe et al., 2009a; see also Beer et al., 2011).”

“1999a, 1999b), auditory cortex also receives efferent connections from multisensory nuclei of the thalamus (Hackett, 2007; Smiley and Falchier, 2009), and is reciprocally connected via direct connections to early visual areas (Falchier et al., 2002; Rockland and Ojima, 2003; Smiley and Falchier, 2009).”

“Some evidence also points to sparse projections from A1 to V1 (Falchier et al., 2002), however, the connection between auditory association areas and V1/V2 appears to be much stronger.”

“Which (anatomical) inputs might shape neuronal response modulation in auditory cortex? How are diverse latencies compensated for? Do effects ‘build up’? in early sensory cortex are also complemented by feedback connections from higher brain areas such as the STS and IPS [60,74–76], and one role for these connections i…”

“These connections have not been seen for higher visual areas and are more numerous in regions corresponding to more peripheral parts of the visual field (Clavagnier et al., 2004; Falchier et al., 2002; Rockland and Ojima, 2003).”

“…(Colmenero et al., 2004; Loke and Song, 1991; Stevens and Neville, 2006). vealed direct connections between auditory and visual cortices for peripheral portions of the visual field (e.g., Falchier et al., 2002), thus offering a possible neural substrate for this spatially selective enhancement.”

“There is feasibility for such a pathway insofar as non-human primate anatomical tracer studies reveal direct connections between auditory and visual sensory cortices (Falchier et al., 2002; Rockland & Ojima, 2003; Cappe & ª The Authors (2007).”

“…tracer studies in normally seeing primates have shown the existence of direct connections going from caudal auditory areas to peripheral V1/V2 (Falchier et al., 2002; Rockland and Ojima, 2003), suggesting that the necessary pathways to mediate crossmodal plasticity likely exist prior to…”

“Given the evidence for auditory input into the visual cortex (e.g., Falchier, Clavagnier, Barone, & Kennedy, 2002 ), however, we are still left with the need to explain why multisensory neurons in the auditory system produce sensory enhancement in loudness, whereas multisensory neurons in the visual system do not prod…”

“Accordingly, CM shares properties of the neighboring temporo-parietotemporal area (Tpt), in which multisensory interactions have been clearly documented (Falchier et al. 2002; Leinonen et al. 1980).”

“In multisensory systems, this is particularly problematic as sensory pathways interconnect at 210 cortical and subcortical levels [22-25,50,51].”

“Indeed, anatomical studies have demonstrated that cortical sensory areas are connected both directly (Falchier et al., 2002; Rockland and Ojima, 2003; Hall and Lomber, 2008; Allman et al., 2009; Meredith and Allman, 2012) as well as via multimodal cortical areas (Cappe and Barone, 2005).”

“How does occipital cortex come to respond to speech? According to one hypothesis, spoken language reaches occipital circuits from primary auditory areas or the auditory nucleus of the thalamus (Miller and Vogt, 1984; Falchier et al., 2002; Clavagnier et al., 2004).”

“Moreover, axonal tracing studies indicate that numerous direct connections exist between primary auditory and visual cortex (Bizley et al., 2007; Driver and Noesselt, 2008; Falchier et al., 2002; Ghazanfar and Schroeder, 2006; Innocenti et al., 1988; Leinweber et al., 2017; Zingg et al., 2014), suggesting that auditor…”