Anatomical Evidence of Multimodal Integration in Primate Striate Cortex

“At the anatomical level, it is possible that this recruitment reflects the unmasking of permanent dormant horizontal connections between the auditory and visual cortices, as recently demonstrated in normal adult primates [24].”

“The need for finer definition of cortical areas becomes more pressing if we consider that even histologically homogeneous areas, such as the primary sensory areas, or area MT, show some variation in their cortical input (Krubitzer and Kaas, 1990; Falchier et al., 2002; Palmer and Rosa, 2006).”

“…areas of the dorsal extrastriate association cortex have been shown to have cortical connections to both primary auditory and visual areas (Falchier et al., 2002; Felleman and Van Essen, 1991) and may provide a route for auditory stimuli to reach visual areas such as V1 (see Sadato et…”

“Alternatively, it could relate to the fact that, in the primate brain, there are projections from the auditory cortex to portions of the visual cortex that represent peripheral visual space (Falchier et al, 2002).”

“…from other primary sensory cortices in the opossum (Kahn et al., 2000; Karlen et al., 2006; Dooley et al., 2013) and rodents (Budinger et al., 2000, 2006, 2008; Campi et al., 2010; Charbonneau et al., 2012; Henschke et al., 2014) than in primates (Falchier et al., 2002; Clavagnier et al., 2004).”

“Although cross-modal projections between primary auditory and visual areas have been documented in monkeys (Falchier et al. 2002; Rockland and Ojima 2003), the present study identified only a few retrogradely labeled neurons in gyral locations that may correspond to A1.”

“2007) or direct ‘‘feedforward’’ afferences arising from the auditory cortex, as suggested by anatomical data gathered in monkeys (Falchier et al. 2002).”

“Anatomical tracer studies reported direct axonal connections between auditory and early visual cortex in non-human primates (Falchier et al., 2002; Rockland and Ojima, 2003; Clavagnier et al., 2004; Bizley et al., 2007).”

“That is, previous studies have shown that the visual cortex can be activated by auditory input [50,86,87] and that there are direct anatomical connections between the superior temporal and occipital regions in primates [88] and humans [89,90].”

“Although studies in sighted animals have clearly established the presence of long-range cortico-cortical connections between early sensory cortices (Schroeder & Foxe, 2005; Clavagnier, Falchier, & Kennedy, 2004; Rockland & Ojima, 2003; Falchier, Clavagnier, Barone, & Kennedy, 2002 ), most evidence suggests that in cas…”

“These auditory projections are denser in V2 than in V1, are found in portions of V1 and V2 representing the more peripheral and lower visual field (Rockland and Ojima 2003), and their density increases as a function of retinal eccentricity in area V1 (Falchier et al. 2002).”

“Indeed, connections between the auditory and visual cortex have been found in monkeys (Falchier et al., 2002) and humans (Eckert et al., 2008) and attended auditory prime words have been shown to activate areas in the primary visual cortex (Cate et al., 2009).”

“Finally, there may be a direct auditory projection to visual cortex that is normally dormant in sighted subjects; such a projection exists in normal macaque monkeys (Falchier et al. 2002).”

“Second, the localization of our effects is consistent with prior hemodynamic imaging studies both for the initial effect within right STS (e.g. Belin et al., 2000) and also for the subsequent effect within the left inferior frontal gyrus (e.g. Fecteau et al., 2004; Cohen et al., 2006).”

“Using tracer injections, both Falchier and colleagues 31 and Rockland and Ojima 32 demonstrated connections between auditory and primary visual areas (V1).”

“Neuroanatomical methods [20] complement these findings and help to understand the underlying connectivity and where association of the senses takes place.”

“More recently, direct projections from the auditory cortex to peripheral V1 have also been showed in the primate (Falchier et al., 2002).”

“Tracing studies in animals also demonstrate direct cortical connections between primary or early sensory cortices in primates (Falchier et al., 2002; Rockland & Ojima, 2003; Clavagnier et al., 2004), cats (Hall & Lomber, 2008) and rodents (Budinger et al., 2000, 2006; Campi et al., 2010).”

“, 2009) but also direct axonal projections between primary sensory cortices that have been documented across multiple species and areas (Falchier et al., 2002; Budinger et al., 2006; Hall and Lomber, 2008; Sieben et al., 2013; Stehberg et al., 2014; Zingg et al., 2014; Sieben et al., 2015).”

“…however, with previous fMRI reports showing strong engagement of peripheral visual regions during auditory tasks (Cate et al. 2009) and aligns with anatomical evidence of direct connections between the primary auditory region and peripheral V1 regions (Falchier et al. 2002; Cappe and Barone 2005).”

“Efferent projections to early visual cortex, particularly peripheral V1, originate in part from auditory cortex, including the superior temporal sulcus (STS) (Doty 1983; Falchier et al. 2002; Rockland and Ojima 2003).”

“Furthermore, the core and parabelt portions of the auditory cortex have anatomical connections with visual areas V1 and V2 (Rockland & Ojima, 2003; Falchier, Clavagnier, Barone, & Kennedy, 2002 ).”

“…in humans (Ghazanfar and Schroeder, 2006; Kayser et al., 2008; Schroeder and Lakatos, 2009; Murray et al., 2016) and in nonhuman primates (Falchier et al., 2002; Lakatos et al.,2007; Schroeder and Lakatos, 2009)(Lakatos et al. 2005, 2007, suggesting an evolutionarily conserved mechanism…”

“Thus, as in other species where at best a weak reciprocal projection from Au1 to V2L has been reported (Miller and Vogt 1984; Falchier et al. 2002; Rockland and Ojima 2003; Budinger et al. 2006; Bizley et al. 2007; Hall and Lomber 2008; Meredith et al. 2009), this connection is likely to be minor…”

“, 1999; Lewis and Van Essen, 2000) and/or feedforward projections from principle primary sensory areas or subcortical structures (Falchier et al., 2002; Clavagnier et al., 2004; Cappe and Barone, 2005).”

“Recent observations demonstrate that the visual cortex receives hetero-modal projections from primary sensory cortices (auditory: Falchier et al. 2002; Rockland and Ojima 2003; somatosensory: Guipponi et al. submitted for publication).”

“This is supported by previous work in demonstrating connections between the STS and auditory/visual areas [Beer et al., 2011; Falchier et al., 2002; Rockland and Pandya, r 5598 r 1981], and that the STS does indeed have a “patchy” organization containing both AV and unisensory areas [Beauchamp et…”

“However, a growing number of studies have shown direct connectivity between the auditory and visual cortices without additional connections through mediating neurons in multisensory regions (Falchier et al., 2002; Rockland and Ojima, 2003; Clavagnier et al., 2004).”

“A second, more hypothetical candidate pathway, is the direct long-range connectivity between the primary visual and somatosensory cortices (Falchier et al., 2002; Rockland and Ojima, 2003), a role for which is suggested by recent studies indicating the presence of cross-modal interactions at…”

“This is the most likely reason that the projections from auditory areas to area V1 were not detected before 2002 (Falchier et al., 2002; Rockland and Ojima, 2003).”

“…effects might arise from interactions in brain regions that have traditionally been considered to be unisensory (in light of Murray et al. 2005), but do not operate via previously described corticocortical pathways between these early sensory cortices (in light of Falchier et al. 2002).”

“(2007), such as long-range corticocortical connections from multimodal parietal areas (Rockland and Ojima, 2003), or from somatosensory or other primary sensory cortices (Falchier et al., 2002; Cappe and Barone, 2005), plastic changes in subcortical pathways (e.”

“In the monkey brain, there is evidence for direct anatomical projections between sensory-specific brain regions (Falchier et al., 2002; Rockland & Ojima, 2003; Cappe & Barone, 2005), and also some evidence of a functional role of these connections in cross-modal processing (e.g. Foxe et al., 2002;…”

“Falchier et al. (2002) identified auditory projections from the core and parabelt areas of the auditory cortex as well as from the polysensory area of the temporal lobe into V1.”

“While there is evidence for direct connections between early visual cortex and auditory cortex (Bizley et al., 2007, Falchier et al., 2002 and Rockland & Ojima, 2003) and studies indicate the possibility of direct connections of auditory and somatosensory cortices (Fu et al., 2003 and Hackett et…”

“…(Cate et al., 2009; Azevedo et al., 2015) and stems from direct connectivity between primary auditory cortices and primarily peripheral retinotopic locations of V1 (Rockland and Van Hoesen, 1994; Falchier et al., 2001; Falchier et al., 2002; Rockland and Ojima, 2003; Borra and Rockland, 2011).”

“For example, tracing experiments in non-human primates [129,130] and rodents [119,132,134] have shown that the primary visual cortex (V1) is connected to low-level auditory areas, including the primary auditory cortex (A1).”

“…be intrinsically multimodal through early subcortical convergence (Ettlinger and Wilson, 1990), synchronized neural oscillation (Senkowski et al., 2007), and/or direct cortico–cortical connections (Falchier et al., 2002; Clavagnier et al., 2004; Small et al., 2013; based on monkey and rodent data).”

“With respect to direct cortico-cortical connectivity between auditory cortices (primary and nonprimary) and visual areas (V1/V2), studies using retrograde tracing showmonosynaptic projections from auditory cortices as well as areas of the superior temporal sulcus to V1 (Falchier et al., 2002).”

“…and vision are in line with neuropsychological findings illustrating that the primary visual cortex (V1) is also sensitive to auditory information (Falchier et al. 2002; Giard & Peronnet, 1999) and that audio-visual stimulation increases activity in multimodal areas but decreases activity in the…”

“…some parts of auditory cortex can receive convergent input from other senses [e.g., see Ghazanfar et al., 2005; Lakatos et al., 2007; see also Bizley et al., 2007; Kayser et al., 2007, 2008; Schroeder and Foxe, 2005] via direct or indirect anatomical connections [see Falchier et al., 2002, 2010].”

“Falchier et al. (2002) showed that the peripheral representation of V1 in cynomolgus monkey received connections, albeit sparsely, from core and association areas of auditory cortex.”

“…sparse direct connectivity between sensory areas or top-down modulation from higher order association areas such as IPS (Lewis and Van Essen 2000b; Falchier et al. 2002; Macaluso, Driver, et al. 2003; Rockland and Ojima 2003; Musacchia and Schroeder 2009; Werner and Noppeney 2010b; Beer et al.…”

“In rodents, primary and secondary visual and auditory cortices share direct anatomical connections (Budinger et al., 2006; Budinger and Scheich, 2009; Campi et al., 2010; Cappe and Barone, 2005; Falchier et al., 2002; Miller and Vogt, 1984; Paperna and Malach, 1991; Rockland and Ojima, 2003) and auditory inputs to pri…”

“In another heavily cited study in macaque, A1 projections to V1 were reported to represent ~0.034% of non-visual cortical inputs that, on average, occur as 0.21 neurons/section (calculated from Table 1, Falchier et al., 2002).”

“Falchier et al. 2002; Rockland and Ojima 2003), as did findings that sensory integration could already occur in hierarchically early regions during the initial feedforward afferent sweep (e.g.”

“It has to be taken into account, however, that brief noise bursts constitute salient stimulation that likely triggers cross-modal attentional reorienting processes (Cate et al., 2009; Falchier et al., 2002).”

“This raises the possibility that the TRN, together with cross-modal connections between sensory cortical areas (Falchier et al., 2002; Rockland & Ojima, 2003; Lurilli et al., 2012) and innervation from higher-order thalamic nuclei (Jones, 1998; Lakatos et al.”

“This model was supported by tracer studies in monkeys that have demonstrated visual input to what was previously thought to be purely auditory cortex (Schroeder & Foxe, 2002) and direct projections from auditory cortex to primary and secondary visual cortex (Falchier et al., 2002; Rockland & Ojima, 2003).”

“For electrophysiological experiments the sections were processed for myelin using the protocol described by Gallyas (1979).”

“In the sighted brain, existing cortico-cortical connections between auditory and visual cortices [81–84] might play a role for the integration of spatial information coming from different modalities or for the inhibition of visual cortices during nonvisual tasks in order to minimize potential effect of interference wi…”

“Concordantly, direct anatomical connections between visual and auditory cortex have been found in macaques, gerbils and humans (Beer et al., 2011; Falchier et al., 2002; Henschke et al., 2015).”

“On the other hand, visual areas such as V1 or V2 receive direct inputs from the core auditory cortex (Smiley & Falchier, 2009; Falchier et al., 2002).”

“In addition, the primary visual cortex receives projections from the core and parabelt areas of the auditory cortex (Falchier et al. 2002).”

“An alternative pathway is that the visual areas receive nonvisual sensory information through corticooccipital connections between these sensory modalities [140, 152, 153].”

“Thus, the main objective of this paper is to stress out the importance of studying the GABAergic networks in animal models of cross-modal plasticity for future experimental work because information on the possible mechanisms involved is presently lacking.”

“Anatomical studies in animals have identified direct, monosynaptic projections between primary and immediately adjacent auditory cortices and primary visual cortices (Falchier et al., 2002; Rockland and Ojima, 2003; Clavagnier et al., 2004; Cappe and Barone, 2005), which are complemented by electrophysiological and fM…”

“Several retrograde labeling studies verified that extrastriate cells project to the primary auditory cortex (monkey: Falchier et al., 2002, Cappe and Berone, 2005; ferret: Bizley et al., 2007; cat: Clemo et al., 2008; gerbil: Budinger et al., 2008; Budinger and Scheich, 2009).”