Cortical and subcortical projections to primary visual cortex in anophthalmic, enucleated and sighted mice

Abstract

The purpose of this study was to identify and compare the afferent projections to the primary visual cortex in intact and enucleated C57BL/6 mice and in ZRDCT/An anophthalmic mice. Early loss of sensory-driven activity in blind subjects can lead to activations of the primary visual cortex by haptic or auditory stimuli. This intermodal activation following the onset of blindness is believed to arise through either unmasking of already present cortical connections, sprouting of novel cortical connections or enhancement of intermodal cortical connections. Studies in humans have similarly demonstrated heteromodal activation of visual cortex following relatively short periods of blindfolding. This suggests that the primary visual cortex in normal sighted subjects receives afferents, either from multisensory association cortices or from primary sensory cortices dedicated to other modalities. Here cortical afferents to the primary visual cortex were investigated to determine whether the visual cortex receives sensory input from other modalities, and whether differences exist in the quantity and/or the structure of projections found in sighted, enucleated and anophthalmic mice. This study demonstrates extensive direct connections between the primary visual cortex and auditory and somatosensory areas, as well as with motor and association cortices in all three animal groups. This suggests that information from different sensory modalities can be integrated at early cortical stages and that visual cortex activations following visual deprivations can partly be explained by already present intermodal corticocortical connections.

Unimodal primary sensory cortices are directly connected by long-range horizontal projections in the rat sensory cortex

“…Several studies have shown that primary sensory cortices can respond to multisensory inputs (Clavagnier et al, 2004; Schroeder and Foxe, 2005; Shams et al, 2005; Ghazanfar and Schroeder, 2006; Kayser et al, 2007; Martuzzi et al, 2007; Mishra et al, 2007; Senkowski et al, 2007; Wang et al, 2008; Sperdin et al, 2009; Koelewijn et al, 2010; Raij et al, 2010). The underpinning anatomical substrate of multisensory integration was always assumed to be projections through white matter (Bizley et al, 2007; Lakatos et al, 2007; Bizley and King, 2009; Cappe et al, 2009; Larsen et al, 2009; Musacchia and Schroeder, 2009; Charbonneau et al, 2012; Laramee et al, 2013). Our study raises the possibility that at least part of multisensory interactions could be carried out by a diffuse projection system that directly connects unimodal cortices.…”

Frizzled3 is required for the development of multiple axon tracts in the mouse central nervous system

“…It would also be interesting to examine the anatomy and physiology of neurons in the thalamus and somatosensory cortex in Cdx1-Cre;Fz3 CKO/− mice to explore the fate of territories that normally process somatosensory information from the trunk and limbs. One might anticipate that there would be a large scale remapping of these territories analogous to the remapping of visual cortex in humans or animals that are congenitally blind (33)(34)(35).…”

Strain differences of the effect of enucleation and anophthalmia on the size and growth of sensory cortices in mice

“…The absence of auditory activation of the primary visual cortex in the enucleated mice is surprizing considering that the visual cortex in intact and enucleated C57Bl/6J mice and ZRDCT/An mice receives similar extensive cortical auditory and somatosensory afferents (Charbonneau et al, 2012) as well as indirect corticocortical projections from the auditory cortex (Laramée et al, 2011). Moreover, auditory activation of the visual cortex was reported in enucleated hamsters (Izraeli et al, 2002), rats (Piché et al, 2007), opossum (Kahn and Krubitzer, 2002) and cats (Kahn and Krubitzer, 2002;Yaka et al, 2000Yaka et al, , 1999.…”

“…There is also evidence for crossmodal plasticity in that the visual cortex is activated by auditory stimuli in ZRDCT/An mice . This auditory activity could originate from a projection from the inferior colliculus to the lateral geniculate nucleus (Chabot et al, 2008) and from direct cortical connections between the auditory and visual cortex (Charbonneau et al, 2012).…”