Auditory Attention Activates Peripheral Visual Cortex

Abstract

BackgroundRecent neuroimaging studies have revealed that putatively unimodal regions of visual cortex can be activated during auditory tasks in sighted as well as in blind subjects. However, the task determinants and functional significance of auditory occipital activations (AOAs) remains unclear.Methodology/Principal FindingsWe examined AOAs in an intermodal selective attention task to distinguish whether they were stimulus-bound or recruited by higher-level cognitive operations associated with auditory attention. Cortical surface mapping showed that auditory occipital activations were localized to retinotopic visual cortex subserving the far peripheral visual field. AOAs depended strictly on the sustained engagement of auditory attention and were enhanced in more difficult listening conditions. In contrast, unattended sounds produced no AOAs regardless of their intensity, spatial location, or frequency.Conclusions/SignificanceAuditory attention, but not passive exposure to sounds, routinely activated peripheral regions of visual cortex when subjects attended to sound sources outside the visual field. Functional connections between auditory cortex and visual cortex subserving the peripheral visual field appear to underlie the generation of AOAs, which may reflect the priming of visual regions to process soon-to-appear objects associated with unseen sound sources.

Corticocortical Connections Mediate Primary Visual Cortex Responses to Auditory Stimulation in the Blind

“…The auditory discrimination task we used led to significant activation in bilateral medial geniculate nucleus, primary auditory cortex, and primary visual cortex in both groups. The activation of primary visual cortex in response to auditory stimulation in the sighted might seem surprising at first sight, but note that previous studies have shown nonvisual responses in primary visual cortex of sighted participants (Maeder et al, 2001;Saito et al, 2005;Cate et al, 2009). More generally, both monkey and human studies have shown that traditional views of unimodal primary cortices have to be reconsidered, as primary cortices also respond to stimuli from other modalities, although to a lesser degree (for review, see Driver and Noesselt, 2008).…”

“…However, if one considers that the visual cortex can also be activated by auditory stimuli in sighted if the task requires high levels of attention (Cate et al, 2009), the results seem more alike: possibly, the visual cortex of blind people is predominantly recruited during demanding tasks or when relevant information is supplied (Röder et al, 1996). This would explain why resting-state studies (no attentional demands) failed to find coupling (Liu et al, 2007;Yu et al, 2008), whereas activation-based effective-connectivity studies did find enhanced coupling in the blind (Fujii et al, 2009;present study).…”

Projection from Visual Areas V2 and Prostriata to Caudal Auditory Cortex in the Monkey

“…This is suggested by experiments in ferrets where visual responses in auditory cortex were clearly tuned to visual stimuli located near the contralateral surface of the head (Bizley et al 2007). Similarly, in humans, attention to the spatial location of auditory stimuli causes activation of visual cortex at the region of peripheral field representation (Cate et al 2009). …”

“…Indeed, caudal auditory areas are considered to be part of a dorsal auditory stream, based on their connections with spatial domains of the frontal lobe and their role in sound spatial localization (Rauschecker 1998;Romanski, Bates, et al 1999;Romanski, Tian, et al 1999;Romanski and Goldman-Rakic 2002;Rauschecker and Tian 2004). Recent findings from fMRI connectivity analysis in humans showed that auditory cortex has a distinct relationship with the peripheral representation of visual field in the calcarine sulcus (Eckert et al 2008;Cate et al 2009). Together, the findings from monkey and other species emphasize the involvement of dorsal visual and auditory streams in low-level cross-modal convergence.…”

“…However, there appears to be some effect of attention as the visual--auditory interactions are more robust in nonanesthetized monkeys (Kayser et al 2007) and in humans during tasks that require attention (Cate et al 2009). Overall, the findings in humans and monkeys suggest that visual input to auditory cortex may be relevant to several cognitive processes, including enhancement of spatial, temporal, and object-related multisensory perception.…”