Separable networks for top-down attention to auditory non-spatial and visuospatial modalities

Abstract

A central question for cognitive neuroscience is whether there is a single neural system controlling the allocation of attention. A dorsal frontoparietal network of brain regions is often proposed as a mediator of top-down attention to all sensory inputs. We used functional magnetic resonance imaging in humans to show that the cortical networks supporting top-down attention are in fact modality-specific, with distinct superior fronto-parietal and fronto-temporal networks for visuospatial and non-spatial auditory attention respectively. In contrast, parts of the right middle and inferior frontal gyri showed a common response to attentional control regardless of modality, providing evidence that the amodal component of attention is restricted to the anterior cortex.

Auditory and visual connectivity gradients in frontoparietal cortex

“…It is unclear whether the same frontoparietal set of putative “multimodal” regions is activated during the cognitive processing of information from all sensory modalities. However, a dorsal–ventral split between visual and auditory regions has been hypothesized previously based on both cognitive neuroimaging and histological evidence [Braga et al, 2013b; Bushara et al, 1999; Kong et al, 2014; Rauschecker and Scott, 2009; Romanski, 2004]. In this study, we provide evidence that this distinction is detectable in humans using both structural and task‐independent functional imaging.…”

“…Specifically, we propose that dorsal frontoparietal activity is more likely to represent visual processes, while ventral frontoparietal activity is more likely to represent auditory processing. This work adds weight to recent theories that auditory and visual attention are subserved by separable dorsal and ventral networks [Braga et al, 2013b; Braga et al, 2016; Degerman et al, 2006; Kong et al, 2014; Salmi et al, 2007; Seydell‐Greenwald et al, 2014] and suggests that further work is necessary to disentangle the precise role of frontoparietal activity in multimodal processing.…”

“…A prominent theory is that dorsal regions are activated for visual top–down attention, while ventral regions are driven by stimulus properties [Corbetta et al, 2002]. There is controversy over whether this same pattern is generalizable to non‐visuospatial tasks [Alho et al, 2015; Braga et al, 2013b; Gottlieb and Snyder, 2010; Kong et al, 2014; Salmi et al, 2009]. It is unclear whether the same frontoparietal set of putative “multimodal” regions is activated during the cognitive processing of information from all sensory modalities.…”

“…Searchlights were passed across the whole brain, but for clarity and consistency with our hypothesis in the present analysis the results were restricted to the prefrontal and parietal cortices by post‐hoc masking. Dual regression was used to reveal the whole‐brain FC patterns of these 10 components [Leech et al, 2012; Braga et al, 2013a, 2013b; Braga and Leech, 2015] as follows. Briefly, a time series was extracted from each of the 10 components in a spherical ROI (first regression).…”

“…Several studies have reported activity in a dorsal frontoparietal network that overlaps with the visual system during auditory stimulus anticipation, processing and attention shifts [Bharadwaj et al, 2014; Downar et al, 2000; Krumbholz et al, 2009; Langner et al, 2011; Lee et al, 2012; Linden et al, 1999; Mayer et al, 2006; Shomstein and Yantis, 2004; Watkins et al, 2007; Wu et al, 2007]. In contrast, there is increasing evidence that visual and auditory attention are subserved by different networks [Braga et al, 2013b; Bushara et al, 1999; Degerman et al, 2006; Kong et al, 2014; Maeder et al, 2001; Salmi et al, 2007; Seydell‐Greenwald et al, 2014]. For example, Bushara et al [1999] showed that while visual spatial localization recruits dorsal regions such as the SPL and FEF, auditory localization recruits ventral frontoparietal regions along the inferior parietal lobe (IPL) and inferior frontal gyrus (IFG).…”