Amodal Processing in Human Prefrontal Cortex

Abstract

Information enters the cortex via modality-specific sensory regions, whereas actions are produced by modality-specific motor regions. Intervening central stages of information processing map sensation to behavior. Humans perform this central processing in a flexible, abstract manner such that sensory information in any modality can lead to response via any motor system. Cognitive theories account for such flexible behavior by positing amodal central information processing (e.g., "central executive," Baddeley and Hitch, 1974; "supervisory attentional system," Norman and Shallice, 1986; "response selection bottleneck," Pashler, 1994). However, the extent to which brain regions embodying central mechanisms of information processing are amodal remains unclear. Here we apply multivariate pattern analysis to functional magnetic resonance imaging (fMRI) data to compare response selection, a cognitive process widely believed to recruit an amodal central resource across sensory and motor modalities. We show that most frontal and parietal cortical areas known to activate across a wide variety of tasks code modality, casting doubt on the notion that these regions embody a central processor devoid of modality representation. Importantly, regions of anterior insula and dorsolateral prefrontal cortex consistently failed to code modality across four experiments. However, these areas code at least one other task dimension, process (instantiated as response selection vs response execution), ensuring that failure to find coding of modality is not driven by insensitivity of multivariate pattern analysis in these regions. We conclude that abstract encoding of information modality is primarily a property of subregions of the prefrontal cortex.

Short-Term Memory for Space and Time Flexibly Recruit Complementary Sensory-Biased Frontal Lobe Attention Networks

“…These methods may have been critical to resolving multiple distinct visual-biased and auditory-biased attention regions where prior studies found responses independent of sensory modality. Consistent with our findings, a recent multivariate analysis study indicated that posterior lateral frontal cortex contains information about sensory modality, but this study did not identify specific visual-biased and auditory-biased frontal cortical areas (Tamber-Rosenau et al, 2013). …”

“…While one recent multivariate analysis indicated that posterior lateral frontal cortex contains information reflecting input sensory modality (Tamber-Rosenau et al, 2013), prior human univariate functional magnetic resonance imaging (fMRI) studies of vision and audition either point to shared multi-sensory structures in lateral frontal cortex (Lewis et al, 2000; Johnson and Zatorre, 2006; Ivanoff et al, 2009; Karabanov et al, 2009; Tark and Curtis, 2009; Tombu et al, 2011; Braga et al, 2013) or report a lateral frontal cortical bias for only one modality (for example, see Crottaz-Herbette et al, 2004; Jantzen et al, 2005; Rämä and Courtney, 2005; Salmi et al, 2007), which could reflect differences in task difficulty rather than sensory modality. Studies in non-human primates have reported distinct areas in lateral frontal cortex that are biased toward audition or vision in anatomical connectivity and/or functional response (for example, see Barbas and Mesulam, 1981; Petrides and Pandya, 1999; Romanski and Goldman-Rakic, 2002; Romanski, 2007).…”

Sensory-biased attention networks in human lateral frontal cortex revealed by intrinsic functional connectivity

“…Duncan, 2010; Duncan & Owen, 2000). Tamber-Rosenau et al (2013) reported evidence for modality sensitivity in posterior LFC using a multivariate analysis approach, however their results did not reveal sensory-biases at the level of individual ROIs. In contrast to many past studies, our previous work used individual subject analyses to reveal the fine-grained pattern of modality bias in LFC (Michalka et al, 2015).…”

“…However, consistent with non-human primate studies, two recent human fMRI studies (Michalka et al, 2015; Mayer et al, 2017) and one study combining functional and structural connectivity (Braga et al, 2017) found that distinct regions of LFC exhibit strong biases for vision or audition. Another study also reported sensitivity to sensory modality within LFC (Tamber-Rosenau et al, 2013). …”

Central attention is serial, but midlevel and peripheral attention are parallel—A hypothesis

“…Second, regions of the prefrontal cortex—including anterior cingulate, frontal operculum, and anterior insula—are activated across a very wide variety of cognitive tasks (Duncan, 2010), consistent with central attention that is required for any non-automatic task, and seem to change control settings at task-level, rather than trial-level, intervals (Dosenbach et al, 2008). Third, subsets of the lateral prefrontal cortex and anterior insula are invariant to perceptual modality and to representational format (i.e., location versus shape) (Tamber-Rosenau, Dux, Tombu, Asplund, & Marois, 2013; Tamber-Rosenau, Newton, et al, in revision), consistent with highly abstract processes or representations involved in central attention. These latter results are especially suggestive of the serial nature of central attention because if a representation does not contain sensory information but instead only represents abstract, task-relevant information, one would predict interference or cross-talk between simultaneous representations (Huestegge & Koch, 2009; Navon & Miller, 1987), consistent with the need for serial processing.…”