Sensory-Biased and Multiple-Demand Processing in Human Lateral Frontal Cortex

• Published in: The Journal of neuroscience Vol. 37; no. 36; pp. 8755 - 8766
• Main Authors: Noyce, Abigail L., Cestero, Nishmar, Michalka, Samantha W., Shinn-Cunningham, Barbara G., Somers, David C.
• Format: Journal Article
• Language: English
• Published: United States Society for Neuroscience 06.09.2017
• Subjects: Adult; Attention; Attention - radiation effects; Auditory Perception - physiology; Auditory tasks; Coexistence; Cognition; Cognition - physiology; Cognitive ability; Cognitive tasks; Cortex (frontal); Cues; Demand; Female; Frontal Lobe - physiology; Functional magnetic resonance imaging; Functional morphology; Humans; Information processing; Male; Nerve Net - physiology; Perceptual Masking - physiology; Sensory integration; Somatosensory cortex; Specialization; Visual cortex; Visual perception; Visual Perception - physiology; Visual tasks; audition; fMRI; vision; multiple demand network; working memory; lateral frontal cortex
• ISSN: 0270-6474; 1529-2401; 1529-2401
• DOI: 10.1523/JNEUROSCI.0660-17.2017

The functionality of much of human lateral frontal cortex (LFC) has been characterized as "multiple demand" (MD) as these regions appear to support a broad range of cognitive tasks. In contrast to this domain-general account, recent evidence indicates that portions of LFC are consistently selective for sensory modality. Michalka et al. (2015) reported two bilateral regions that are biased for visual attention, superior precentral sulcus (sPCS) and inferior precentral sulcus (iPCS), interleaved with two bilateral regions that are biased for auditory attention, transverse gyrus intersecting precentral sulcus (tgPCS) and caudal inferior frontal sulcus (cIFS). In the present study, we use fMRI to examine both the multiple-demand and sensory-bias hypotheses within caudal portions of human LFC (both men and women participated). Using visual and auditory 2-back tasks, we replicate the finding of two bilateral visual-biased and two bilateral auditory-biased LFC regions, corresponding to sPCS and iPCS and to tgPCS and cIFS, and demonstrate high within-subject reliability of these regions over time and across tasks. In addition, we assess MD responsiveness using BOLD signal recruitment and multi-task activation indices. In both, we find that the two visual-biased regions, sPCS and iPCS, exhibit stronger MD responsiveness than do the auditory-biased LFC regions, tgPCS and cIFS; however, neither reaches the degree of MD responsiveness exhibited by dorsal anterior cingulate/presupplemental motor area or by anterior insula. These results reconcile two competing views of LFC by demonstrating the coexistence of sensory specialization and MD functionality, especially in visual-biased LFC structures. Lateral frontal cortex (LFC) is known to play a number of critical roles in supporting human cognition; however, the functional organization of LFC remains controversial. The "multiple demand" (MD) hypothesis suggests that LFC regions provide domain-general support for cognition. Recent evidence challenges the MD view by demonstrating that a preference for sensory modality, vision or audition, defines four discrete LFC regions. Here, the sensory-biased LFC results are reproduced using a new task, and MD responsiveness of these regions is tested. The two visual-biased regions exhibit MD behavior, whereas the auditory-biased regions have no more than weak MD responses. These findings help to reconcile two competing views of LFC functional organization.