Abstract

According to contemporary views, the lateral frontal cortex is organized along a rostro-caudal functional axis with increasingly complex cognitive/behavioral control implemented rostrally, and increasingly detailed motor control implemented caudally. Whether the medial frontal cortex follows the same organization remains to be elucidated. To address this issue, the functional connectivity of the 3 cingulate motor areas (CMAs) in the human brain with the lateral frontal cortex was investigated. First, the CMAs and their representations of hand, tongue, and eye movements were mapped via task-related functional magnetic resonance imaging (fMRI). Second, using resting-state fMRI, their functional connectivity with lateral prefrontal and lateral motor cortical regions of interest (ROIs) were examined. Importantly, the above analyses were conducted at the single-subject level to account for variability in individual cingulate morphology. The results demonstrated a rostro-caudal functional organization of the CMAs in the human brain that parallels that in the lateral frontal cortex: the rostral CMA has stronger functional connectivity with prefrontal regions and weaker connectivity with motor regions; conversely, the more caudal CMAs have weaker prefrontal and stronger motor connectivity. Connectivity patterns of the hand, tongue and eye representations within the CMAs are consistent with that of their parent CMAs. The parallel rostral-to-caudal functional organization observed in the medial and lateral frontal cortex could likely contribute to different hierarchies of cognitive-motor control.

Highlights

  • Prevailing theories about the functional organization of the frontal lobe suggest that the lateral frontal cortex is organized along a rostral-to-caudal axis of behavioral/cognitive control where higher level cognitive processing is implemented rostrally and motor control processing, caudally (Petrides, 2005a,b; Koechlin and Summerfield, 2007; Badre and D’Esposito, 2009)

  • Based on individual cingulate morphology, subjects could be divided into 3 main groups (Table 1): Group 1 included 10 subjects who had a paracingulate sulcus (PCGS) in one hemisphere but not the other

  • The analysis revealed a significant cingulate motor areas (CMAs) x ROIline interaction (Figure 4D, df = 3, F = 66.3, p < 2 × 10−16, ANOVA with CMAs and ROIline as factors), which indicates that the linear trends in connectivity within the rostral-to-caudal axis of lateral frontal cortex differed between the CMAs: a negative linear trend was observed for RCZa, positive slopes were observed for the other CMAs

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Summary

Introduction

Prevailing theories about the functional organization of the frontal lobe suggest that the lateral frontal cortex is organized along a rostral-to-caudal axis of behavioral/cognitive control where higher level cognitive processing is implemented rostrally and motor control processing, caudally (Petrides, 2005a,b; Koechlin and Summerfield, 2007; Badre and D’Esposito, 2009). The most rostral region, CMAr, in contrast with the more caudal CMAd and CMAv, has denser connections with the pre-SMA, orbital, medial and lateral prefrontal cortex, weaker connections with the dorsal premotor and primary motor cortex, and fewer but a more complex pattern of corticospinal projections (Dum and Strick, 1991; Luppino et al, 1993; He et al, 1995; Hatanaka et al, 2003; Morecraft et al, 2004, 2012; Petrides and Pandya, 2006) These findings suggest that, along a rostro-caudal axis, CMAs show graded relationships with prefrontal (decreasing connectivity) and motor regions (increasing connectivity). These connectivity trends corroborate that the anterior CMA is more implicated in higher-order cognitive functions in association with the prefrontal cortex and the posterior CMAs in motor functions associated with the motor, premotor cortex and spinal cord

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