Variations of cingulate sulcal organization and link with cognitive performance

Abstract

The sulcal morphology of the human medial frontal cortex has received marked interest because of (1) its remarkable link with the functional organization of this region, and (2) observations that deviations from 'normal' sulcal morphological variability correlate with the prevalence of some psychiatric disorders, cognitive abilities, or personality traits. Unfortunately, background studies on environmental or genetic factors influencing the ontogenesis of the sulcal organization in this region are critically lacking. We analysed the sulcal morphological organization in this region in twins and non-twin siblings, as well as in control subjects for a total of 599 subjects from the Human Connectome Project. The data first confirm significant biases in the presence of paracingulate sulci in left vs right hemispheres in the whole population (twin: p < 2.4.10^-9; non-twin: p < 2.10^-6) demonstrating a clear general laterality in human subjects. Second, measures of similarity between siblings and estimations of heritability suggest significant environmental factors, in particular in-womb environment, and weak additive genetic factors influencing the presence of a paracingulate sulcus. Finally, we found that relationships between sulcal organization and performance in cognitive, motor, and affective tests depend on the twin status (Twins versus Non-twins). These results provide important new insights to the issue of the significance of sulcal organization in the human medial frontal cortex.

Figure 1

Examples of sulcal morphology in the medial wall. On the left panel, the left (LH) and right (RH) hemispheres of 2 typical subjects displaying only a cingulate sulcus (CGS, yellow). On the middle panel, the left (LH) and right (RH) hemispheres of 2 typical subjects displaying a PROMINENT paracingulate sulcus (PCGS, blue). On the right panel, the left (LH) and right (RH) hemispheres of 2 typical subjects displaying a PRESENT PCGS. Note that a PRESENT PCGS can be observed in the ACC only (top right panel) or in the MCC only (bottom right panel) or at the interface between the ACC and MCC (not shown).

Figure 2

Proportions of subjects with or without a paracingulate sulcus (PCGS). (a) Proportion of subjects with no PCGS in either side (none), one pcgs on the right (R) or on the left (L), or a PCGS in both hemispheres (both), and for each population (Control: group of single individuals, SING: group of not twin siblings, MZ: monozygotic twins, DZ: dizygotic twins). (b) Proportion of subjects with a PCGS on the left (top) or right (bottom) hemisphere according to handedness and family status. Note the higher incidence of a PCGS on the left hemisphere for both left-handed and right-handed subjects.

Figure 3

Occurrence of paracingulate sulcus (PCGS). (a) Three levels of PCGS are identified: Prominent, Present, and Absent (see Methods). The figure shows the proportion of each case in the different groups of individuals. (b) Proportion of individuals with at least one PCGS in one hemisphere.

Figure 4

Average scores in the PMAT24 (a) and DDisc (b) tests in the Non-Twin and the Twin populations displaying a leftward asymmetry (left panels). On the right panels are displayed the distributions (count) of scores for the Non-Twin and the Twin populations displaying a leftward asymmetry.

Figure 5

Similarity of patterns in the medial wall in siblings. (a) Proportion of cases with identical patterns (with or without a PCGS) for both hemispheres (left panel) and individually for the left and right hemispheres (panels on the right). Data are presented for the 3 groups of siblings. Note a higher occurrence of similarity for monozygotic twins, which is particularly related to a higher similarity for the right hemisphere. (b) Simulations. Frequency of similarity between the hemispheric pattern of 2 randomly sampled individuals in simulated populations with various basal frequencies of sulcus occurrence. At 0 percent of sulcus in the population the probability to find similar patterns (no sulcus) in the population is on average maximal (100%). Same for a population in which a PCGS would be present in 100% of cases. If the likelihood of a PCGS is at 50% (x axis) then the probability of having two individuals with the same pattern in the same hemisphere is 50%. At that level, the variance is maximal. The mean probability of similarity is indicated with the red curve. Real data from the human database is represented by single points overlapped on the simulation to show their relationship to randomly generated data. Disks and triangles represent data (percent of similarity) for the left and right hemispheres respectively. Colors represent the different groups of siblings.