The architecture of functional lateralisation and its relationship to callosal connectivity in the human brain

Abstract

Functional lateralisation is a fundamental principle of the human brain. However, a comprehensive taxonomy of functional lateralisation and its organisation in the brain is missing. Here, we report the first complete map of functional hemispheric asymmetries in the human brain, reveal its low dimensional structure, and its relationship with structural inter-hemispheric connectivity. Our results suggest that the lateralisation of brain functions is distributed along four functional axes: symbolic communication, perception/action, emotion, and decision-making. The similarity between this finding and recent work on neurological symptoms give rise to new hypotheses on the mechanisms that support brain recovery after a brain lesion. We also report that cortical regions showing asymmetries in task-evoked activity have reduced connections with the opposite hemisphere. This latter result suggests that during evolution, brain size expansion led to functional lateralisation to avoid excessive conduction delays between the hemispheres.

Fig. 1

Low-dimensional structure of functional lateralisation. Embedded in two-dimensional (a) and three-dimensional (b) space according to similarity in their lateralisation profile (MATLAB interactive 3D file available as Supplementary Data 1). See Supplementary Figures 1 and 2 for the spatial embedding of all Neurosynth terms. Here, to provide a graphical summary of all results reported in the section, we plotted the significantly lateralised components maps, named by the highest-loading terms (Supplementary Table 3), in place of the actual Neurosynth terms (Supplementary Table 1)

Fig. 2

Archetypes of functional lateralisation. The maps correspond to the symbolic communication (a), perception/action (b), emotion (c) and decision (d) axes. Upper panel corresponds to the lateral view, middle panel to the medial view and lower panel to the cerebellum view (lateral and posterior views) of the reconstructed pattern of activations. VWFA visual word form area, WA Wernicke area, VFC ventral frontal cortex, IFg inferior frontal gyrus, MFg middle frontal gyrus, TPJ temporo-parietal junction, IPL inferior parietal lobule, STg superior temporal gyrus, IPs intraparietal sulcus, SS somatosensory cortex, M motor cortex, FEF frontal eye field, PTL posterior temporal lobe, PFC prefrontal cortex, SMA supplementary motor area, preSMA presupplementary motor area, ACC anterior cingulate cortex, BF basal forebrain (maps are available as Supplementary Data 2–5)

Fig. 3

Lateralisation and inter-hemispheric connectivity. a Tractography of the corpus callosum in a representative subject of our study (top left); cortical projection of the corpus callosum derived from axonal tracing in monkeys (top right); cortical projections of the corpus callosum derived from tractography in the participants of our study (bottom). b Histogram of the difference between lateralised and non-lateralised regions in the corpus callosum axonal water fraction, averaged across participants. c Histogram of the difference between lateralised and non-lateralised regions in the corpus callosum probability of connection. The measure was calculated as the proportion of participants in which a connection exists between brain’s voxels and corpus callosum to the overall HCP sample size. d Dimensional relationship between the degree of functional lateralisation and the corpus callosum probability of connectivity. LOF lateral orbitofrontal cortex, SS somatosensory cortex, STG superior temporal gyrus, AT anterior temporal, V1 primary visual area, M primary motor area, PC posterior cingulate gyrus, MC middle cingulate gyrus, AC anterior cingulate gyrus, PH parahippocampal gyrus