The effect of handedness on the shape of the central sulcus
Graphical abstract
Highlights
► The hand knob position can shift along the central sulcus according to individuals. ► Manifold learning can quantify the shape of the central sulcus. ► The left hand knob is sited more dorsally in dextrals than in sinistrals. ► Unlike sulcus size, the location of the hand knob is unchanged by forced dextrality. ► Cortical morphology holds a record of both innate biases and early experience.
Introduction
The folding pattern of the human cerebral cortex is intriguingly complex. While folding is variable among individuals, an overall species-specific pattern is preserved. The mechanisms that determine individual folding pattern variations are still unclear (Lefèvre and Mangin, 2010, Lohmann et al., 2008, Régis et al., 2005, Toro and Burnod, 2005, Van Essen, 1997, Welker, 1988, White et al., 2010). In addition to genetic factors, there are environmental influences on folding dynamics during development that contribute to individualized folding patterns (Kochunov et al., 2010b, Le Goualher et al., 2000, Leonard et al., 2006). Neuroscientists and neurosurgeons have been intrigued by this variability and its impact on cortical architectonics, developmental disturbances and specific behaviors (Fischl et al., 2008, Leonard et al., 2006, Ono et al., 1990, Welker, 1988).
The central sulcus is one of the most stable and prominent folds of the human brain; it marks the functional separation between motor and somatosensory areas. An inverted homunculus is represented in each of these areas (Penfield and Boldrey, 1937). The hand motor region maps onto a characteristic notch of the sulcus, commonly referred to as the “hand knob” (Sastre-Janer et al., 1998, Yousry et al., 1997). Although the central sulcus is one of the simplest cortical folds its size and shape vary substantially across individuals and between hemispheres (see Fig. 1).
Several studies have revealed links between certain morphological characteristics of the central sulcus and handedness (Amunts et al., 2000, Cykowski et al., 2008, Hopkins et al., 2010, Klöppel et al., 2010, Mangin et al., 2004a, White et al., 1994). They consistently report increased folding of the central sulcus of the dominant hemisphere resulting in a deeper or longer sulcus than in the non-dominant hemisphere. This asymmetry could arise from genetically determined early developmental factors, or from late brain plasticity. Several experiments (Draganski et al., 2004, Granert et al., 2011, Hyde et al., 2009, Scholz et al., 2009) have provided consistent evidence that prolonged learning or specific training can result in mesoscopic structural changes in specific brain structures implicated functionally by training. These experience-related changes in regional brain morphology occur not only during brain maturation but persist throughout life.
In order to clarify the origin of central sulcus asymmetry we previously studied the effect of switching hand use during childhood (Klöppel et al., 2010). In adults who retain right or left lateralisation of handedness, asymmetry of the central sulcus is in favor of the dominant (contralateral) hemisphere. Asymmetry manifests as a greater surface area of the dominant sulcus quantified using the morphometry toolbox of BrainVISA (http://brainvisa.info) (Mangin et al., 2004a). Acquisition of dextrality by innate sinistrals forced to write with the right hand results in a transfer of this asymmetry such that the brains of acquired and natural dextrals become similar. This result strongly supports the hypothesis that the asymmetry of folding observed in adults is largely environmentally induced, reflecting considerable local structural plasticity.
In this study, we set out to identify handedness-related features of central sulcus morphology that are less likely to be use-dependent, implying a resistance to late plasticity. We examined first to which extent the 3D shape of the central sulcus differs between consistent dextrals and sinistrals. Then we studied the sulcal shape of individuals with acquired dextrality. Our hypothesis was that forced dextrality will modify the shape of the central sulcus less than its size because its shape is sculpted early during human development (appearing during the 21st gestational week (Feess-Higgins and Laroche, 1987)) and so is less readily modifiable post-partum.
We compared the shapes of the central sulci of the previous study (Klöppel et al., 2010) using a new algorithmic approach sensitized to the problem. Isomap, a modern multidimensional scaling technique (Tenenbaum et al., 2000), was used to quantify central sulcus shape.
Section snippets
Material
We examined 34 forced dextrals (mean age 40, range 24–56 years; 22 males, 12 females) and compared them with 23 consistent age and sex matched natural dextrals (mean age 34, range 22–59 years; 17 males, 6 females) and 18 similar natural sinistrals (mean age 36, range 25–56 years; 12 males, 6 females). Individuals were only labelled as a forced dextral if the subjects and their parents clearly recollected that writing commenced with the left hand at school, but was switched to the right. Subjects
Central sulcus representations
The central sulci of each subject were extracted from the MRI data using the Morphologist toolbox of BrainVisa [http://brainvisa.info] (Mangin et al., 2004a, Perrot et al., 2011). The software represents the central sulcus by a set of 3D points that sample the medial surface of the cerebrospinal fluid filling the fold (see Fig. 1). An expert confirmed that the software correctly identified the central sulcus. To control for the influence of variable brain size the central sulcus representations
The hand knob shift
Plotting the 3D shapes of all (left and right) central sulci along the Isomap axis reveals a simple shape characteristic that has been captured by the manifold; the position of the “hand knob” moves dorsally from one side to the other side of the axis (see Fig. 4). Local averages of sulcus shapes show that as the “hand knob” representation shifts dorsally along the Isomap axis, a second distinct lower “knob” appears. In the following, we call the shape at the left extremity of the axis a
Discussion
Many alternative shape similarity measures could have been experimented to perform our study. We have evaluated in previous work the potential of sophisticated shape descriptors called 3D moment invariants for representing the shape of the cortical sulci (Mangin et al., 2004b, Sun et al., 2007). They rely on coordinate moments which are often used for pattern recognition. However, complex tensor calculus is required to achieve invariance to orientation when dealing with 3D objects. Therefore,
Acknowledgments
We thank S. Dehaene and G. Dehaene-Lambertz for their comments on the manuscript.
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