New human-specific brain landmark: The depth asymmetry of superior temporal sulcus

Abstract

Identifying potentially unique features of the human cerebral cortex is a first step to understanding how evolution has shaped the brain in our species. By analyzing MR images obtained from 177 humans and 73 chimpanzees, we observed a human-specific asymmetry in the superior temporal sulcus at the heart of the communication regions and which we have named the "superior temporal asymmetrical pit" (STAP). This 45-mm-long segment ventral to Heschl's gyrus is deeper in the right hemisphere than in the left in 95% of typical human subjects, from infanthood till adulthood, and is present, irrespective of handedness, language lateralization, and sex although it is greater in males than in females. The STAP also is seen in several groups of atypical subjects including persons with situs inversus, autistic spectrum disorder, Turner syndrome, and corpus callosum agenesis. It is explained in part by the larger number of sulcal interruptions in the left than in the right hemisphere. Its early presence in the infants of this study as well as in fetuses and premature infants suggests a strong genetic influence. Because this asymmetry is barely visible in chimpanzees, we recommend the STAP region during midgestation as an important phenotype to investigate asymmetrical variations of gene expression among the primate lineage. This genetic target may provide important insights regarding the evolution of the crucial cognitive abilities sustained by this sulcus in our species, namely communication and social cognition.ince Geschwind and Levitsky's (1) first attempt to identify a specifically human cortical landmark, the identification of unique features of the human brain that might explain the cognitive success of the human species has remained elusive so that anatomical targets still do not exist to inform the search for genetic mutations contributing to the human cognitive phenotype. Because hemispheric asymmetry and language processing are fundamental human traits, the perisylvian language areas have been especially scrutinized for such markers, but until now none has been forthcoming. In particular, the reported asymmetries in the planum temporale and the inferior frontal region are not as robust as initially thought (1-3) and also are observed, albeit often less marked, in other primates (4). However, we show here that asymmetry of the superior temporal sulcus (STS), at the core of the human communication system, represents a species-specific perisylvian anatomical marker. This finding is consistent with functional brain imaging studies that have emphasized the importance of STS not only for language processing in the left hemisphere but also for social communication in the right hemisphere (5, 6). Notably, in the left hemisphere a hierarchy of areas sensitive to increased levels of acoustical complexity is observed along superior temporal regions and become specifically linguistic along the STS (7, 8), whereas in the right hemisphere the presence of areas involved in voice and face recognition, gaze perception, and theory o...

Meta-analytic connectivity modeling of the human superior temporal sulcus

“…Importantly, inter-hemispheric volumetric differences likely do not impact the main results, as the main results are the comparisons between STS subregion coactivation maps within the same hemisphere. Others have reported a depth asymmetry of the STS, where the right STS has been shown to have a deeper sulcus in the middle to posterior regions (Ochiai et al 2004; Bonte et al 2013; Leroy et al 2015), regardless of handedness (Leroy et al 2015), and overall more variability across individuals as compared to the left STS (Bonte et al 2013). With respect to handedness, neither the lpba40 max probabilistic atlas (Shattuck et al 2008) nor the AAL atlas (derived from a single subject; Tzourio-Mazoyer et al 2002) reports handedness.…”

Relation between clinical risk factors, early cortical changes, and neurodevelopmental outcome in preterm infants

“…The STS remains asymmetrical in adults, suggesting an underlying difference in structure rather than a delay in folding to be responsible for this early asymmetry (Van Essen, 2005;Ochiai et al 2004;Leroy et al 2015).…”

Quasi-isometric length parameterization of cortical sulci: Application to handedness and the central sulcus morphology

“…A subset of 15 subjects was selected for validation of the algorithmic process. For these subjects, the heatpropagation parameterization process that was previously used in [1,6,9,7] was applied to the left central sulcus, and both sulcus extremities were marked manually by an operator.…”

“…In particular this method provides a normalized localization along the length of the sulcus, which has been used for the localization of depth asymmetries of the central sulcus [1,6] or the superior temporal sulcus [9], for the automatic detection and localization of the hand-knob [7], a morphological marker of the primary motor area of the hand [10], or for inter-species comparisons [11]. Any point on the sulcus is localized with a value between 0 and 100 relative to its position between the dorsal This work has been supported by the Agence Nationale de la Recherche (ANR MoDeGy, ANR-12-JS03-001-01).…”