Ensemble learning for the detection of pli-de-passages in the superior temporal sulcus.

The surface of the cerebral cortex is very convoluted, with a large number of folds, the cortical sulci. These folds are extremely variable from one individual to another, and this large variability is a problem for many applications in neuroscience and brain imaging. In particular, sulcal geometry (shape) and sulcal topology (branches, number of pieces) are very variable. "Plis de passages" (PPs) or "annectant gyri" can explain part of the topological variability, namely why sulci have a variable number of pieces across subjects. The concept of PPs was first introduced by Gratiolet (1854) to describe transverse gyri that interconnect both sides of a sulcus, that are frequently buried in the depth of sulci, and that are sometimes apparent on the cortical surface, hence seemingly interrupting the course of sulci and separating them in several pieces. Nevertheless, the difficulty of identifying PPs and the lack of systematic methods to automatically detect them has limited their use. However, based on a recent characterization of PPs in the superior temporal sulcus, we present here a method to automatically detect PPs in the superior temporal sulcus. Local morphology within the sulcus is characterized using cortical surface profiling, and the three-dimensional PP recognition problem is performed as a two-dimensional image classification problem with class-imbalance. This is solved by using an ensemble support vector machine model (EnsSVM) with a rebalancing strategy. Cross validation and quantitative experimental results on an external dataset show the effectiveness and robustness of our approach.

Anatomo-functional correspondence in the voice-selective regions of human prefrontal cortex.

Group level analyses of functional regions involved in voice perception show evidence of 3 sets of bilateral voice-sensitive activations in the human prefrontal cortex, named the anterior, middle and posterior Frontal Voice Areas (FVAs). However, the relationship with the underlying sulcal anatomy, highly variable in this region, is still unknown. We examined the inter-individual variability of the FVAs in conjunction with the sulcal anatomy. To do so, anatomical and functional MRI scans from 74 subjects were analyzed to generate individual contrast maps of the FVAs and relate them to each subject's manually labeled prefrontal sulci. We report two major results. First, the frontal activations for the voice are significantly associated with the sulcal anatomy. Second, this correspondence with the sulcal anatomy at the individual level is a better predictor than coordinates in the MNI space. These findings offer new perspectives for the understanding of anatomical-functional correspondences in this complex cortical region. They also shed light on the importance of considering individual-specific variations in subject's anatomy.

Imaging evolution of the primate brain: the next frontier?

Evolution, as we currently understand it, strikes a delicate balance between animals' ancestral history and adaptations to their current niche. Similarities between species are generally considered inherited from a common ancestor whereas observed differences are considered as more recent evolution. Hence comparing species can provide insights into the evolutionary history. Comparative neuroimaging has recently emerged as a novel subdiscipline, which uses magnetic resonance imaging (MRI) to identify similarities and differences in brain structure and function across species. Whereas invasive histological and molecular techniques are superior in spatial resolution, they are laborious, post-mortem, and oftentimes limited to specific species. Neuroimaging, by comparison, has the advantages of being applicable across species and allows for fast, whole-brain, repeatable, and multi-modal measurements of the structure and function in living brains and post-mortem tissue. In this review, we summarise the current state of the art in comparative anatomy and function of the brain and gather together the main scientific questions to be explored in the future of the fascinating new field of brain evolution derived from comparative neuroimaging.

Genetic Influence on the Sulcal Pits: On the Origin of the First Cortical Folds.

The influence of genes on cortical structures has been assessed through various phenotypes. The sulcal pits, which are the putative first cortical folds, have for long been assumed to be under tight genetic control, but this was never quantified. We estimated the pit depth heritability in various brain regions using the high quality and large sample size of the Human Connectome Project pedigree cohort. Analysis of additive genetic variance indicated that their heritability ranges between 0.2 and 0.5 and displays a regional genetic control with an overall symmetric pattern between hemispheres. However, a noticeable asymmetry of heritability estimates is observed in the superior temporal sulcus and could thus be related to language lateralization. The heritability range estimated in this study reinforces the idea that cortical shape is determined primarily by nongenetic factors, which is consistent with the important increase of cortical folding from birth to adult life and thus predominantly constrained by environmental factors. Nevertheless, the genetic cues, implicated with various local levels of heritability in the formation of sulcal pits, play a fundamental role in the normal gyral pattern development. Quantifying their influence and identifying the underlying genetic variants would provide insight into neurodevelopmental disorders.

Dynamic Reconfiguration of Visuomotor-Related Functional Connectivity Networks.

Cognitive functions arise from the coordination of large-scale brain networks. However, the principles governing interareal functional connectivity dynamics (FCD) remain elusive. Here, we tested the hypothesis that human executive functions arise from the dynamic interplay of multiple networks. To do so, we investigated FCD mediating a key executing function, known as arbitrary visuomotor mapping, using brain connectivity analyses of high-gamma activity recorded using MEG and intracranial EEG. Visuomotor mapping was found to arise from the dynamic interplay of three partly overlapping cortico-cortical and cortico-subcortical functional connectivity (FC) networks. First, visual and parietal regions coordinated with sensorimotor and premotor areas. Second, the dorsal frontoparietal circuit together with the sensorimotor and associative frontostriatal networks took the lead. Finally, cortico-cortical interhemispheric coordination among bilateral sensorimotor regions coupled with the left frontoparietal network and visual areas. We suggest that these networks reflect the processing of visual information, the emergence of visuomotor plans, and the processing of somatosensory reafference or action's outcomes, respectively. We thus demonstrated that visuomotor integration resides in the dynamic reconfiguration of multiple cortico-cortical and cortico-subcortical FC networks. More generally, we showed that visuomotor-related FC is nonstationary and displays switching dynamics and areal flexibility over timescales relevant for task performance. In addition, visuomotor-related FC is characterized by sparse connectivity with density <10%. To conclude, our results elucidate the relation between dynamic network reconfiguration and executive functions over short timescales and provide a candidate entry point toward a better understanding of cognitive architectures. SIGNIFICANCE STATEMENT: Executive functions are supported by the dynamic coordination of neural activity over large-scale networks. The properties of large-scale brain coordination processes, however, remain unclear. Using tools combining MEG and intracranial EEG with brain connectivity analyses, we provide evidence that visuomotor behaviors, a hallmark of executive functions, are mediated by the interplay of multiple and spatially overlapping subnetworks. These subnetworks span visuomotor-related areas, the cortico-cortical and cortico-subcortical interactions of which evolve rapidly and reconfigure over timescales relevant for behavior. Visuomotor-related functional connectivity dynamics are characterized by sparse connections, nonstationarity, switching dynamics, and areal flexibility. We suggest that these properties represent key aspects of large-scale functional networks and cognitive architectures.

The chaotic morphology of the left superior temporal sulcus is genetically constrained.

The asymmetry of the superior temporal sulcus (STS) has been identified as a species-specific feature of the human brain. The so-called superior temporal asymmetrical pit (STAP) area is observed from the last trimester of gestation onwards and is far less pronounced in the chimpanzee brain. This asymmetry is associated with more frequent sulcal interruptions, named plis de passage (PPs), leading to the irregular morphology of the left sulcus. In this paper, we aimed to characterize the variability, asymmetry, and heritability of these interruptions in the STS in comparison with the other main sulci. We developed an automated method to extract PPs across the cortex based on a highly reproducible grid of sulcal pits across individuals, which we applied to a subset of Human Connectome Project (HCP) subjects (N = 820). We report that only a few PPs across the cortex are genetically constrained, namely in the collateral, postcentral and superior temporal sulci and the calcarine fissure. Moreover, some PPs occur more often in one hemisphere than the other, namely in the precentral, postcentral, intraparietal sulci, as well as in both inferior and superior temporal sulci. Most importantly, we found that only the interruptions within the STAP region are both asymmetric and genetically constrained. Because this morphological pattern is located in an area of the left hemisphere related to speech, our results suggest structural constraints on the architecture of the linguistic network.

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

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.

The average baboon brain: MRI templates and tissue probability maps from 89 individuals.

The baboon (Papio) brain is a remarkable model for investigating the brain. The current work aimed at creating a population-average baboon (Papio anubis) brain template and its left/right hemisphere symmetric version from a large sample of T1-weighted magnetic resonance images collected from 89 individuals. Averaging the prior probability maps output during the segmentation of each individual also produced the first baboon brain tissue probability maps for gray matter, white matter and cerebrospinal fluid. The templates and the tissue probability maps were created using state-of-the-art, freely available software tools and are being made freely and publicly available: http://www.nitrc.org/projects/haiko89/ or http://lpc.univ-amu.fr/spip.php?article589. It is hoped that these images will aid neuroimaging research of the baboon by, for example, providing a modern, high quality normalization target and accompanying standardized coordinate system as well as probabilistic priors that can be used during tissue segmentation.

MarsAtlas: A cortical parcellation atlas for functional mapping.

An open question in neuroimaging is how to develop anatomical brain atlases for the analysis of functional data. Here, we present a cortical parcellation model based on macroanatomical information and test its validity on visuomotor-related cortical functional networks. The parcellation model is based on a recently developed cortical parameterization method (Auzias et al., [2013]: IEEE Trans Med Imaging 32:873-887), called HIP-HOP. This method exploits a set of primary and secondary sulci to create an orthogonal coordinate system on the cortical surface. A natural parcellation scheme arises from the axes of the HIP-HOP model running along the fundus of selected sulci. The resulting parcellation scheme, called MarsAtlas, complies with dorsoventral/rostrocaudal direction fields and allows inter-subject matching. To test it for functional mapping, we analyzed a MEG dataset collected from human participants performing an arbitrary visuomotor mapping task. Single-trial high-gamma activity, HGA (60-120 Hz), was estimated using spectral analysis and beamforming techniques at cortical areas arising from a Talairach atlas (i.e., Brodmann areas) and MarsAtlas. Using both atlases, we confirmed that visuomotor associations involve an increase in HGA over the sensorimotor and fronto-parietal network, in addition to medial prefrontal areas. However, MarsAtlas provided: (1) crucial functional information along both the dorsolateral and rostrocaudal direction; (2) an increase in statistical significance. To conclude, our results suggest that the MarsAtlas is a valid anatomical atlas for functional mapping, and represents a potential anatomical framework for integration of functional data arising from multiple techniques such as MEG, intracranial EEG and fMRI.

Evolution of the central sulcus morphology in primates.

The central sulcus (CS) divides the pre- and postcentral gyri along the dorsal-ventral plane of which all motor and sensory functions are topographically organized. The motor-hand area of the precentral gyrus or KNOB has been described as the anatomical substrate of the hand in humans. Given the importance of the hand in primate evolution, here we examine the evolution of the motor-hand area by comparing the relative size and pattern of cortical folding of the CS surface area from magnetic resonance images in 131 primates, including Old World monkeys, apes and humans. We found that humans and great apes have a well-formed motor-hand area that can be seen in the variation in depth of the CS along the dorsal-ventral plane. We further found that great apes have relatively large CS surface areas compared to Old World monkeys. However, relative to great apes, humans have a small motor-hand area in terms of both adjusted and absolute surface areas.

Planum temporale asymmetry in newborn monkeys predicts the future development of gestural communication's handedness.

The planum temporale (PT), a key language area, is specialized in the left hemisphere in prelinguistic infants and considered as a marker of the pre-wired language-ready brain. However, studies have reported a similar structural PT left-asymmetry not only in various adult non-human primates, but also in newborn baboons. Its shared functional links with language are not fully understood. Here we demonstrate using previously obtained MRI data that early detection of PT left-asymmetry among 27 newborn baboons (Papio anubis, age range of 4 days to 2 months) predicts the future development of right-hand preference for communicative gestures but not for non-communicative actions. Specifically, only newborns with a larger left-than-right PT were more likely to develop a right-handed communication once juvenile, a contralateral brain-gesture link which is maintained in a group of 70 mature baboons. This finding suggests that early PT asymmetry may be a common inherited prewiring of the primate brain for the ontogeny of ancient lateralised properties shared between monkey gesture and human language.

The Arcuate Fasciculus and language origins: Disentangling existing conceptions that influence evolutionary accounts.

The Arcuate Fasciculus (AF) is of considerable interdisciplinary interest, because of its major implication in language processing. Theories about language brain evolution are based on anatomical differences in the AF across primates. However, changing methodologies and nomenclatures have resulted in conflicting findings regarding interspecies AF differences: Historical knowledge about the AF originated from human blunt dissections and later from monkey tract-tracing studies. Contemporary tractography studies reinvestigate the fasciculus' morphology, but remain heavily bound to unclear anatomical priors and methodological limitations. First, we aim to disentangle the influences of these three epistemological steps on existing AF conceptions, and to propose a contemporary model to guide future work. Second, considering the influence of various AF conceptions, we discuss four key evolutionary changes that propagated current views about language evolution: 1) frontal terminations, 2) temporal terminations, 3) greater Dorsal- versus Ventral Pathway expansion, 4) lateralisation. We conclude that new data point towards a more shared AF anatomy across primates than previously described. Language evolution theories should incorporate this more continuous AF evolution across primates.

Broca's cerebral asymmetry reflects gestural communication's lateralisation in monkeys (Papio anubis).

Manual gestures and speech recruit a common neural network, involving Broca's area in the left hemisphere. Such speech-gesture integration gave rise to theories on the critical role of manual gesturing in the origin of language. Within this evolutionary framework, research on gestural communication in our closer primate relatives has received renewed attention for investigating its potential language-like features. Here, using in vivo anatomical MRI in 50 baboons, we found that communicative gesturing is related to Broca homologue's marker in monkeys, namely the ventral portion of the Inferior Arcuate sulcus (IA sulcus). In fact, both direction and degree of gestural communication's handedness - but not handedness for object manipulation are associated and correlated with contralateral depth asymmetry at this exact IA sulcus portion. In other words, baboons that prefer to communicate with their right hand have a deeper left-than-right IA sulcus, than those preferring to communicate with their left hand and vice versa. Interestingly, in contrast to handedness for object manipulation, gestural communication's lateralisation is not associated to the Central sulcus depth asymmetry, suggesting a double dissociation of handedness' types between manipulative action and gestural communication. It is thus not excluded that this specific gestural lateralisation signature within the baboons' frontal cortex might reflect a phylogenetical continuity with language-related Broca lateralisation in humans.

Long-term follow-up of neurodegenerative phenomenon in severe traumatic brain injury using MRI.

BACKGROUND: Traumatic brain injury (TBI) lesions are known to evolve over time, but the duration and consequences of cerebral remodelling are unclear. Degenerative mechanisms occurring in the chronic phase after TBI could constitute "tertiary" lesions related to the neurological outcome. OBJECTIVE: The objective of this prospective study of severe TBI was to longitudinally evaluate the volume of white and grey matter structures and white matter integrity with 2 time-point multimodal MRI. METHODS: Longitudinal MRI follow-up was obtained for 11 healthy controls (HCs) and 22 individuals with TBI (mean [SD] 60 [15] months after injury) along with neuropsychological assessments. TBI individuals were classified in the "favourable" recovery group (Glasgow Outcome Scale Extended [GOSE] 6-8) and "unfavourable" recovery group (GOSE 3-5) at 5 years. Variation in brain volumes (3D T1-weighted image) and white matter integrity (diffusion tensor imaging [DTI]) were quantitatively assessed over time and used to predict neurological outcome. RESULTS: TBI individuals showed a marked decrease in volumes of whole white matter (median -11.4% [interquartile range -5.8; -14.6]; p < 0.001) and deep grey nuclear structures (-17.1% [-10.6; -20.5]; p < 0.001). HCs did not show any significant change over the same time period. Median volumetric loss in several brain regions was higher with GOSE 3-5 than 6-8. These lesions were associated with lower fractional anisotropy and higher mean diffusivity at baseline. Volumetric variations were positively correlated with normalized fractional anisotropy and negatively with normalized mean diffusivity at baseline and follow-up. A computed predictive model with baseline DTI showed good accuracy to predict neurological outcome (area under the receiver operating characteristic curve 0.82 [95% confidence interval 0.81-0.83]) CONCLUSIONS: We characterised the striking atrophy of deep brain structures after severe TBI. DTI imaging in the subacute phase can predict the occurrence and localization of these tertiary lesions as well as long-term neurological outcome. TRIAL REGISTRATION: ClinicalTrials.gov: NCT00577954. Registered on October 2006.

Browsing Multiple Subjects When the Atlas Adaptation Cannot Be Achieved via a Warping Strategy.

Brain mapping studies often need to identify brain structures or functional circuits into a set of individual brains. To this end, multiple atlases have been published to represent such structures based on different modalities, subject sets, and techniques. The mainstream approach to exploit these atlases consists in spatially deforming each individual data onto a given atlas using dense deformation fields, which supposes the existence of a continuous mapping between atlases and individuals. However, this continuity is not always verified, and this "iconic" approach has limits. We present in this study an alternative, complementary, "structural" approach, which consists in extracting structures from the individual data, and comparing them without deformation. A "structural atlas" is thus a collection of annotated individual data with a common structure nomenclature. It may be used to characterize structure shape variability across individuals or species, or to train machine learning systems. This study exhibits Anatomist, a powerful structural 3D visualization software dedicated to building, exploring, and editing structural atlases involving a large number of subjects. It has been developed primarily to decipher the cortical folding variability; cortical sulci vary enormously in both size and shape, and some may be missing or have various topologies, which makes iconic approaches inefficient to study them. We, therefore, had to build structural atlases for cortical sulci, and use them to train sulci identification algorithms. Anatomist can display multiple subject data in multiple views, supports all kinds of neuroimaging data, including compound structural object graphs, handles arbitrary coordinate transformation chains between data, and has multiple display features. It is designed as a programming library in both C++ and Python languages, and may be extended or used to build dedicated custom applications. Its generic design makes all the display and structural aspects used to explore the variability of the cortical folding pattern work in other applications, for instance, to browse axonal fiber bundles, deep nuclei, functional activations, or other kinds of cortical parcellations. Multimodal, multi-individual, or inter-species display is supported, and adaptations to large scale screen walls have been developed. These very original features make it a unique viewer for structural atlas browsing.

U-shape short-range extrinsic connectivity organisation around the human central sulcus.

The central sulcus is probably one of the most studied folds in the human brain, owing to its clear relationship with primary sensory-motor functional areas. However, due to the difficulty of estimating the trajectories of the U-shape fibres from diffusion MRI, the short structural connectivity of this sulcus remains relatively unknown. In this context, we studied the spatial organization of these U-shape fibres along the central sulcus. Based on high quality diffusion MRI data of 100 right-handed subjects and state-of-the-art pre-processing pipeline, we first define a connectivity space that provides a comprehensive and continuous description of the short-range anatomical connectivity around the central sulcus at both the individual and group levels. We then infer the presence of five major U-shape fibre bundles at the group level in both hemispheres by applying unsupervised clustering in the connectivity space. We propose a quantitative investigation of their position and number of streamlines as a function of hemisphere, sex and functional scores such as handedness and manual dexterity. Main findings of this study are twofold: a description of U-shape short-range connectivity along the central sulcus at group level and the evidence of a significant relationship between the position of three hand related U-shape fibre bundles and the handedness score of subjects.

Surface Regularity via the Estimation of Fractional Brownian Motion Index.

The recent definition of fractional Brownian motions on surfaces has raised the statistical issue of estimating the Hurst index characterizing these models. To deal with this open issue, we propose a method which is based on a spectral representation of surfaces built upon their Laplace-Beltrami operator. This method includes a first step where the surface supporting the motion is recovered using a mean curvature flow, and a second one where the Hurst index is estimated by linear regression on the motion spectrum. The method is evaluated on synthetic surfaces. The interest of the method is further illustrated on some fetal cortical surfaces extracted from magnetic resonance images as a means to quantify the brain complexity during the gestational age.

Developmental changes of the central sulcus morphology in young children.

The human brain grows rapidly in early childhood, reaching 95% of its final volume by age 6. Understanding brain growth in childhood is important both to answer neuroscience questions about anatomical changes in development, and as a comparison metric for neurological disorders. Metrics for neuroanatomical development including cortical measures pertaining to the sulci can be instrumental in early diagnosis, monitoring, and intervention for neurological diseases. In this paper, we examine the development of the central sulcus in children aged 12-60 months from structural magnetic resonance images. The central sulcus is one of the earliest sulci to develop at the fetal stage and is implicated in diseases such as Attention Deficit Hyperactive Disorder and Williams syndrome. We investigate the relationship between the changes in the depth of the central sulcus with respect to age. In our results, we observed a pattern of depth present early on, that had been previously observed in adults. Results also reveal the presence of a rightward depth asymmetry at 12 months of age at a location related to orofacial movements. That asymmetry disappears gradually, mostly between 12 and 24 months, and we suggest that it is related to the development of language skills.

Group-level cortical surface parcellation with sulcal pits labeling.

Sulcal pits are the points of maximal depth within the folds of the cortical surface. These shape descriptors give a unique opportunity to access to a rich, fine-scale representation of the geometry and the developmental milestones of the cortical surface. However, using sulcal pits analysis at group level requires new numerical tools to establish inter-subject correspondences. Here, we address this issue by taking advantage of the geometrical information carried by sulcal basins that are the local patches of surfaces surrounding each sulcal pit. Our framework consists in two phases. First, we present a new method to generate a population-specific atlas of this sulcal basins organi- zation as a fold-level parcellation of the cortical surface. Then, we address the labeling of individual sulcal pits and corresponding basins with respect to this atlas. To assess their validity, we applied these methodological advances on two different populations of healthy subjects. The first database of 137 adults allowed us to compare our method to the state-of-the-art and the second database of 209 children, aged between 0 and 18 years, illustrates the adaptability and relevance of our method in the context of pediatric data showing strong variations in cortical volume and folding.