Inter-individual deep image reconstruction via hierarchical neural code conversion.

The sensory cortex is characterized by general organizational principles such as topography and hierarchy. However, measured brain activity given identical input exhibits substantially different patterns across individuals. Although anatomical and functional alignment methods have been proposed in functional magnetic resonance imaging (fMRI) studies, it remains unclear whether and how hierarchical and fine-grained representations can be converted between individuals while preserving the encoded perceptual content. In this study, we trained a method of functional alignment called neural code converter that predicts a target subject's brain activity pattern from a source subject given the same stimulus, and analyzed the converted patterns by decoding hierarchical visual features and reconstructing perceived images. The converters were trained on fMRI responses to identical sets of natural images presented to pairs of individuals, using the voxels on the visual cortex that covers from V1 through the ventral object areas without explicit labels of the visual areas. We decoded the converted brain activity patterns into the hierarchical visual features of a deep neural network using decoders pre-trained on the target subject and then reconstructed images via the decoded features. Without explicit information about the visual cortical hierarchy, the converters automatically learned the correspondence between visual areas of the same levels. Deep neural network feature decoding at each layer showed higher decoding accuracies from corresponding levels of visual areas, indicating that hierarchical representations were preserved after conversion. The visual images were reconstructed with recognizable silhouettes of objects even with relatively small numbers of data for converter training. The decoders trained on pooled data from multiple individuals through conversions led to a slight improvement over those trained on a single individual. These results demonstrate that the hierarchical and fine-grained representation can be converted by functional alignment, while preserving sufficient visual information to enable inter-individual visual image reconstruction.

A Sensorimotor Pathway via Higher-Order Thalamus.

We now know that sensory processing in cortex occurs not only via direct communication between primary to secondary areas, but also via their parallel cortico-thalamo-cortical (i.e., trans-thalamic) pathways. Both corticocortical and trans-thalamic pathways mainly signal through glutamatergic class 1 (driver) synapses, which have robust and efficient synaptic dynamics suited for the transfer of information such as receptive field properties, suggesting the importance of class 1 synapses in feedforward, hierarchical processing. However, such a parallel arrangement has only been identified in sensory cortical areas: visual, somatosensory, and auditory. To test the generality of trans-thalamic pathways, we sought to establish its presence beyond purely sensory cortices to determine whether there is a trans-thalamic pathway parallel to the established primary somatosensory (S1) to primary motor (M1) pathway. We used trans-synaptic viral tracing, optogenetics in slice preparations, and bouton size analysis in the mouse (both sexes) to document that a circuit exists from layer 5 of S1 through the posterior medial nucleus of the thalamus to M1 with glutamatergic class 1 properties. This represents a hitherto unknown, robust sensorimotor linkage and suggests that the arrangement of parallel direct and trans-thalamic corticocortical circuits may be present as a general feature of cortical functioning.SIGNIFICANCE STATEMENT During sensory processing, feedforward pathways carry information such as receptive field properties via glutamatergic class 1 synapses, which have robust and efficient synaptic dynamics. As expected, class 1 synapses subserve the feedforward projection from primary to secondary sensory cortex, but also a route through specific higher-order thalamic nuclei, creating a parallel feedforward trans-thalamic pathway. We now extend the concept of cortical areas being connected via parallel, direct, and trans-thalamic circuits from purely sensory cortices to a sensorimotor cortical circuit (i.e., primary sensory cortex to primary motor cortex). This suggests a generalized arrangement for corticocortical communication.

Encoding schemes in somatosensation: From micro- to meta-topography.

Encoding schemes are systematic large-scale arrangements that convert incoming sensory information into a format required for further information processing. The increased spatial resolution of brain images obtained with ultra-high field magnetic resonance imaging at 7 T (7T-MRI) and above increases the granularity and precision of processing units that mediate the link between neuronal encoding and functional readouts. Here, these new developments are reviewed with a focus on human tactile encoding schemes derived from small-scale processing units (in the order of 0.5-5 mm) that are relevant for theoretical and practical concepts of somatosensory encoding and cortical plasticity. Precisely, we review recent approaches to characterize meso-scale maps, layer units, and cortical fields in the sensorimotor cortex of the living human brain and discuss their impact on theories of perception, motor control, topographic encoding, and cortical plasticity. Finally, we discuss concepts on the integration of small-scale processing units into functional networks that span multiple topographic maps and multiple cortical areas. Novel research areas are highlighted that may help to bridge the gap between cortical microstructure and meta-topographic models on brain anatomy and function.

Sensorimotor maps can be dynamically calibrated using an adaptive-filter model of the cerebellum.

Substantial experimental evidence suggests the cerebellum is involved in calibrating sensorimotor maps. Consistent with this involvement is the well-known, but little understood, massive cerebellar projection to maps in the superior colliculus. Map calibration would be a significant new role for the cerebellum given the ubiquity of map representations in the brain, but how it could perform such a task is unclear. Here we investigated a dynamic method for map calibration, based on electrophysiological recordings from the superior colliculus, that used a standard adaptive-filter cerebellar model. The method proved effective for complex distortions of both unimodal and bimodal maps, and also for predictive map-based tracking of moving targets. These results provide the first computational evidence for a novel role for the cerebellum in dynamic sensorimotor map calibration, of potential importance for coordinate alignment during ongoing motor control, and for map calibration in future biomimetic systems. This computational evidence also provides testable experimental predictions concerning the role of the connections between cerebellum and superior colliculus in previously observed dynamic coordinate transformations.

Adaptation of brain functional stream architecture in athletes with fast demands of sensorimotor integration.

Training-induced neuroplasticity has been described in athletes' population. However, it remains largely unknown how regular training and sports proficiency modifies neuronal circuits in the human brain. In this study, we used voxel-based morphometry and stepwise functional connectivity (SFC) analyses to uncover connectivity changes in the functional stream architecture in student-athletes at early stages of sensorimotor skill training. Thirty-two second-year student-athletes whose major was little-ball sports and thirty-four nonathlete controls were recruited for the study. We found that athletes showed greater gray matter volume in the right sensorimotor area, the limbic lobe, and the anterior lobe of the cerebellum. Furthermore, SFC analysis demonstrated that athletes displayed significantly smaller optimal connectivity distance from those seed regions to the dorsal attention network (DAN) and larger optimal connectivity distance to the default mode network (DMN) compared to controls. The Attention Network Test showed that the reaction time of the orienting attention subnetwork was positively correlated with SFC between the seeds and the DAN, while negatively correlated with SFC between the seeds and the DMN. Our findings suggest that neuroplastic adaptations on functional connectivity streams after motor skill training may enable novel information flow from specific areas of the cortex toward distributed networks such as the DAN and the DMN. This could potentially regulate the focus of external and internal attention synchronously in athletes, and consequently accelerate the reaction time of orienting attention in athletes.

"Plis de passage" Deserve a Role in Models of the Cortical Folding Process.

Cortical folding is a hallmark of brain topography whose variability across individuals remains a puzzle. In this paper, we call for an effort to improve our understanding of the pli de passage phenomenon, namely annectant gyri buried in the depth of the main sulci. We suggest that plis de passage could become an interesting benchmark for models of the cortical folding process. As an illustration, we speculate on the link between modern biological models of cortical folding and the development of the Pli de Passage Frontal Moyen (PPFM) in the middle of the central sulcus. For this purpose, we have detected nine interrupted central sulci in the Human Connectome Project dataset, which are used to explore the organization of the hand sensorimotor areas in this rare configuration of the PPFM.

Structural Connections of Functionally Defined Human Insular Subdivisions.

The organization of the human insular cortex has traditionally been considered as an anterior-posterior dichotomy, where anterior and posterior subdivisions have unique structural and functional connections. However, recent functional neuroimaging research proposes a tripartite organization where insular subdivisions have both unique and overlapping functional profiles. Studies examining unique profiles show that the dorsal anterior insula (dAI) has connections with frontal areas supporting higher-level cognitive processes, the ventral anterior insula (vAI) has connections with limbic areas supporting affective processes, and the posterior insula (PI) has connections with sensorimotor areas supporting interoceptive processes. Studies examining overlapping profiles demonstrate that all 3 subdivisions can also have similar functional profiles. The structural organization supporting a functional tripartite insula organization presenting with overlapping and unique connections is currently unknown. We used a large HARDI diffusion magnetic resonance imaging (MRI) dataset (n = 199) to demonstrate novel visualizations of insula white matter tracts supporting a tripartite structure-function insula organization. Overlapping connections of all 3 insula subdivisions consisted of association pathways (inferior fronto-occipital fasciculus, uncinate fasciculus, arcuate fasciculus) while unique connections included the corona radiata, subcortical-cortical tracts, and horizontal and u-shaped tracts. These results generally support a tripartite structure-function organization of the insular cortex, with subdivisions that exhibit both overlapping and unique connectivity profiles.

Mapping of fine-scale rat prefrontal cortex connections: Evidence for detailed ordering of inputs and outputs connecting the temporal cortex and sensory-motor regions.

Cerebral cortex structure is crucially important for cortical organization and function. The organization of prefrontal cortex (PFC) is controversial and here we seek to understand it more clearly through the study of fine-scale cortical connections. To determine the ordering of microscale input and output connections in the rat PFC, we injected small volumes (20-30 nl) of anterograde (Fluro-Ruby) and retrograde (Fluoro-Gold) neuroanatomical tracers into PFC. These injections revealed several connected regions of the brain but here we report findings restricted to PFC to temporal cortex and sensory-motor cortex pathways. In agreement with previous studies incorporating larger injection volumes we found that smaller injection volumes revealed a more detailed, fine-scale ordering of both prefrontal inputs and output connections to the temporal cortex and sensory-motor cortex regions. These findings are also supported by labelling observed from additional tracer injections made into corresponding regions of temporal cortex. The topography observed reflected the ordering seen at a larger level (i.e., with larger injection volumes) but there were some differences in the topography, such as in relation to the direction of ordering. In agreement with earlier work, we found that fine-scale input and output connections were not always aligned with respect to one another. These results provide evidence for topographically arranged inputs and outputs in two distinct PFC pathways, along with evidence for different connectional patterns within the same pathways. Based on theories of functional connectivity, these findings provide evidence for prefrontal cortical regions residing within networks that contribute to different cognitive functions.

The postcentral sulcal complex and the transverse postcentral sulcus and their relation to sensorimotor functional organization.

It has been demonstrated that the postcentral sulcus, which forms the posterior boundary of the sensorimotor region, is a complex of distinct sulcal segments. Although the general somatotopic arrangement in the human sensorimotor cortex is relatively well known, we do not know whether the different segments of the postcentral sulcus relate in a systematic way to the sensorimotor functional representations. Participants were scanned with functional magnetic resonance imaging while they made movements of different body parts and the location of functional activity was examined on a subject-by-subject basis with respect to the morphological features of the postcentral sulcus. The findings demonstrate that the postcentral sulcus of each subject may be divided into five segments and there is a tight relationship between sensorimotor representations of different body parts and specific segments of the postcentral sulcus. The results also addressed the issue of the transverse postcentral sulcus, a short sulcus that is present within the ventral part of the postcentral gyrus in some brains. It was shown that, when present, this sulcus is functionally related to the oral (mouth and tongue) sensorimotor representation. When this sulcus is not present, the inferior postcentral sulcus which is also related to the oral representation is longer. Thus, the sulcal morphology provides an improved framework for functional assignments in individual subjects.

Functional organization of human subgenual cortical areas: Relationship between architectonical segregation and connectional heterogeneity.

Human subgenual anterior cingulate cortex (sACC) is involved in affective experiences and fear processing. Functional neuroimaging studies view it as a homogeneous cortical entity. However, sACC comprises several distinct cyto- and receptorarchitectonical areas: 25, s24, s32, and the ventral portion of area 33. Thus, we hypothesized that the areas may also be connectionally and functionally distinct. We performed structural post mortem and functional in vivo analyses. We computed probabilistic maps of each area based on cytoarchitectonical analysis of ten post mortem brains. Maps, publicly available via the JuBrain atlas and the Anatomy Toolbox, were used to define seed regions of task-dependent functional connectivity profiles and quantitative functional decoding. sACC areas presented distinct co-activation patterns within widespread networks encompassing cortical and subcortical regions. They shared common functional domains related to emotion, perception and cognition. A more specific analysis of these domains revealed an association of s24 with sadness, and of s32 with fear processing. Both areas were activated during taste evaluation, and co-activated with the amygdala, a key node of the affective network. s32 co-activated with areas of the executive control network, and was associated with tasks probing cognition in which stimuli did not have an emotional component. Area 33 was activated by painful stimuli, and co-activated with areas of the sensorimotor network. These results support the concept of a connectional and functional specificity of the cyto- and receptorarchitectonically defined areas within the sACC, which can no longer be seen as a structurally and functionally homogeneous brain region.

Development of the sensorimotor cortex in the human fetus: a morphological description.

Twenty-one human fetal brains from 13 to 28 gestational weeks were studied macroscopically to describe the morphological stages of sulcal and gyral development in the sensorimotor cortex. In particular, the morphological appearance of the pericentral lateral cortex (sensorimotor cortex) and opercula was noted, as well as the vascularization of these regions. The central cerebral sulci were the first macroscopical structures to be identified on the lateral surface of the human cerebral hemisphere. Four chronological stages of sensorimotor cortex development were defined: stage 1: appearance at 18-19 gestational weeks (GWs) of the inferior part of the central cerebral sulcus; stage 2: development of the pericentral lateral regions and the beginning of opercularization at 20-22 GWs; stage 3: development of parietal and temporal cortices and the covering of the postcentral insular region at 24-26 GWs; and finally stage 4: maturation of the central cerebral regions at 27-28 GWs. These observations indicate the concomitance in the initiation of maturation of the pericentral cerebral cortices.

Does motion-related brain functional connectivity reflect both artifacts and genuine neural activity?

Imaging research on functional connectivity is uniquely contributing to characterize the functional organization of the human brain. Functional connectivity measurements, however, may be significantly influenced by head motion that occurs during image acquisition. The identification of how motion influences such measurements is therefore highly relevant to the interpretation of a study's results. We have mapped the effect of head motion on functional connectivity in six different populations representing a wide range of potential influences of motion on functional connectivity. Group-level voxel-wise maps of the correlation between a summary head motion measurement and functional connectivity degree were estimated in 80 young adults, 71 children, 53 older adults, 20 patients with Down syndrome, 24 with Prader-Willi syndrome and 20 with Williams syndrome. In highly compliant young adults, motion correlated with functional connectivity measurements showing a system-specific anatomy involving the sensorimotor cortex, visual areas and default mode network. Further characterization was strongly indicative of these changes expressing genuine neural activity related to motion, as opposed to pure motion artifact. In the populations with larger head motion, results were more indicative of widespread artifacts, but showing notably distinct spatial distribution patterns. Group-level regression of motion effects was efficient in removing both generalized changes and changes putatively related to neural activity. Overall, this study endorses a relatively simple approach for mapping distinct effects of head motion on functional connectivity. Importantly, our findings support the intriguing hypothesis that a component of motion-related changes may reflect system-specific neural activity.

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.

[Human traveling wave EEG during voluntary movement of the hand].

The traveling wave trajectories connected with the movements of the right hand were revealed. Above sensomotor cortex 28 electrodes were set as a rectangle--4 rows with 7 electrodes in each one. 2D center-out reaching task was used. The target appeared on the screen edge through the random intervals 0.5-2.5 s equiprobably at the left, on the right, from above or from below. The task was to touch the target with the joystick-operated cursor displacing the cursor in one of the sides from the center to edge. EEG from the target occurrence till cursor contact with it was analyzed. Leading on phase of spontaneous EEG waves in the local area of the left sensomotor cortex and in the centre of back-parietal cortex during cursor movement downwards (the hand with joystick moves to oneself) comparing to rest state and movements in three other directions is revealed. The over time smoothing of data concerning phase alignment reveals hidden constant components in EEG resembling evoked potentials.

Considerations for implanting speech brain computer interfaces based on functional magnetic resonance imaging.

Objective.Brain-computer interfaces (BCIs) have the potential to reinstate lost communication faculties. Results from speech decoding studies indicate that a usable speech BCI based on activity in the sensorimotor cortex (SMC) can be achieved using subdurally implanted electrodes. However, the optimal characteristics for a successful speech implant are largely unknown. We address this topic in a high field blood oxygenation level dependent functional magnetic resonance imaging (fMRI) study, by assessing the decodability of spoken words as a function of hemisphere, gyrus, sulcal depth, and position along the ventral/dorsal-axis.Approach.Twelve subjects conducted a 7T fMRI experiment in which they pronounced 6 different pseudo-words over 6 runs. We divided the SMC by hemisphere, gyrus, sulcal depth, and position along the ventral/dorsal axis. Classification was performed on in these SMC areas using multiclass support vector machine (SVM).Main results.Significant classification was possible from the SMC, but no preference for the left or right hemisphere, nor for the precentral or postcentral gyrus for optimal word classification was detected. Classification while using information from the cortical surface was slightly better than when using information from deep in the central sulcus and was highest within the ventral 50% of SMC. Confusion matrices where highly similar across the entire SMC. An SVM-searchlight analysis revealed significant classification in the superior temporal gyrus and left planum temporale in addition to the SMC.Significance.The current results support a unilateral implant using surface electrodes, covering the ventral 50% of the SMC. The added value of depth electrodes is unclear. We did not observe evidence for variations in the qualitative nature of information across SMC. The current results need to be confirmed in paralyzed patients performing attempted speech.

Cortical patterning of morphometric similarity gradient reveals diverged hierarchical organization in sensory-motor cortices.

The topological organization of the cerebral cortex provides hierarchical axes, namely gradients, which reveal systematic variations of brain structure and function. However, the hierarchical organization of macroscopic brain morphology and how it constrains cortical function along the organizing axes remains unclear. We map the gradient of cortical morphometric similarity (MS) connectome, combining multiple features conceptualized as a "fingerprint" of an individual's brain. The principal MS gradient is anchored by motor and sensory cortices at two extreme ends, which are reliable and reproducible. Notably, divergences between motor and sensory hierarchies are consistent with the laminar histological thickness gradient but contrary to the canonical functional connectivity (FC) gradient. Moreover, the MS dissociates with FC gradients in the higher-order association cortices. The MS gradient recapitulates fundamental properties of cortical organization, from gene expression and cyto- and myeloarchitecture to evolutionary expansion. Collectively, our findings provide a heuristic hierarchical organization of cortical morphological neuromarkers.

Parallel organization of the avian sensorimotor arcopallium: Tectofugal visual pathway in the pigeon (Columba livia).

The sensory-motor division of the avian arcopallium receives parallel inputs from primary and high-order pallial areas of sensory and vocal control pathways, and sends a prominent descending projection to ascending and premotor, subpallial stages of these pathways. While this organization is well established for the auditory and trigeminal systems, the arcopallial subdivision related to the tectofugal visual system and its descending projection to the optic tectum (TeO) has been less investigated. In this study, we charted the arcopallial area displaying tectofugal visual responses and by injecting neural tracers, we traced its connectional anatomy. We found visual motion-sensitive responses in a central region of the dorsal (AD) and intermediate (AI) arcopallium, in between previously described auditory and trigeminal zones. Blocking the ascending tectofugal sensory output, canceled these visual responses in the arcopallium, verifying their tectofugal origin. Injecting PHA-L into the visual, but not into the auditory AI, revealed a massive projection to tectal layer 13 and other tectal related areas, sparing auditory, and trigeminal ones. Conversely, CTB injections restricted to TeO retrogradely labeled neurons confined to the visual AI. These results show that the AI zone receiving tectofugal inputs sends top-down modulations specifically directed to tectal targets, just like the auditory and trigeminal AI zones project back to their respective subpallial sensory and premotor areas, as found by previous studies. Therefore, the arcopallium seems to be organized in a parallel fashion, such that in spite of expected cross-modal integration, the different sensory-motor loops run through separate subdivisions of this structure.

A Novel 2D Standard Cartesian Representation for the Human Sensorimotor Cortex.

For some experimental approaches in brain imaging, the existing normalization techniques are not always sufficient. This may be the case if the anatomical shape of the region of interest varies substantially across subjects, or if one needs to compare the left and right hemisphere in the same subject. Here we propose a new standard representation, building upon existing normalization methods: Cgrid (Cartesian geometric representation with isometric dimensions). Cgrid is based on imposing a Cartesian grid over a cortical region of interest that is bounded by anatomical (atlas-based) landmarks. We applied this new representation to the sensorimotor cortex and we evaluated its performance by studying the similarity of activation patterns for hand, foot and tongue movements between subjects, and similarity between hemispheres within subjects. The Cgrid similarities were benchmarked against the similarities of activation patterns when transformed into standard MNI space using SPM, and to similarities from FreeSurfer's surface-based normalization. For both between-subject and between-hemisphere comparisons, similarity scores in Cgrid were high, similar to those from FreeSurfer normalization and higher than similarity scores from SPM's MNI normalization. This indicates that Cgrid allows for a straightforward way of representing and comparing sensorimotor activity patterns across subjects and between hemispheres of the same subjects.

The anatomo-functional organization of the hyperdirect cortical pathway to the subthalamic area using in vivo structural connectivity imaging in humans.

The subthalamic nucleus (STN) receives direct cortical inputs which constitute the so-called hyperdirect pathway. In monkeys, motor cortices innervate the whole extent of the STN whereas limbic cortices innervate only its anteromedial part extending more medially outside the nucleus. Tractography studies in humans have also identified motor cortical inputs to the STN, but little is known about the associative and limbic cortical projections. Therefore, the aim of this study was to investigate the anatomo-functional organization of the cortical projections to the STN and to the adjacent medial subthamic region (MSR). We used diffusion-weighted imaging-based tractography acquired from 30 subjects from the Human Connectome Project. We performed a whole-brain probabilistic tractography using MRTrix and extracted streamlines of interest between 39 cortical masks and both the STN and the MSR to provide track-density maps. Agglomerative clustering method was used to classify the voxels of the regions of interest. We found that the STN receives major inputs from the sensorimotor cortices and few inputs from the limbic cortices. On the other hand, the MSR receives mainly cortical limbic projections and few from the sensorimotor cortices. Weak connections were found between the associative cortices and both the STN and the MSR. We found a dominant motor cluster located in the posterolateral STN, a limbic cluster located medially in the MSR, and an intermediate motor-limbic cluster in between. Our findings show that the hyperdirect pathway is anatomo-functionally organized with a poor participation of associative cortices.