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Emotion-related impulsivity (ERI) refers to chronically poor self-control during periods of strong emotion. ERI robustly predicts psychiatric disorders and related problems, yet its neuroanatomical correlates are largely unknown. We tested whether local brain morphometry in targeted brain regions that integrate emotion and control could explain ERI severity.One hundred twenty-two adults (ages 18-55 years) with internalizing or externalizing psychopathology completed a structural magnetic resonance imaging (MRI) scan, the Three-Factor Impulsivity Index, and the Structured Clinical Interview for DSM-5. The Three-Factor Impulsivity Index measures two types of ERI and a third type of impulsivity not linked to emotion. Cortical reconstruction yielded cortical thickness and local gyrification measurements. We evaluated whether morphometry in the orbitofrontal cortex (OFC), insula, amygdala, and nucleus accumbens was associated with ERI severity. Hypotheses and analyses were preregistered.Lower cortical gyrification in the right lateral OFC was associated with high ERI severity in a full, preregistered model. Separate examinations of local gyrification and cortical thickness also showed a positive association between gyrification in the left lateral OFC and ERI. An integrated measure of hemispheric imbalance in lateral OFC gyrification (rightleft) correlated with ERI severity. These findings were specific to ERI and did not appear with non-emotion-related impulsivity.Local gyrification in the lateral OFC is associated with ERI severity. The current findings fit with existing theories of OFC function, strengthen the connections between the transdiagnostic literature in psychiatry and neuroscience, and may guide future treatment development.

Transcriptomic contributions to the anatomical, functional, and network layout of the human cerebral cortex (HCC) has become a major interest in cognitive and systems neuroscience. Here, we tested if transcriptomic differences support a modern, algorithmic cytoarchitectonic parcellation of HCC. Using a data-driven approach, we identified a sparse subset of genes that differentially contributed to the cytoarchitectonic parcellation of HCC. A novel metric (cortical thickness/myelination ratio; CT/M ratio), as well as cell density, correlated with gene expression. Enrichment analyses showed that genes specific to the cytoarchitectonic parcellation of the HCC were related to molecular functions such as transmembrane transport and ion channel activity. Together, the novel relationship between transcriptomics and the CT/M ratio bridges the gap among i) gradients at the macroscale, ii) areas at the meso-scale, and iii) cell density at the microscale, as well as supports the recently proposed cortical spectrum theory.

Gene expression gradients radiating from regions of primary sensory cortices have recently been described and are thought to underlie the large-scale organization of the human cerebral cortex. However, the role of transcription in the functional layout of a single region within the adult brain has yet to be clarified, likely owing to the difficulty of identifying a brain region anatomically consistent enough across individuals with dense enough tissue sampling. Overcoming these hurdles in human primary visual cortex (V1), we show a relationship between differential gene expression and the cortical layout of eccentricity in human V1. Interestingly, these genes are unique from those previously identified that contribute to the positioning of cortical areas in the visual processing hierarchy. Enrichment analyses show that a subset of the identified genes encode for structures related to inhibitory interneurons, ion channels, as well as cellular projections, and are expressed more in foveal compared to peripheral portions of human V1. These findings predict that tissue density should be higher in foveal compared to peripheral V1. Using a histological pipeline, we validate this prediction using Nissl-stained sections of postmortem occipital cortex. We discuss these findings relative to previous studies in non-human primates, as well as in the context of an organizational pattern in which the adult human brain employs transcription gradients at multiple spatial scales: across the cerebral cortex, across areas within processing hierarchies, and within single cortical areas.

Previous findings show that the morphology of folds (sulci) of the human cerebral cortex flatten during postnatal development. However, previous studies did not consider the relationship between sulcal morphology and cognitive development in individual participants. Here, we fill this gap in knowledge by leveraging cross-sectional morphological neuroimaging data in the lateral prefrontal cortex (LPFC) from individual human participants (6-36 years old, males and females; N = 108; 3672 sulci), as well as longitudinal morphological and behavioral data from a subset of child and adolescent participants scanned at two timepoints (6-18 years old; N = 44; 2992 sulci). Manually defining thousands of sulci revealed that LPFC sulcal morphology (depth, surface area, gray matter thickness, and local gyrification index) differed between children (6-11 years old)/adolescents (11-18 years old) and young adults (22-36 years old) cross-sectionally, but only cortical thickness showed both cross-sectional differences between children and adolescents and presented longitudinal changes during childhood and adolescence. Furthermore, a data-driven approach relating morphology and cognition identified that longitudinal changes in cortical thickness of four rostral LPFC sulci predicted longitudinal changes in reasoning performance, a higher-level cognitive ability that relies on LPFC. Contrary to previous findings, these results suggest that sulci may flatten either after this time frame or over a longer longitudinal period of time than previously presented. Crucially, these results also suggest that longitudinal changes in the cortex within specific LPFC sulci are behaviorally meaningful—providing targeted structures, and areas of the cortex, for future neuroimaging studies examining the development of cognitive abilities.Significance StatementRecent work has shown that individual differences in neuroanatomical structures (indentations, or sulci) within the lateral prefrontal cortex (LPFC) are behaviorally meaningful during childhood and adolescence. Here, we describe how specific LPFC sulci develop at the level of individual participants for the first time—from both cross-sectional and longitudinal perspectives. Further, we show, also for the first time, that the longitudinal morphological changes in these structures are behaviorally relevant. These findings lay the foundation for a future avenue to precisely study the development of the cortex and highlight the importance of studying the development of sulci in other cortical expanses and charting how these changes relate to the cognitive abilities those areas support at the level of individual participants.

Understanding brain structure-function relationships, and their development and evolution, is central to neuroscience research. Here, we show that morphological differences in posterior cingulate cortex (PCC), a hub of functional brain networks, predict individual differences in macroanatomical, microstructural, and functional features of PCC. Manually labeling 4511 sulci in 572 hemispheres, we found a shallow cortical indentation (termed the inframarginal sulcus; ifrms ) within PCC that is absent from neuroanatomical atlases yet colocalized with a focal, functional region of the lateral frontoparietal network implicated in cognitive control. This structural-functional coupling generalized to meta-analyses consisting of hundreds of studies and thousands of participants. Additional morphological analyses showed that unique properties of the ifrms differ across the life span and between hominoid species. These findings support a classic theory that shallow, tertiary sulci serve as landmarks in association cortices. They also beg the question: How many other cortical indentations have we missed?

Two recent parallel research tracks link tertiary sulcal morphology—sulci that emerge last in gestation and continue to develop after birth—with functional features of the cerebral cortex and cognition, respectively. The first track identified a relationship between the mid-fusiform sulcus (MFS) in ventral temporal cortex (VTC) and cognition in individuals with Autism Spectrum Disorder (ASD). The second track identified a new tertiary sulcus, the inframarginal sulcus (IFRMS), that serves as a tripartite landmark within the posteromedial cortex (PMC). As VTC and PMC are structurally and functionally different in individuals with ASD compared to neurotypical controls (NTs), here, we integrated these two tracks with a twofold approach. First, we tested if there are morphological differences in VTC and PMC sulci between 50 NTs and 50 individuals with ASD. Second, we tested if tertiary sulcal morphology was linked to cognition in ASD individuals. Our twofold approach replicates and extends recent findings in five ways. First, in terms of replication, the standard deviation (STD) of MFS cortical thickness (CT) was increased in ASDs compared to NTs. Second, MFS length was shorter in ASDs compared to NTs. Third, the CT STD effect extended to other VTC and PMC sulci. Fourth, a subset of VTC and PMC morphological features were correlated between regions in ASD. Fifth, IFRMS depth was negatively associated with ADOS-GS score. These results empirically support a relationship between later-developing, tertiary sulci and ASD, providing a novel framework to study the relationship between brain structure and cognition in additional neurodevelopmental disorders in future studies.Lay SummaryWe observed that some, but not all, morphological features of later-developing tertiary indentations (sulci) in the cerebral cortex differed significantly between neurotypical controls and individuals with autism spectrum disorder (ASD). In ASD, a subset of sulcal morphological features also correlated between brain areas and one feature reflected differences in cognition. Thus, studying these structures provides insight into how individual variability in structure is related to individual variability in cognition in ASD.

Superficial white matter (SWM) represents a significantly understudied part of the human brain, despite comprising a large portion of brain volume and making up a majority of cortical structural connections. Using multiple, high-quality, datasets with large sample sizes (N=2421, age range 5-100) in combination with methodological advances in tractography, we quantified features of SWM volume and thickness across the brain and across the lifespan. We address four questions: (1) How does U-fiber volume change with age? (2) What does U-fiber thickness look like across the brain? (3) How does SWM thickness change with age? (4) Are there relationships between SWM thickness and cortical features? Our main findings are that (1) SWM volume shows unique volumetric trajectories with age that are distinct from gray matter and other white matter trajectories; (2) SWM thickness varies across the brain, with patterns robust across individuals and across the population at the region-level and vertex-level; (3) SWM shows nonlinear changes across the lifespan that vary across regions; and (4) SWM thickness is associated with cortical thickness and curvature. For the first time, we show that SWM volume follows a similar trend as overall white matter volume, peaking at a similar time in adolescence, leveling off throughout adulthood, and decreasing with age thereafter. Notably, the relative fraction of total brain volume of SWM continuously increases with age, and consequently takes up a larger proportion of total white matter volume, unlike the other tissue types that decrease with respect to total brain volume. This study represents the first characterization of SWM features across the lifespan and provides the background for characterizing normal aging and insight into the mechanisms associated with SWM development and decline.

Posterior cingulate cortex (PCC) is an enigmatic region implicated in psychiatric and neurological disease, yet its role in cognition remains unclear. Human studies link PCC to episodic memory and default mode network (DMN), while findings from the non-human primate emphasize executive processes more associated with the cognitive control network (CCN) in humans. We hypothesized this difference reflects an important functional division between dorsal (executive) and ventral (episodic) PCC. To test this, we utilized human intracranial recordings of population and single unit activity targeting dorsal PCC during an alternated executive/episodic processing task. Dorsal PCC population responses were significantly enhanced for executive, compared to episodic, task conditions, consistent with the CCN. Single unit recordings, however, revealed four distinct functional types with unique executive (CCN) or episodic (DMN) response profiles. Our findings provide critical electrophysiological data from human PCC, bridging incongruent views within and across species, furthering our understanding of PCC function.

The Fusiform Face Area (FFA) is a widely studied region causally involved in face perception. Even though cognitive neuroscientists have been studying the FFA for over two decades, answers to foundational questions regarding the structure, function, and connectivity of the FFA from a large (N>1000) group of participants are still lacking. To fill this gap, we quantified structural, functional, and connectivity features of fusiform face-selective regions in 1080 participants in the Human Connectome Project (HCP). After manually defining over 4,000 fusiform face-selective regions, we report five main findings. First, 68.94% of hemispheres have two cortically separate regions (pFus-faces/FFA-1 and mFus-faces/FFA-2). Second, in 26.48% of hemispheres, pFus-faces/FFA-1 and mFus-faces/FFA-2 are spatially contiguous, yet functionally and structurally distinct. Third, pFus-faces/FFA-1 is more face-selective than mFus-faces/FFA-2, and the two regions have distinct functional connectivity fingerprints. Fourth, pFus-faces/FFA-1 is cortically thinner and more heavily myelinated than mFus-faces/FFA-2. Fifth, face-selective patterns and functional connectivity fingerprints of each region were more similar in monozygotic than dizygotic twins and more so than structural gradients. As we share our areal definitions with the field, future studies can explore how structural and functional features of these regions will inform theories regarding how visual categories are represented in the brain.

Similarities and differences in brain structure and function across species is of major interest in systems neuroscience, comparative biology, and brain mapping. Recently, increased emphasis has been placed on tertiary sulci, which are shallow indentations of the cerebral cortex that appear last in gestation, continue to develop after birth, and are largely either human- or hominoid-specific. While tertiary sulcal morphology in lateral prefrontal cortex (LPFC) has been linked to functional representations and cognition in humans, it is presently unknown if LPFC tertiary sulci also exist in non-human hominoids. To fill this gap in knowledge, we leveraged two freely available multimodal datasets to address the following main question: Can LPFC tertiary sulci be defined in chimpanzee cortical surfaces from human predictions? We found that 1-3 components of the posterior middle frontal sulcus (pmfs) in the posterior middle frontal gyrus are identifiable in nearly all chimpanzee hemispheres. In stark contrast to the consistency of the pmfs components, we could only identify components of the paraintermediate frontal sulcus (pimfs) in two chimpanzee hemispheres. LPFC tertiary sulci were relatively smaller and shallower in chimpanzees compared to humans. In both species, two of the pmfs components were deeper in the right compared to the left hemisphere. As these results have direct implications for future studies interested in the functional and cognitive role of LPFC tertiary sulci across species, we share probabilistic predictions of the three pmfs components to guide the definitions of these sulci in future studies.

The evolution and development of anatomical–functional relationships in the cerebral cortex is of major interest in neuroscience. Here, we leveraged the fact that a functional region selective for visual scenes is located within a sulcus in the medial ventral temporal cortex (VTC) in both humans and macaques to examine the relationship between sulcal depth and place selectivity in the medial VTC across species and age groups. To do so, we acquired anatomical and functional magnetic resonance imaging scans in 9 macaques, 26 human children, and 28 human adults. Our results revealed a strong structural–functional coupling between sulcal depth and place selectivity across age groups and species in which selectivity was strongest near the deepest sulcal point (the sulcal pit). Interestingly, this coupling between sulcal depth and place selectivity strengthens from childhood to adulthood in humans. Morphological analyses suggest that the stabilization of sulcal–functional coupling in adulthood may be due to sulcal deepening and areal expansion with age as well as developmental differences in cortical curvature at the pial, but not the white matter surfaces. Our results implicate sulcal features as functional landmarks in high-level visual cortex and highlight that sulcal–functional relationships in the medial VTC are preserved between macaques and humans despite differences in cortical folding.

We have an amazing ability to categorize objects in the world around us. Nevertheless, how cortical regions in human ventral temporal cortex (VTC), which is critical for categorization, support this behavioral ability, is largely unknown. Here, we examined the relationship between neural responses and behavioral performance during the categorization of morphed silhouettes of faces and hands, which are animate categories processed in cortically adjacent regions in VTC. Our results reveal that the combination of neural responses from VTC face- and body-selective regions more accurately explains behavioral categorization than neural responses from either region alone. Furthermore, we built a model that predicts a person’s behavioral performance using estimated parameters of brain–behavior relationships from a different group of people. Moreover, we show that this brain–behavior model generalizes to adjacent face- and body-selective regions in lateral occipitotemporal cortex. Thus, while face- and body-selective regions are located within functionally distinct domain-specific networks, cortically adjacent regions from both networks likely integrate neural responses to resolve competing and perceptually ambiguous information from both categories.

The relationship between structural variability in late-developing association cortices like the lateral prefrontal cortex (LPFC) and the development of higher-order cognitive skills is not well understood. Recent findings show that the morphology of LPFC sulci predicts reasoning performance; this work led to the observation of substantial individual variability in the morphology of one of these sulci, the para-intermediate frontal sulcus (pimfs). Here, we sought to characterize this variability and assess its behavioral significance. To this end, we identified the pimfs in a developmental cohort of 72 participants, ages 6–18. Subsequent analyses revealed that the presence or absence of the ventral component of the pimfs was associated with reasoning, even when controlling for age. This finding shows that the cortex lining the banks of sulci can support the development of complex cognitive abilities and highlights the importance of considering individual differences in local morphology when exploring the neurodevelopmental basis of cognition.

Human perception requires complex cortical networks that function at neuroanatomical scales of microns and temporal scales of milliseconds. Despite this complexity, what if just one morphological feature of the brain could predict perceptual ability? Here, we tested this hypothesis with pre-registered analyses of neuroanatomy and face perception in neurotypical controls (NTs) and individuals with developmental prosopagnosia (DPs). Results show that the length of the mid-fusiform sulcus (MFS), a hominoid-specific tertiary sulcus in ventral temporal cortex (VTC), was shorter in DPs than NTs. Furthermore, individual differences in MFS length in the right, but not left, hemisphere predicted individual differences in face perception. These results support theories linking brain structure and function to perception, as well as indicate that one feature – variability in MFS length – can predict face perception. Finally, these findings add to growing evidence supporting a role of morphological variability of late developing, tertiary sulci and individual differences in cognition.

Recent findings spanning fields, from braincases in paleoneurobiology to invivo measurements in cognitive neuroscience, provide insights into the evolution of cognition. Here, we integrate these findings and propose that studying small, evolutionarily new cortical structures has significant implications for identifying new links between neuroanatomical substrates and human-specific aspects of cognition.

The neuroanatomical changes that underpin cognitive development is of major interest in neuroscience. Of the many aspects of neuroanatomy to consider, tertiary sulci are particularly appealing as they emerge last in gestation, show a protracted development after birth, and are either human- or hominoid-specific. Thus, they are ideal targets for exploring morphological-cognitive relationships with cognitive skills, such as verbal working memory (WM), that also show protracted development. Yet, the relationship between sulcal morphology and verbal WM is unknown, either in development or more generally. To fill this gap, we adopted a data-driven approach with cross-validation to examine the relationship between sulcal depth in lateral prefrontal cortex (LPFC) and verbal WM in 60 participants ages 6-18. These analyses identified nine left, but not right, LPFC sulci (of which six were tertiary) whose depth predicted verbal WM performance. Most of these sulci are located within and around contours of functionally defined parcellations of LPFC proposed previously. This sulcal depth model out-performed models with age or cortical thickness. Taken together, these findings contribute to building empirical support for a classic theory that tertiary sulci serve as landmarks in association cortices that contribute to aspects of human behavior that show a protracted development.

The lateral prefrontal cortex (LPFC) is disproportionately expanded in humans compared to non-human primates, although the relationship between LPFC brain structures and uniquely human cognitive skills is largely unknown. Here, we test the relationship between variability in LPFC tertiary sulcal morphology and reasoning scores in a cohort of children and adolescents. Using a data-driven approach in independent discovery and replication samples, we show that the depth of specific LPFC tertiary sulci is associated with individual differences in reasoning scores beyond age. To expedite discoveries in future neuroanatomical-behavioral studies, we share tertiary sulcal definitions with the field. These findings support a classic but largely untested theory linking the protracted development of tertiary sulci to late-developing cognitive processes., Tertiary sulci are shallow cortical folds that emerge late in gestation. Here the authors link prefrontal tertiary sulcal depth with reasoning scores in children and adolescents.

Comparative neuroanatomy studies improve understanding of brain structure and function and provide insight regarding brain development, evolution, and also what features of the brain are uniquely human. With modern methods such as diffusion MRI (dMRI) and quantitative MRI (qMRI), we are able to measure structural features of the brain with the same methods across human and non-human primates. In this review article, we discuss how recent dMRI measurements of vertical occipital connections in humans and macaques can be compared with previous findings from invasive anatomical studies that examined connectivity, including relatively forgotten classic strychnine neuronography studies. We then review recent progress in understanding the neuroanatomy of vertical connections within the occipitotemporal cortex by combining modern quantitative MRI and classical histological measurements in human and macaque. Finally, we a) discuss current limitations of dMRI and tractography and b) consider potential paths for future investigations using dMRI and tractography for comparative neuroanatomical studies of white matter tracts between species. While we focus on vertical association connections in visual cortex in the present paper, this same approach can be applied to other white matter tracts. Similar efforts are likely to continue to advance our understanding of the neuroanatomical features of the brain that are shared across species, as well as to distinguish the features that are uniquely human.

In the human brain, the mid-fusiform sulcus (MFS; sulcus sagittalis gyri fusiformis) divides the fusiform gyrus (FG) into lateral and medial partitions. Recent studies show that the MFS is identifiable in every hemisphere and is a landmark that identifies (a) cytoarchitectonic transitions among four areas of the FG, (b) functional transitions in many large-scale maps, and (c) the location of fine-scale functional regions. Thus, simply identifying the MFS in a person's brain provides researchers with knowledge regarding: (a) how cells are organized across layers within a particular cortical location, (b) how functional representations will be laid out in cortex, and (c) the precise location of functional regions from cortical folding alone. The predictive power of the MFS can guide future studies examining the anatomical-functional organization of the FG, as well as the development of translational applications for different patient populations. Nevertheless, progress has been slow in incorporating the MFS into the broader anatomical community and into neuroanatomical reference sources. For example, even though the MFS is a rare structural-functional landmark in human association cortex as just described, it is not recognized in the recently published Terminologia Neuroanatomica (TNA). In this review, I collate the anatomical and functional details of the MFS in one place for the first time. Together, this article serves as a comprehensive reference regarding the anatomical and functional details of the MFS, as well as provides a growing number of reasons to include the MFS as a recognized neuroanatomical structure in future revisions of the TNA. Anat Rec, 302:1491-1503, 2019. © 2018 American Association for Anatomy.

Primate cerebral cortex is highly convoluted with much of the cortical surface buried in sulcal folds. The origins of cortical folding and its functional relevance has been a major focus of systems and cognitive neuroscience. Stereotyped patterns of cortical folding across individuals and multiple primate species indicate common evolutionary pressures in their development. However, foundational questions regarding organizing principles shared across species remain unanswered. Taking a cross-species comparative approach with a careful consideration of historical observations, we investigate cortical folding within the calcarine sulcus, a primary fold in primates. We identify two macroanatomical structures – the retrocalcarine and external calcarine sulci – in 24 humans and 6 macaque monkeys. We show that within species, these sulci are identifiable in all individuals, fall on a similar part of the V1 retinotopic map, and thus, serve as anatomical landmarks predictive of functional organization. Yet, across species, the actual underlying visual field representations differ strikingly across humans and macaques. Thus, the structure-function correspondence for an evolutionarily old structure like V1 is species-specific and suggests intriguing differences in developmental constraints across primates.

Primate cerebral cortex is highly convoluted with much of the cortical surface buried in sulcal folds. The origins of cortical folding and its functional relevance have been a major focus of systems and cognitive neuroscience, especially when considering stereotyped patterns of cortical folding that are shared across individuals within a primate species and across multiple species. However, foundational questions regarding organizing principles shared across species remain unanswered. Taking a cross-species comparative approach with a careful consideration of historical observations, we investigate cortical folding relative to primary visual cortex (area V1). We identify two macroanatomical structures—the retrocalcarine and external calcarine sulci—in 24 humans and 6 macaque monkeys. We show that within species, these sulci are identifiable in all individuals, fall on a similar part of the V1 retinotopic map, and thus, serve as anatomical landmarks predictive of functional organization. Yet, across species, the underlying eccentricity representations corresponding to these macroanatomical structures differ strikingly across humans and macaques. Thus, the correspondence between retinotopic representation and cortical folding for an evolutionarily old structure like V1 is species-specific and suggests potential differences in developmental and experiential constraints across primates.

The inference of cortical sulcal labels often focuses on deep (primary and secondary) sulcal regions, whereas shallow (tertiary) sulcal regions are largely overlooked in the literature due to the scarcity of manual/well-defined annotations and their large neuroanatomical variability. In this paper, we present an automated framework for regional labeling of both primary/secondary and tertiary sulci of the dorsal portion of lateral prefrontal cortex (LPFC) using spherical convolutional neural networks. We propose two core components that enhance the inference of sulcal labels to overcome such large neuroanatomical variability: (1) surface data augmentation and (2) context-aware training. (1) To take into account neuroanatomical variability, we synthesize training data from the proposed feature space that embeds intermediate deformation trajectories of spherical data in a rigid to non-rigid fashion, which bridges an augmentation gap in conventional rotation data augmentation. (2) Moreover, we design a two-stage training process to improve labeling accuracy of tertiary sulci by informing the biological associations in neuroanatomy: inference of primary/secondary sulci and then their spatial likelihood to guide the definition of tertiary sulci. In the experiments, we evaluate our method on 13 deep and shallow sulci of human LPFC in two independent data sets with different age ranges: pediatric (N = 60) and adult (N = 36) cohorts. We compare the proposed method with a conventional multi-atlas approach and spherical convolutional neural networks without/with rotation data augmentation. In both cohorts, the proposed data augmentation improves labeling accuracy of deep and shallow sulci over the baselines, and the proposed context-aware training offers further improvement in the labeling of shallow sulci over the proposed data augmentation. We share our tools with the field and discuss applications of our results for understanding neuroanatomical-functional organization of LPFC and the rest of cortex (https://github.com/ilwoolyu/SphericalLabeling).

Stuss considered the human PFC as a “cognitive globe” [Stuss, D. T., & Benson, D. F. Neuropsychological studies of the frontal lobes. Psychological Bulletin, 95, 3–28, 1984] on which functions of the frontal lobe could be mapped. Here, we discuss classic and recent findings regarding the evolution, development, function, and cognitive role of shallow indentations or tertiary sulci in PFC, with the goal of using tertiary sulci to map the “cognitive globe” of PFC. First, we discuss lateral PFC (LPFC) tertiary sulci in classical anatomy and modern neuroimaging, as well as their development, with a focus on those within the middle frontal gyrus. Second, we discuss tertiary sulci in comparative neuroanatomy, focusing on primates. Third, we summarize recent findings showing the utility of tertiary sulci for understanding structural–functional relationships with functional network insights in ventromedial PFC and LPFC. Fourth, we revisit and update unresolved theoretical perspectives considered by C. Vogt and O. Vogt (Allgemeinere ergebnisse unserer hirnforschung. Journal für Psychologie und Neurologie, 25, 279–462, 1919) and F. Sanides (Structure and function of the human frontal lobe. Neuropsychologia, 2, 209–219, 1964) that tertiary sulci serve as landmarks for cortical gradients. Together, the consideration of these classic and recent findings indicate that tertiary sulci are situated in a unique position within the complexity of the “cognitive globe” of PFC: They are the smallest and shallowest of sulci in PFC, yet can offer insights that bridge spatial scales (microns to networks), modalities (functional connectivity to behavior), and species. As such, the map of tertiary sulci within each individual participant serves as a coordinate system specific to that individual on which functions may be further mapped. We conclude with new theoretical and methodological questions that, if answered in future research, will likely lead to mechanistic insight regarding the structure and function of human LPFC.

Existing models propose that primate visual cortex is divided into two functionally distinct pathways. The ventral pathway computes the identity of an object; the dorsal pathway computes the location of an object, and the actions related to that object. Despite remaining influential, the two visual pathways model requires revision. Both human and non-human primate studies reveal the existence of a third visual pathway on the lateral brain surface. This third pathway projects from early visual cortex, via motion-selective areas, into the superior temporal sulcus (STS). Studies demonstrating that the STS computes the actions of moving faces and bodies (e.g., expressions, eye-gaze, audio-visual integration, intention, mood) show that the third visual pathway is specialized for the dynamic aspects of social perception.

While the disproportionate expansion of lateral prefrontal cortex (LPFC) in humans compared to non-human primates is accepted, the relationship between evolutionarily new LPFC brain structures and uniquely human cognitive skills is largely unknown. Here, we tested the relationship between variability in evolutionarily new LPFC tertiary sulci and reasoning skills in a pediatric cohort. A novel data-driven approach in independent discovery and replication samples revealed that the depth of specific LPFC tertiary sulci predicts individual differences in reasoning skills beyond age. These findings support a classic, yet untested, theory linking the protracted development of tertiary sulci to late-developing cognitive processes. We suggest that deeper LPFC tertiary sulci reflect reduced short-range connections in white matter, which in turn, improve the efficiency of local neural signals underlying cognitive skills such as reasoning that are central to human cognitive development. To expedite discoveries in future neuroanatomical-behavioural studies, we share sulcal definitions with the field.

Understanding the relationship between neuroanatomy and function in portions of human cortex that are expanded compared to other mammals such as lateral prefrontal cortex (LPFC) is of major interest in systems and cognitive neuroscience. When considering neuroanatomical-functional relationships in LPFC, shallow indentations in cortex known as tertiary sulci have been largely ignored. Here, by implementing a multi-modal approach and manually defining 936 neuroanatomical structures in 72 hemispheres (males and females), we show that a subset of these overlooked tertiary sulci serve as a meso-scale link between microstructural (myelin content) and functional (network connectivity) properties of human LPFC in individuals. For example, the posterior middle frontal sulcus (pmfs) is a tertiary sulcus with three components that differ in their myelin content, resting state connectivity profiles, and engagement across meta-analyses of 83 cognitive tasks. Further, generating microstructural profiles of myelin content across cortical depths for each pmfs component and the surrounding middle frontal gyrus (MFG) shows that both gyral and sulcal components of the MFG have greater myelin content in deeper compared to superficial layers and that the myelin content in superficial layers of the gyral components is greater than sulcal components. These findings support a classic, yet largely unconsidered theory that tertiary sulci may serve as landmarks in association cortices, as well as a modern cognitive neuroscience theory proposing a functional hierarchy in LPFC. As there is a growing need for computational tools that automatically define tertiary sulci throughout cortex, we share pmfs probabilistic sulcal maps with the field.Significance statementLateral prefrontal cortex (LPFC) is critical for higher-order cognitive control and goal-directed behavior and is disproportionately expanded in the human brain. However, relationships between fine-scale neuroanatomical structures largely specific to hominoid cortex and functional properties of LPFC remain elusive. Here, we show that these structures, which have been largely neglected throughout history, surprisingly serve as markers for anatomical and functional organization in human LPFC. These findings have theoretical, methodological, developmental, and evolutionary implications for improved understanding of neuroanatomical-functional relationships not only in LPFC, but also in association cortices more broadly. Finally, these findings ignite new questions regarding how morphological features of these neglected neuroanatomical structures contribute to functions of association cortices that are critical for human-specific aspects of cognition.

Human ventral temporal cortex (VTC) is a cortical expanse that performs different functions and computations, but is especially critical for visual categorization. Nevertheless, accumulating evidence shows that category-selective regions persist in VTC in the absence of visual experience – for example, in congenitally blind (CB) participants. Despite this evidence, a large body of previous work comparing functional representations in VTC between sighted and CB participants performed univariate analyses at the group level, which assume a homogeneous population – an assumption that has not been formally tested until the present study. Specifically, using fMRI in CB and sighted participants (male and female), we empirically show that at the group level, distributed category representations in VTC are more reliable in the sighted (when viewing visual stimuli) compared to the CB (when hearing auditorily-substituted visual stimuli). Despite these group differences, there is extensive heterogeneity in VTC category representations in the CB to the point that VTC category representations in a subset of CB participants (some who were born without eyes, but not all) are more similar to sighted individuals compared to other CB participants. Together, our findings support a novel idea that driving factors contributing to the formation of VTC category representations in the blind are subject-specific, which complements factors that may generalize across group members. More broadly, the present findings caution conclusions of homogeneity across subjects within a group when performing group neuroimaging analyses without explicitly quantifying individual differences.

pFs is a functionally-defined region in the human brain that is involved in recognizing objects. A recent trend refers to pFs as the posterior fusiform sulcus, which is a neuroanatomical structure that does not exist. Here, we correct this mistake. To achieve this goal, we first recount the original definitions of pFs and then review the identification of sulci within and surrounding the fusiform gyrus (FG) including the mid-fusiform sulcus (MFS), which is a tertiary sulcus within the FG. We highlight that tertiary sulci, such as the MFS, are often absent from brain atlases, which complicates the accurate localization of functional regions, as well as the understanding of structural-functional relationships in ventral temporal cortex (VTC). When considering the location of object-selective pFs from previously published data relative to the sulci surrounding the FG, as well as the MFS, we illustrate that (1) pFs spans several macroanatomical structures, which is consistent with the original definitions of pFs (Grill-Spector etal., 1999, 2000), and (2) the topological relationship between pFs and MFS has both stable and variable features. To prevent future confusion regarding the anatomical location of functional regions within VTC, as well as to complement tools that automatically identify sulci surrounding the FG, we provide a method to automatically identify the MFS in individual brains using FreeSurfer. Finally, we highlight the benefits of using cortical surface reconstructions in large datasets to identify and quantify tertiary sulci compared to classic dissection methods because the latter often fail to differentiate tertiary sulci from shallow surface indentations produced by veins and arteries. Altogether, we propose that the inclusion of definitions and labels for tertiary sulci in neuroanatomical atlases and neuroimaging software packages will enhance understanding of functional-structural relationships throughout the human brain.

Repeated stimulus presentations commonly produce decreased neural responses - a phenomenon known as repetition suppression (RS) or adaptation – in ventral temporal cortex (VTC) in humans and nonhuman primates. However, the temporal features of RS in human VTC are not well understood. To fill this gap in knowledge, we utilized the precise spatial localization and high temporal resolution of electrocorticography (ECoG) from 9 human subjects implanted with intracranial electrodes in VTC. Subjects viewed non-repeated and repeated images of faces with (long-lagged) intervening stimuli between repeats. We report three main findings: (i) robust RS occurs for VTC activity in high-frequency broadband (HFB), but not lower frequency bands, (ii) RS is associated with lower peak magnitude, lower total responses of the HFB signal, and earlier peak responses, and (iii) RS effects occur early within initial stimulus processing and persist for the entire stimulus duration. We discuss these findings in the context of early and late components of visual perception, as well as theoretical models of RS in which these ECoG data empirically support timing predictions stemming from the facilitation model of RS in human VTC for the first time.

International audience; Human face perception requires a network of brain regions distributed throughout the occipital and temporal lobes with a right hemisphere advantage. Present theories consider this network as either a processing hierarchy beginning with the inferior occipital gyrus (occipital face area; IOG-faces/OFA) or a multiple-route network with nonhierarchical components. The former predicts that removing IOG-faces/OFA will detrimentally affect downstream stages, whereas the latter does not. We tested this prediction in a human patient (Patient S.P.) requiring removal of the right inferior occipital cortex, including IOG-faces/OFA. We acquired multiple fMRI measurements in Patient S.P. before and after a preplanned surgery and multiple measurements in typical controls, enabling both within-subject/across-session comparisons (Patient S.P. before resection vs Patient S.P. after resection) and between-subject/across-session comparisons (Patient S.P. vs controls). We found that the spatial topology and selectivity of downstream ipsilateral face-selective regions were stable 1 and 8 month(s) after surgery. Additionally, the reliability of distributed patterns of face selectivity in Patient S.P. before versus after resection was not different from across-session reliability in controls. Nevertheless, postoperatively, representations of visual space were typical in dorsal face-selective regions but atypical in ventral face-selective regions and V1 of the resected hemisphere. Diffusion weighted imaging in Patient S.P. and controls identifies white matter tracts connecting retinotopic areas to downstream face-selective regions, which may contribute to the stable and plastic features of the face network in Patient S.P. after surgery. Together, our results support a multiple-route network of face processing with nonhierarchical components and shed light on stable and plastic features of high-level visual cortex following focal brain damage.SIGNIFICANCE STATEMENT Brain networks consist of interconnected functional regions commonly organized in processing hierarchies. Prevailing theories predict that damage to the input of the hierarchy will detrimentally affect later stages. We tested this prediction with multiple brain measurements in a rare human patient requiring surgical removal of the putative input to a network processing faces. Surprisingly, the spatial topology and selectivity of downstream face-selective regions are stable after surgery. Nevertheless, representations of visual space were typical in dorsal face-selective regions but atypical in ventral face-selective regions and V1. White matter connections from outside the face network may support these stable and plastic features. As processing hierarchies are ubiquitous in biological and nonbiological systems, our results have pervasive implications for understanding the construction of resilient networks.

Burt Green Wilder (1841-1925) was a pioneering naturalist and anatomist who is historically known for his brain collection and for his contributions to neuroanatomical nomenclature. During his 42-year career, Wilder also used brain measurements for education and outreach, especially in regard to issues of race and gender. Additionally, Wilder influenced neuroscience education and acted as a scientific liaison to the public. For example, he designed early implementations of the sheep brain dissections that are still being conducted today, as well as likely conducted the first "Brain Day." This article reviews each of these topics, as well as others, with the aim of accurately placing Wilder in the history of neuroscience as a naturalist and anatomist who, among other achievements, pioneered the use of brain measurements for education and outreach.

Microstructural mechanisms underlying apparent cortical thinning during childhood development are unknown. Using functional, quantitative, and diffusion magnetic resonance imaging in children and adults, we tested if tissue growth (lower T1 relaxation time and mean diffusivity (MD)) or pruning (higher T1 and MD) underlies cortical thinning in ventral temporal cortex (VTC). After age 5, T1 and MD decreased in mid and deep cortex of functionally-defined regions in lateral VTC, and in their adjacent white matter. T1 and MD decreases were (i) consistent with tissue growth related to myelin proliferation, which we verified with adult postmortem histology and (ii) correlated with apparent cortical thinning. Thus, contrary to prevailing theories, cortical tissue does not thin during childhood, it becomes more myelinated, shifting the gray-white matter boundary deeper into cortex. As tissue growth is prominent in regions with protracted functional development, our data suggest an intriguing hypothesis that functional development and myelination are interlinked.

Throughout history, researchers who examine the structure and function of the brain debate one another about how cortical areas are defined, as well as how these areas should be named. Different pieces of empirical evidence are used to define brain areas and it is important to preserve the accurate history of this evidence and the timeline of studies that lead to areal definitions that are either still used today or have been modified. As such, this paper traces the early history of a brain area located at the junction between the occipital and temporal lobes of the macaque known as TEO. This historical analysis leads to four main findings. First, even though Bonin and Bailey are credited with the definition of area TEO in 1947, they did not have the cytoarchitectonic evidence to support the distinction of TEO from adjacent areas. Second, the first evidence definitively separating area TEO from TE was actually based on connectivity as identified with strychnine neuronography by Petr et al. in 1949. Third, causal evidence from ablation studies conducted by Iwai and Mishkin (Experimental Neurology 25(4):585–594, 1969) supported this distinction by showing that TEO and TE were functionally distinct from one another. Fourth, researchers in the 1970s began referring to TEO as posterior inferotemporal (PIT) and TE as anterior inferotemporal (AIT), which is an important historical clarification as the PIT/AIT nomenclature is presently attributed to studies conducted more than a decade later. Altogether, this paper aims to preserve the historical origin of area TEO, as well as the empirical evidence that was used to originally differentiate this cortical expanse from surrounding areas.

Prevailing hierarchical models propose that temporal processing capacity--the amount of information that a brain region processes in a unit time--decreases at higher stages in the ventral stream regardless of domain. However, it is unknown if temporal processing capacities are domain general or domain specific in human high-level visual cortex. Using a novel fMRI paradigm, we measured temporal capacities of functional regions in high-level visual cortex. Contrary to hierarchical models, our data reveal domain-specific processing capacities as follows: (1) regions processing information from different domains have differential temporal capacities within each stage of the visual hierarchy and (2) domain-specific regions display the same temporal capacity regardless of their position in the processing hierarchy. In general, character-selective regions have the lowest capacity, face- and place-selective regions have an intermediate capacity, and body-selective regions have the highest capacity. Notably, domain-specific temporal processing capacities are not apparent in V1 and have perceptual implications. Behavioral testing revealed that the encoding capacity of body images is higher than that of characters, faces, and places, and there is a correspondence between peak encoding rates and cortical capacities for characters and bodies. The present evidence supports a model in which the natural statistics of temporal information in the visual world may affect domain-specific temporal processing and encoding capacities. These findings suggest that the functional organization of high-level visual cortex may be constrained by temporal characteristics of stimuli in the natural world, and this temporal capacity is a characteristic of domain-specific networks in high-level visual cortex. Significance statement: Visual stimuli bombard us at different rates every day. For example, words and scenes are typically stationary and vary at slow rates. In contrast, bodies are dynamic and typically change at faster rates. Using a novel fMRI paradigm, we measured temporal processing capacities of functional regions in human high-level visual cortex. Contrary to prevailing theories, we find that different regions have different processing capacities, which have behavioral implications. In general, character-selective regions have the lowest capacity, face- and place-selective regions have an intermediate capacity, and body-selective regions have the highest capacity. These results suggest that temporal processing capacity is a characteristic of domain-specific networks in high-level visual cortex and contributes to the segregation of cortical regions.

Summary Ventral temporal cortex (VTC) is the latest stage of the ventral "what" visual pathway, which is thought to code the identity of a stimulus regardless of its position or size [1, 2]. Surprisingly, recent studies show that position information can be decoded from VTC [3–5]. However, the computational mechanisms by which spatial information is encoded in VTC are unknown. Furthermore, how attention influences spatial representations in human VTC is also unknown because the effect of attention on spatial representations has only been examined in the dorsal "where" visual pathway [6–10]. Here, we fill these significant gaps in knowledge using an approach that combines functional magnetic resonance imaging and sophisticated computational methods. We first develop a population receptive field (pRF) model [11, 12] of spatial responses in human VTC. Consisting of spatial summation followed by a compressive nonlinearity, this model accurately predicts responses of individual voxels to stimuli at any position and size, explains how spatial information is encoded, and reveals a functional hierarchy in VTC. We then manipulate attention and use our model to decipher the effects of attention. We find that attention to the stimulus systematically and selectively modulates responses in VTC, but not early visual areas. Locally, attention increases eccentricity, size, and gain of individual pRFs, thereby increasing position tolerance. However, globally, these effects reduce uncertainty regarding stimulus location and actually increase position sensitivity of distributed responses across VTC. These results demonstrate that attention actively shapes and enhances spatial representations in the ventral visual pathway.

Face perception is critical for normal social functioning and is mediated by a network of regions in the ventral visual stream. In this review, we describe recent neuroimaging findings regarding the macro- and microscopic anatomical features of the ventral face network, the characteristics of white matter connections, and basic computations performed by population receptive fields within face-selective regions composing this network. We emphasize the importance of the neural tissue properties and white matter connections of each region, as these anatomical properties may be tightly linked to the functional characteristics of the ventral face network. We end by considering how empirical investigations of the neural architecture of the face network may inform the development of computational models and shed light on how computations in the face network enable efficient face perception.

We compare the major white matter tracts in human and macaque occipital lobe using diffusion MRI. The comparison suggests similarities but also significant differences in spatial arrangement and relative sizes of the tracts. There are several apparently homologous tracts in the two species, including the vertical occipital fasciculus (VOF), optic radiation, forceps major, and inferior longitudinal fasciculus (ILF). There is one large human tract, the inferior fronto-occipital fasciculus, with no corresponding fasciculus in macaque. The macaque VOF is compact and its fibers intertwine with the dorsal segment of the ILF, but the human VOF is much more elongated in the anterior-posterior direction and may be lateral to the ILF. These similarities and differences will be useful in establishing which circuitry in the macaque can serve as an accurate model for human visual cortex.Contact informationHiromasa Takemura, Center for Information and Neural Networks (CiNet), National Institute of Information and Communications Technology, and Osaka University, Japan htakemur@nict.go.jpAuthor contributionDesigned the study: HT FP BAW. Performed the experiments. HT FP GAK SML JS FQY DAL WAF NKL. Analyzed the data. HT FP KSW MAB BAW. Contributed analysis tools. FP KSW MAB. Wrote the paper. HT FP KSW BAW.

The goal of cognitive neuroscience is to understand how mental operations are performed by the brain. Given the complexity of the brain, this is a challenging endeavor that requires the development of formal models. Here, we provide a perspective on models of neural information processing in cognitive neuroscience. We define what these models are, explain why they are useful, and specify criteria for evaluating models. We also highlight the difference between functional and mechanistic models, and call attention to the value that neuroanatomy has for understanding brain function. Based on the principles we propose, we proceed to evaluate the merit of recently touted deep neural network models. We contend that these models are promising, but substantial work is necessary to (i) clarify what type of explanation these models provide, (ii) determine what specific effects they accurately explain, and (iii) improve our understanding of how they work.