On presentation of the human cerebral sulci from inside of the cerebrum

Abstract

The human cerebral cortex is highly convoluted forming patterns of gyri separated by sulci. The cerebral sulci and gyri are fundamental in cortical anatomy as well as neuroimage processing and analysis. Narrow and deep cerebral sulci are not fully discernible either on the cortical or white matter surface. To cope with this limitation, I propose a new sulci presentation method that employs the inner cortical surface for sulci examination from the inside of the cerebrum. The method has four steps, construct the cortical surface, segment and label the sulci, dissect (open) the cortical surface, and explore the fully exposed sulci from the inside. The inside sulcal maps are created for the left and right lateral, left and right medial, and basal hemispheric surfaces with the sulci parcellated by color and labeled. These three‐dimensional sulcal maps presented here are probably the first of this kind created. The proposed method demonstrates the full course and depths of sulci, including narrow, deep, and/or convoluted sulci, which has an educational value and facilitates their quantification. In particular, it provides a straightforward identification of sulcal pits which are valuable markers in studying neurologic disorders. It enhances the visibility of sulci variations by exposing branches, segments, and inter‐sulcal continuity. The inside view also clearly demonstrates the sulcal wall skewness along with its variability and enables its assessment. Lastly, this method exposes the sulcal 3‐hinges introduced here.

Narrow and deep human cerebral sulci are not fully discernible or on the cortical or white matter surface. To cope with this limitation, I employ the inner cortical surface for sulci examination from the inside of the cerebrum. The inside sulcal maps are created for the left and right lateral, left and right medial, and basal hemispheric surfaces with the sulci parcellated by color and labeled. The inside view also demonstrates the sulcal wall skewness and exposes sulcal 3‐hinges.

1. INTRODUCTION

The human cerebral cortex is highly convoluted forming patterns of gyri separated by sulci. The sulcal patterns are very characteristic for humans, whereas the individual sulci present extensive variability (Nieuwenhuys et al., 2008). The cerebral sulci and gyri are fundamental in cortical anatomy as well as neuroimage processing and analysis. Sulcal‐related neuroimage processing and analysis are employed, among others, in brain registration (Thompson & Toga, 1996), examination of healthy brain variations (Mangin et al., 2004), investigation of discrepancies between normal and diseased brains (Ashburner et al., 2003), age‐related studies (Kochunov et al., 2005), gyro‐sulcal functional difference studies (Wang et al., 2023), morphometry (Yun et al., 2013), and especially cortical folding analysis that may provide insight into the biological underpinnings of diseases (Lefrere et al., 2023), such as a reduced sulcal depth in depression (Shin et al., 2022) and a decreased number of sulcal pits in attention‐deficit/hyperactivity disorder (Li et al., 2021).

The sulcal anatomy is typically presented on the cortical (hemispheric) surface. This presentation, however, is incomplete as two‐thirds of the cortical surface is hidden deeply in the walls of the sulci (Nolte, 2009). Consequently, the course, continuity, shape, size, width, depth, side branches, and pattern of a sulcus cannot be fully demonstrated. To cope with this problem, I have earlier proposed a new method for sulci presentation by employing dual spatially co‐registered surfaces, the cortical surface and the white matter surface (Nowinski, 2022a). Subsequently, I have created 64 dual‐image labeled sulcal maps serving as a sulcal reference, with eight orthogonal maps including the anterior, left lateral, posterior, right lateral, superior, inferior, medial left, and medial right maps presented in Nowinski (2022a) and 54 sulcus‐oriented maps put for public use at the NOWinBRAIN three‐dimensional (3D) neuroimage repository in gallery G9 at https://www.nowinbrain.org/index.php?/category/1936.

Despite its advantages, this novel way of sulci presentation along with the created sulcal maps has a certain limitation, as the course and depth of some narrow and deep sulci may not be fully depicted. Therefore, here I propose another method aiming to employ the inner cortical surface and examine the sulci from the inside of the cerebrum.

The main purpose of this work is threefold to (1) describe this new method of sulcal presentation, (2) illustrate the resulting inner sulcal maps with the sulci parcellated by color and labeled on the inner lateral, medial, and basal orthogonal cortical surfaces, and (3) discuss method's advantages including exposing the full course and depths of sulci, enhancing the visibility of variations of the sulci by depicting their branches and segments as well as inter‐sulcal continuity, facilitating quantification (including a straightforward localization of the sulcal pits), clearly exhibiting the sulcal wall skewness and its properties, and exposing and illustrating the sulcal 3‐hinges introduced here. Moreover, future extensions are proposed including the combination of both methods and the creation of sulcal maps with the triplets of spatially corresponding images.

2. MATERIAL AND METHOD

The method has four steps: construction of the entire cortical surface, segmentation and labeling of the cerebral sulci to be explored, dissection (opening) of the cortical surface by a given plane, and exploration of the sulci from the inside.

To construct the cortical surface, some existing methods can be employed, for example, those proposed by Dale and Sereno (1993) and Dale et al. (1999). A comparison of various cortical surface reconstruction algorithms, including Freesurfer, BrainVISA, and CLASP, is presented by Lee et al. (2006). Such a cortical surface is polygonal, composed of triangles with known coordinates of their vertices.

To segment the sulci, several methods can be used which employ various approaches (such as region growing, watersheds, curvatures, and zero level of convexity) as reviewed by Nowinski (2022a). A segmented sulcus remains a polygonal model. A sulcus can be distinguished by applying a unique color. Then, all the triangles in the sulcus shall be colored with the same color on both sides. A table with the mapping from a given color to the corresponding sulcal index is constructed to enable sulcal labeling (naming).

The cortical surface as a polygonal model can be intersected by another polygonal model, in particular, dissected by a plane. This dissection can efficiently be computed by polygonal surface clipping which refers to the process of removing parts of a polygonal surface that lie outside a given viewing region. Clipping is a standard operation in computer graphics and several algorithms are proposed for it, for example, the Liang‐Barsky and Sutherland‐Hodgman algorithms (Foley et al., 1996).

A dissected cortical surface is opened and can be explored either from its outside or inside as proposed here. To create 3D realistic images, surface lighting and shading which are standard computer graphics techniques are applied on both surface sides (Foley et al., 1996).

To embody the method and illustrate the results, a 3D interactive atlas The Human Brain, Head and Neck in 2953 Pieces by Nowinski et al. (2015) is used to generate (static) images. The atlas contains a dissectible virtual brain model with the cortical surface parceled into color‐coded sulci and gyri located in a stereotactic space based on the anterior and posterior commissures as well as provides automatic color‐based structure labeling (Nowinski, 2017).

3. RESULTS AND DISCUSSION

The cerebral sulci from the inside of the cerebrum are presented on five orthogonal hemispheric surfaces, namely, the left and right lateral, left and right medial, and basal for both hemispheres. The cerebral sulci are parcellated by color and labeled.

Figure 1 demonstrates the inside presentation of the left and right lateral hemispheric surfaces. The left surface is viewed from the right (top image), and the right surface is viewed from the left (bottom image). In each view, the corresponding sagittal dissecting plane is set 25 mm apart from the midsagittal plane.

FIGURE 1.

Inside presentation of the left and right lateral hemispheric surfaces with the cerebral sulci parcellated by color and labeled: (top image) the left surface viewed from the right; (bottom image) the right surface viewed from the left. In each view, the hemispheric surface is sagittally dissected at 25 mm from the midsagittal plane.

On the lateral hemispheric surface, depending on the location of a sagittal dissection plane, the following sulci may be fully or partly visible from the inside: central, precentral, postcentral, superior frontal, inferior frontal, frontomarginal, frontoorbital, superior temporal, inferior temporal, intraparietal, angular, parieto‐occipital, superior occipital, inferior occipital, lunate, collateral, occipitotemporal, lateral (Sylvian fissure), and orbital sulci (Figure 1). The most important landmarks on the lateral hemispheric surface are the Sylvian fissure and central sulcus (Rhoton, 2003; Figure 1). The course, width, and depth of the central sulcus, separating the frontal and parietal lobes and the sensory and motor areas, are clearly visible from the inside (Figure 1). The Sylvian fissure, demarcating the frontal and parietal lobes from the temporal lobe, is complicated and contains a superficial and a deep (cisternal) part. The deep part of the Sylvian fissure, which is more complex than the superficial part, is divided into sphenoidal (anterior) and operculoinsular (posterior) compartments. This deep part, especially the medial wall formed by the insula, is visible only when the lips of the Sylvian fissure are widely separated (Rhoton, 2003; Figure 2). With the proposed presentation, the deep part of the Sylvian fissure including the insula is exposed (Figure 1).

FIGURE 2.

Inside presentation of the left and right medial hemispheric surfaces with the cerebral sulci parcellated by color and labeled: (top image) the left surface viewed from the left; (bottom image) the right surface viewed from the right. In each view, the hemispheric surface is sagittally dissected at 20 mm from the midsagittal plane.

Figure 2 illustrates the inside presentation of the left and right medial hemispheric surfaces. The left surface is viewed from the left (top image), and the right surface is viewed from the right (bottom image). In each view, the corresponding sagittal dissecting plane is set 20 mm apart from the midsagittal plane.

On the medial hemispheric surface, depending on the location of a sagittal dissection plane, the following sulci may be fully or partly visible from the inside: callosal, cingulate, parieto‐occipital, subparietal, superior rostral, inferior rostral, central, postcentral, transverse occipital, and lunate sulcus (note that the rhinal sulcus is on the outer surface). In particular, the parieto‐occipital sulcus (or fissure), which separates the parietal and occipital lobes as well as the precuneus and cuneus, forms a deep and convoluted cleft. Therefore, this sulcus is hardly visible from the outside contrary to its inside view (Figure 2). It is also clearly evident that the parieto‐occipital sulcus joins the anterior calcarine sulcus forming a Y‐shape configuration (Rhoton, 2003; Figure 2). Moreover, on the inside medial hemispheric surface, the callosal and cingulate sulci are fully exposed and they mark a three‐layer organization formed by the corpus callosum, the cingulate gyrus, and the medial frontal gyrus (Figure 2).

The inside presentation of the basal hemispheric surface viewed from the top is shown in Figure 3. The surface is dissected axially at the commissural level.

FIGURE 3.

Inside presentation of the basal hemispheric surface (superior view) dissected axially at the commissural level with color‐coded and labeled sulci.

On the basal cortical surface, depending on the location of a sagittal dissection plane, the following sulci may be fully or partly visible from the inside: olfactory, superior rostral, inferior rostral, frontoorbital, frontomarginal, cingulate, collateral, occipitotemporal, superior temporal, inferior temporal, lateral, inferior occipital, lunate, calcarine, and orbital sulci. Although there are no complex sulci on the basal surface, such as the Sylvian and parieto‐occipital fissures, the inside view nicely exposes narrow sulci, such as the olfactory, collateral, occipitotemporal, and H‐shaped orbital sulci (Figure 3).

There are several approaches to present the human cerebral sulci as reviewed in (Nowinski, 2022a). In particular, multiple electronic brain dissections reveal the course of intracranial arteries running deeply within the cerebral sulci (Nowinski, 2022b). To improve the presentation of deep and narrow sulci, I propose to use the inner cortical surface and examine the sulci from the inside of the cerebrum as illustrated here on the lateral, medial, and basal orthogonal surfaces. The introduced method for sulci presentation is new and produces novel, yet unfamiliar, and possibly a bit challenging images of sulci. A resulting sulcus image may be termed a “negative image”, a “sulcal cast” in the parenchyma, or an “inside‐out” view. To my best knowledge, the neuroanatomical images created here are probably the first of this kind demonstrated.

Besides exposing the full course and depths of sulci, including deep, narrow, and/or convoluted sulci, the inside presentation has several other advantages. Namely, on the inside surfaces certain sulcal folding patterns are formed as the conjunction of three sulcal crests. Earlier, Zhang et al. (2020) introduced a gyral folding pattern termed a 3‐hinge defined as the conjunction of three gyral crests and claimed that these gyral 3‐hinges could serve as hubs in a cortico‐cortical connective network. Consequently, I term these sulcal patterns the sulcal 3‐hinges. According to a review by Jiang et al. (2021), the functional connectivity between gyro‐gyral regions is strong and sulco‐sulcal regions is weak, so the sulcal 3‐hinges, contrary to their gyral counterparts, rather do not play the role of hubs, but they may be a sort of “information forks.” They also may play some special role similar to the sulcal pits considered below. Sulcal 3‐hinges are present on both sides of the Sylvian fissure and precentral sulcus (Figure 1); cingulate sulcus, subparietal sulcus, and calcarine sulcus (Figure 2); collateral sulcus, parietotemporal sulcus, and orbital sulci (double each) (Figure 3).

I have earlier introduced the sulcal wall skewness that characterizes the amount of shift between the sulcus midline at its top and the fundus line at its bottom (Nowinski, 2022a). The inside view clearly demonstrates this skewness along with its variability and facilitates its quantification, as observable, for instance, for the olfactory sulcus and collateral sulcus (Figure 3).

The inside view also enhances the visibility of variations by exposing the sulcal branches and segments as well as inter‐sulcal continuity. For instance, sulcal continuity or connectivity is noticeable for the left and right superior temporal sulcus with the angular sulcus (Figure 1), the left and right inferior frontal sulcus with the precentral sulcus (Figure 1), the left inferior frontal sulcus with the frontomarginal sulcus (Figure 1 top) (consequently three sulci the precentral, inferior frontal and frontomarginal are connected), the left and right calcarine sulcus with the parieto‐occipital sulcus (Figure 2), the left cingulate sulcus with the subparietal sulcus (Figure 2 bottom), and the right postcentral sulcus with the intraparietal sulcus (Figure 1 bottom).

Having the complete, fully exposed sulci facilitates their quantification especially since the brain atlas employed is stereotactic and provides the coordinate readout (Nowinski, 2017) making the measurement of the Euclidean sulcal depth easy. In particular, the identification and localization (by providing the stereotactic coordinates) of sulcal pits, that is, the deepest local points of sulcal fundi, is straightforward with our approach as the sulcal pits simply become the highest local points of an examined sulcus. The sulcal pits are important anatomical features closely related to human brain function (Im & Grant, 2019) and valuable markers to distinguish atypical from typical patterns of development by means of sulcal pit‐based analyses, as has been demonstrated in autism spectrum disorder (Brun et al., 2016), dyslexia (Im et al., 2016), attention‐deficit/hyperactivity disorder (Li et al., 2021), and bipolar disorders (Lefrere et al., 2023).

It shall be noted that the use of static images with fixed views may impose some restrictions on sulcus presentation for certain sulci and viewing directions. In particular, the 3D manifestation and depth of dark and narrow sulci whose walls are close to parallel to the viewing direction may not be fully apparent, as, for example, for the calcarine sulcus in the medial view (Figure 2). Some sulci are dark as a sulcus color setting is influenced by the colors of its surrounding gyri. As narrow sulci have small areas on the outer cortical surface, the color complementarity was applied to better reflect the difference between large gyral and small sulcal outer regions. A suitable change in view usually improves the sulcus appearance, see, for example, the superior view of the calcarine sulcus in Figure 3 where the sulcal walls are more perpendicular to the viewing direction.

A natural extension of this work is threefold, namely, (1) the creation of sequences of orthogonal sulcal maps for various locations of the dissecting plane, (2) the creation of individual sulcus‐oriented, view‐dependent maps providing maximum exposure for each examined sulcus, and (3) combining the dual cortical‐white matter surface sulcal maps with those created by the proposed method and generation of triple‐image orthogonal and sulcus‐oriented maps. The last extension bridges the novel method proposed here and the already‐known approaches for sulci presentation facilitating its acceptance.

FUNDING INFORMATION

This publication is supported by the European Union's Horizon 2020 research and innovation program under grant agreement Sano No 857533. This publication is supported by Sano project carried out within the International Research Agendas program of the Foundation for Polish Science and co‐financed by the European Union under the European Regional Development Fund.

CONFLICT OF INTEREST STATEMENT

The author declared no conflict of interest.

Nowinski, W.L. (2023) On presentation of the human cerebral sulci from inside of the cerebrum. Journal of Anatomy, 243, 690–696. Available from: 10.1111/joa.13880

DATA AVAILABILITY STATEMENT

The presented method is freely available.