Anatomical delineations of the chimpanzee cerebellum
The chimpanzee cerebellum was segmented into its lobular components and the average volume of each region was computed (Table 1). Given that this atlas is meant to provide a basis for comparisons with the human cerebellum and that human cerebellar nomenclature has undergone extensive revisions, care was taken in this section to ensure that it is clear how the lobules presented herein correspond to the most common terminology used in current human cerebellar literature. The anterior lobe consists of 5 lobules: lobules I, II, III, IV, and V (Fig. 2). In accordance with previous work done in the human cerebellum, there is no true vermis in the anterior lobe of the chimpanzee cerebellum (Schmahmann et al. 1999). Therefore, all lobules of the anterior lobe are presented including the combination of both the vermal and hemispheric portions. In Larsell’s (1970) nomenclature, lobules I and II are referred to as the lingula, lobule III is the centralis or central lobule, and lobules IV and V comprise the culmen. It is worth noting that lobule V is sometimes referred to as the anterior portion of the quadrangular lobe in light of the classic cerebellar schema devised by Henle (1901) that is modified and used by Press et al. (1989). A comparison of common cerebellar nomenclature systems is provided in Table 2.
Table 1: Chimpanzee Cerebellar Atlas Delineations and ROI Volumes
Structure
|
Color Code
|
Volume (mm3)
|
Lobules of the cerebellar anterior lobe
|
|
|
Right I/II
|
|
32.24
|
Right III
|
|
261.71
|
Right IV
|
|
1234.46
|
Right V
|
|
1236.17
|
Left I/II
|
|
32.93
|
Left III
|
|
348.49
|
Left IV
|
|
1276.99
|
Left V
|
|
1154.54
|
Hemispheric lobules of the cerebellar posterior lobe
|
|
|
Right HVI
|
|
3168.29
|
Right Crus I of HVII
|
|
5495.20
|
Right Crus II of HVII
|
|
1176.15
|
Right HVIIB
|
|
393.76
|
Right HVIIIA
|
|
437.67
|
Right HVIIIB
|
|
622.54
|
Right XI
|
|
533.71
|
Left HVI
|
|
3172.75
|
Left Crus I of HVII
|
|
5144.66
|
Left Crus II of HVII
|
|
1712.60
|
Left HVIIB
|
|
566.64
|
Left HVIIIA
|
|
435.95
|
Left HVIIIB
|
|
500.78
|
Left XI
|
|
533.36
|
Lobules of the Flocculonodular lobe
|
|
|
Right X
|
|
153.32
|
Left X
|
|
153.32
|
Vermis X
|
|
162.93
|
Vermis of Posterior Lobe
|
|
|
Vermis VI
|
|
528.91
|
Vermis VIIAa (Crus I)
|
|
55.57
|
Vermis VIIAb (Crus II)
|
|
47.68
|
Vermis VIIB
|
|
60.37
|
Vermis VIIIA
|
|
316.59
|
Vermis VIIIB
|
|
168.07
|
Vermis IX
|
|
285.72
|
Table 2
Comparison of Cerebellar Nomenclature Systems
Structures in this Atlas
Parks et al. (2022)
|
Consensus
|
Larsell (1936–1972)
|
Schmahmann et al. (1999)
|
Press et al. (1989)
Courchesne et al. (1989)
|
Lobules of the cerebellar anterior lobe**
|
Lobule I/II
|
Lingula
|
I,II
lingula
|
I, II
|
Lingula
|
Lobule III
|
Centralis
|
III
centralis
|
III
|
Central lobule
|
Lobule IV
|
Culmen
|
IV
culmen
|
IV
|
Quadrangular lobule, anterior portion
|
Lobule V
|
V
culmen
|
V
|
Hemispheric lobules of the cerebellar posterior lobe
|
Lobule HVI
|
Simplex
|
H VI
Lobulus simplex
|
VI
|
Quadrangular lobule,
posterior portion
|
Lobule Crus I of HVII
|
Crus I,
Semilunar lobule
|
Crus I of
H VIIA/
lobuli ansiformis
|
Crus I
|
Semilunar lobule,
Superior portion
|
Lobule Crus II of HVII
|
Crus II,
Semilunar lobule
|
Crus II of
H VIIA/
lobuli ansiformis
|
Crus II
|
Semilunar lobule,
Inferior portion
|
Lobule HVIIB
|
HVIIB,
Paramedian lobule
|
H VIIB
lobulus paramedianus
|
VIIB
|
Gracile lobule
|
Lobule HVIIIA
|
Biventer lobule
|
H VIIIA
lobulus biventer,
pars copularis
|
VIIIA
|
Biventer lobule
|
Lobule HVIIIB
|
H VIIIB
Lobulus biventer, pars paraflocculus dorsalis
|
VIIIB
|
Lobule XI
|
Tonsil
|
Paraflocculus ventralis
|
IX
|
Tonsil
|
Lobules of the Flocculonodular lobe
|
Lobule HX
|
Flocculus
|
Flocculus
|
X
|
Flocculus
|
Vermis X
|
Nodulus
|
X, Nodulus
|
X
|
Nodule
|
Vermis of Posterior Lobe
|
Vermis VI
|
Declive
|
VI, declive
|
VI
|
Declive
|
Vermis VIIAa (Crus I)
|
Folium
|
VIIA, folium
|
VIIAf
|
Folium Vermis
|
Vermis VIIAb (Crus II)
|
Tuber
|
VIIA, tuber
|
VIIAt
|
Tuber Vermis
|
Vermis VIIB
|
Caudal aspect of tuber
|
VIIB
Caudal aspect of tuber
|
VIIB
|
Vermis VIIIA
|
Pyramis
|
VIIIA, pyramis
|
VIIIA
|
Pyramis
|
Vermis VIIIB
|
Pyramis
|
VIIIB, pyramis
|
VIIIB
|
Vermis IX
|
Uvula
|
IX, uvula
|
IX
|
Uvula
|
Table 3
Structure
|
Dice Similarity Coefficient (DSC) across raters
|
Right Crus I
|
0.85
|
Right Crus II
|
0.78
|
Right HVIIB
|
0.73
|
Vermis VI
|
0.84
|
Vermis X
|
0.83
|
The posterior lobe consists of a midline vermis and two hemispheric portions that extend laterally from the vermis. The vermal lobules of the posterior lobe are lobules VII, VIIAf, VIIAt, VIIB, VIIIA, VIIIB, and IX (Fig. 3). Vermal lobule VI comprises the declive. Vermal VIIA (the combination of VIIAf and VIIAt) comprise the folium/tuber. In this atlas, VIIAf and VIIAt of Schmahmann (Schmahmann et al. 1999) nomenclature are referred to as Vermis Crus I and Vermis Crus II, respectively, for easy comparison with the human MRI cerebellar atlas of Diedrichsen (Diedrichsen et al. 2009). This also avoids confusion regarding which vermal segments of lobule VII correspond to the hemispheric extensions of lobule VII. Vermis VIIB is the caudal aspect of the tuber according to Larsell (1970). Vermis lobule VII corresponds to the pyramis, while vermal lobule IX is regarded as the uvula.
The hemispheres of the posterior lobe are broad and extend laterally. Hemispheric lobules of the posterior lobe of the cerebellum include lobules HVI, lobule HVII (including Crus I, Crus II, and HVIIB), lobule HVIII (including HVIIIA and HVIIIB), and lobule HIX (Fig. 4). In Larsell’s nomenclature, HVI is the lobulus simplex, but it is often referred to as the posterior portion of the quadrangular lobe following the classifications of Press et al. (1989). Crus I and Crus II of HVIIIA are commonly referred to as the ansiform lobule of Larsell (1970) or the semilunar lobule of Press et al. (1989), respectively. HVIIB is the paramedian lobule of Larsell (1970) or the gracile lobule of Press et al. (1989). Lobule HVIII is collectively referred to as the biventer lobule (Press et al. 1989). In Larsell’s nomenclature, lobule HVIIIA is lobulus biventer, pars copularis and lobule HVIIIB is lobulus biventer, pars paraflocculus dorsalis. Lobule HIX corresponds to the ventral paraflocculus of Larsell (1970) or the tonsil of classical nomenclature. All hemispheric lobules are bilateral; thus, all hemispheric lobules drawn in this atlas comprise separately delineated right and left masks.
Finally, the flocculonodular lobe of the cerebellum comprises the vermal lobule X, the nodulus, and the HX, the flocculus.
Cerebellar segmentation relies on the ability to identify cerebellar fissures, which divide the cerebellum into lobes and subdivide those into lobules (Fig. 5). The midline portions of most fissures can be most readily identified in the midsagittal section (Fig. 5A). The anterior lobe is divided from the posterior lobe by the primary fissure and the posterior lobe is separated from the flocculonodular lobe by the posterolateral fissure. The relationship between lobules and fissures are described in the results presented here. The following anatomical delineations correspond to the structures listed in Table 1.
Lobules of the cerebellar anterior lobe
Lobule I/II – Consistent with the human cerebellum, lobules I and II of the anterior lobe do not extend laterally into the hemispheres (Fig. 6C, arrow a). The folia of lobules I and II are merged together. In accordance with Larsell, Lobule I/II are defined as the folia covering the medullary sheath that is continuous with the anterior medullary velum (Fig. 6A). The furrow separating lobules I and II, referred to as a homologue of “precentral fissure a” by Larsell, is not distinguishable in the MR images. The superior extent of the lobule II is defined by the presence of the precentral fissure.
Lobule III – Lobule III of the chimpanzee cerebellum extends anteriorly before terminating superficially as two large lamellae (Fig. 7B, white arrows). Unlike lobules I and II, lobule III extends laterally such that it contains both a midline and a hemispheric component (Fig. 7C). Lobule III is bounded anteriorly by the precentral sulcus and posteriorly by the preculminate sulcus.
Lobule IV – Lobule IV extends from the same medullary ray that gives rise to Lobule V, such that lobule IV appears to be branching directly off of Lobule V (Fig. 8A). Because of this, the intraculminate fissure that separates Lobules IV and V is shallow in comparison to the preculminate fissure (located anterior to lobule IV) as well as the deep primary fissure that is located posterior to lobule V (Fig. 8A, dotted lines). Lobule IV extends anteriorly and terminates as two large, very distinct lamellae (Fig. 8, white arrows).
Lobule V – In the MRI atlas, Lobule V extends supero-posteriorly as two large lamellae with the faint presence of four superficial lamellae (Fig. 9A, lamellae a,b). The lack of distinct boundaries between superficial lamellae are likely a result of group averaging given the relatively large amount of variation in the superficial lamellae of the chimpanzee lobule V with respect to other lobules of the anterior lobe (Larsell 1970). Two deep lamellae extend from the posterior aspect of its medullary ray (Fig. 9A, lamellae c,d). These are buried deep in the primary fissure, which is the posterior boundary of Lobule V. The depth and width of the primary fissure is easily identifiable in all three cross sections (Fig. 9, dotted line). The primary fissure also defines the posterior boundary of the anterior lobe and the anterior boundary of the posterior lobe of the cerebellum. Unlike Lobules III and IV, there is a clear separation between the midline (vermal) portion of lobule V and its lateral, hemispheric component (Figs. 9B and 9C). This distinction can be visualized most clearly in the horizontal cross section.
Lobules of the cerebellar vermis of the posterior lobe
Vermis Lobule VI – The foliations of vermal lobule VI are most clearly visible in the midsagittal section (Fig. 10A). Lobule VI vermis extends posterosuperiorly and terminates superficially in three superficial lamellae (Fig. 10A, lamellae a, b, and c). Three anteriorly located, deep lamellae are buried deep within the primary fissure (Fig. 10A, lamellae d, e, f). In the midsagittal section, lobule VI vermis is seen branching anteriorly off of the same medullary ray as lobule VII vermis (Fig. 10A, “MR”). Lobules VI is demarcated posteriorly by the shallow superior posterior fissure (Fig. 10, dotted line), thus dividing the superficial lamellae of lobules VI and VII such that they appear as a fork at the end of the medullary ray. All boundaries between the vermal and hemispheric components of a lobule, including those of lobule VI, were identified in the horizontal cross section (Fig. 10B, white arrows).
Vermis Lobule VII – The vermis of lobule VII is divided into 2 sublobules, lobules VIIA and VIIB (Figs. 11 and 12). Rather than lying adjacent to its own hemispheric expansions, the vermis of VIIA is positioned medial to the posterior lamellae of lobule HVI (Larsell 1970; see Fig. 11). Sublobule VIIA is further divided into lobules VIIAa and VIIAb, corresponding to vermal Crus I and vermal Crus II of the human MRI cerebellar atlas, respectively (Schmahmann et al. 2000; Diedrichsen et al. 2009). The vermal portions of Crus I and Crus II are relatively small at the midsagittal section, extending superficially as two indistinct lamellae (Fig. 12A, “VIIA”). The presence of the horizontal fissure, which separates these lobules, was indeterminate in the midsagittal section (Fig. 12A). Previous evidence suggests that there is more variability in the sublobules of lobule VII (Larsell 1970). Based on visual inspection of individual chimpanzees, we observed that the blurring of vermal VII’s sublobules are likely due to the effects of averaging across more variable lobules. Therefore, the distinction between vermal Crus I (VIIAa) and vermal Crus II (VIIAb) relied on the presence of the horizontal fissure in the coronal section (Fig. 12B). The vermis of sublobule VIIA is defined posteriorly by the shallow ansoparamedian, which dually serves as the anterior boundary of the vermis of VIIB (Fig. 12A, “ap”). The vermis of VIIB is a single, elongate lamellae extending posteroinferiorly from the sublobule VIIA (Fig. 12A, “VIIB”). It is distinguished from the vermis lobule VIII by a deep prepyramidal (or prebiventer) fissure (Fig. 12A, “pp”).
Vermis Lobule VIII – The vermis of lobule VIII is split into two clear sublobules, VIIIA and VIIIB, by a deep intrapyramidal (or intrabiventer) sulcus (Fig. 13). Two short folia extending posteriorly and inferiorly from VIIIA are apparent in the horizontal and coronal cross sections (Figs. 13B and 13C, “a” and “b”). These folia are separate from the midsagittal cleft of VIIIB by the continuation of the intrabiventer (or intrapyramidal) fissure, such that they are directly lateral to VIIIB, but not continuous with it (Fig. 13B, note “VIIIB” position relative to “a” and “b” marked by white arrows). VIIIB also has two short folia that extend inferiorly (Fig. 13D, “d” and “e”) and they are situated just inferior to the short folia of VIIIA (Fig. 13D, “a” and “b”), although they do not project as far posteriorly as the short folia of VIIIA. VIIB is defined posteriorly by the presence of the deep secondary fissure, which marks the anterior boundary of the vermis IX (Fig. 13, “sec”).
Vermis Lobule IX – Lobule IX is relatively large in the midsagittal section, with clear ventral and dorsal divisions that extend posteroinferiorly (Fig. 14A, “v” and “d”). The ventral and dorsal divisions of vermis lobule IX are separated by a deep uvular sulcus 1 (Larsell 1970) (Fig. 14A, “uv1”). Each of the divisions terminates in two superficial lamellae; however, the superficial lamellae cannot be distinguished from one another in the midsagittal section of the MRI scans at current resolution. Vermal lobule IX is very narrow and is defined laterally and anteriorly by the presence of a deep posterolateral fissure (Fig. 14, “pl”). The posterolateral fissure divides the posterior lobe from the flocculonodular lobe of the cerebellum.
Hemispheric lobules of the posterior lobe of the cerebellum
Lobule HVI – Lobule HVI has an extensive superficial surface that extends laterally and terminates as 4 superficial lamellae (Fig. 15, white arrows). Lobule HVI divides into a pars anterior and a pars posterior by a deep fissure that is clearly present across all sections (Fig. 15, “PA”, “PP”, and “f”, respectively). The pars anterior of HVI is continuous with vermal sublobules VIe, VIa, and VIb at the midline (although only VIa and VIb are visible superficially, see Fig. 11). Pars posterior of HVI is most closely associated with vermal Crus I (VIIAa) and vermal Crus II (VIIAb) (Fig. 11). HVI is bounded posteriorly from HVII by the posterolateral fissure (Fig. 16, “pl”), while the pars posterior of HVI is delineated medially from vermal VIIA (i.e. vermal Crus I and vermal Crus II) by the deep continuation of the superior posterior fissure (Fig. 16, “sp”).
Crus I of Lobule HVII – Lobule HVIIA refers to the combination of two hemispheric lobules, Crus I and Crus II, which are separated from one another by a deep horizontal fissure (Fig. 17, “hor”). Crus I is further subdivided into an anterior and posterior division. The anterior division is small and projects superiorly and anteriorly in the posterior wall of the posterolateral fissure (Fig. 17, white arrows). The posterior portion of Crus I (Fig. 17, bracket) is much larger, and it marks the lateral-most extent of the cerebellum. In the axial cross section, one medullary ray (Fig. 17, asterisk) extends laterally before creating a Y-shaped fork that gives Crus I its idiosyncratic shape.
Crus II of Lobule HVII – Crus II is bounded superiorly and anteriorly by the horizontal fissure and posteriorly by the ansoparamedian fissure (Fig. 18, “hor” and “ap”). In the coronal section, it is apparent that the hemispheric and vermal portions of the ansoparamedian fissure do not align at the lateral aspect of the vermis, such that the vermal portion of the fissure is located superior to the hemispheric portion (Fig. 18B, white arrow). Thus, Crus II is associated medially with lateral-most expansions of the vermis of lobule HVIIIa (Fig. 18B, “a” and “b”). The medullary ray of Crus II arches anteriorly and medially towards the white matter of Crus I (Fig. 18B, “MR”). Crus II extends superficially as two distinct lamellae and is defined posteriorly by the posterior aspect of the transverse cerebellar fossa (Fig. 18A, “TCF”).
Lobule HVIIB – HVIIB projects inferolaterally from the medullary ray of Crus II (Fig. 19). HVIIB is defined superolaterally by the ansoparamedian fissure, posteriorly by the transverse cerebellar fossa, and medially by the prepyramidal (prebiventer) fissure (Fig. 19, “ap”, “TCF”, “pp”). In the horizontal cross sections, lobule HVIIB can be described as arching from posteromedial to the lateral, inferior surface of the cerebellum (Fig. 19B).
Lobule HVIIIA – Lobule HVIIIA is defined laterally by the prepyramidal fissure and medially by the intrapyramidal (intrabiventer) fissure (Fig. 20, “pp” and “ip”, respectively). HVIIIA is medial and parallel to HVIIB (Fig. 20A, not HVIIIA position relative to HVIIB). It comprises three superficially projecting lamellae; however, these divisions are unclear at the current resolution. The intrapyramidal fissure is deep and clearly separates the lamellae of HVIIIA from those of the more medially located HVIIIB (Fig. 20, “ip”).
Lobule HVIIIB – As noted by Larsell (1970), HVIIIB is ‘almond-shaped’ and is connected to the vermis of VIIIB by a short peduncle (Fig. 21, green crosshatch “p”). It is defined laterally by the intrapyramidal (intrabiventer) fissure and medially by the secondary fissure (Fig. 20, “ip” and “sec”, respectively). Its lamellae project inferomedially whereas the lamellae of HVIIIA project inferolaterally (Fig. 20). Lobules HVIIIA and HVIIIB correspond to the human biventer lobule.
Lobule HIX – Lobule HIX, the cerebellar tonsil, is defined laterally by the presence of the secondary fissure and medially by the deep posterolateral fissure, which separates the posterior lobe from the flocculonodular lobe (Figs. 22 and 23, “sec” and “pl”, respectively). The tonsils lie lateral to the vermal portion of lobule IX, the uvula; however, there is no apparent continuity between the folia of the tonsil and the vermal portion of lobule IX (Fig. 22B). This observation is consistent with those of Larsell (1970).
Flocculonodular lobe
Vermis Lobule X (Nodule) – Vermal lobule X, the nodule, is defined in the midsagittal section as the relatively large, inferiorly-projecting lamellae that is separated posteriorly from vermal IX by the presence of the deep posterolateral fissure (Fig. 23A, “pl”). The nodule is bounded anteriorly by a thin layer of meningeal pia mater and ependyma called the inferior (or posterior) medullary vellum, which lines the inferior border of the 4th ventricle (Fig. 23A, “4V”).
Hemispheric Lobule X (Flocculus) – Hemispheric lobule HX, known more commonly as the flocculus, is the lateral-most extent of the flocculonodular lobe (Figs. 23B and 23C). Previous evidence suggests that the chimpanzee flocculus is relatively large, protruding farther laterally than it does in humans (Larsell 1970). The middle cerebellar peduncle passes from anteromedial, superior, and then posterolateral to the flocculus, forming its superior-most boundary (Fig. 23C, “MCP”). The flocculus is defined posteriorly by the presence of the posterolateral fissure (Fig. 23B).
Interobserver reliability of delineation protocols
Five masks were selected in which to test interrater reliability using dice similarity coefficients (DSC). Our dice coefficients range from 0.73 DSC (Right HVIIB) to 0.85 (Right Crus II), demonstrating high interobserver reliability between anatomists. Thus, the results of the delineation protocol provided here are highly reproducible between observers (Table 2).