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3 Pivotal Insights: The Contributions of Gordon Holmes (1876–1965) and Olof Larsell (1886–1964) to Our Understanding…

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pig, and human using developmental stages and adult specimens (Larsell 1952, 1953a, b, 1954; Larsell and Dow 1939; Larsell and Whitlock 1952). Using these mammals, he clearly showed that the mature mammalian cerebellum was composed of subdivisions called “… lobules…”.

I have pointed out…the striking similarities between folia I–X of birds and the vermian segments of the rat which the present investigation has brought to light … I shall call these segments lobules I–X, corresponding to the similarly named avian folia.

Each lobule of the vermis, beginning with the lingual and ending with the nodulus, was identied by Roman numerals (I, II, III … X). The lateral extension of each vermis lobule, the hemisphere portion, was identied by the same Roman numeral but with the prex H (HII, HIII … HX) specifying “hemisphere portion of…”. Larsell recognized that the basic pattern of a cerebellar plate being transected by two ssures (joining to make one– the posterolateral) formed a larger corpus cerebelli and a smaller occulonodular lobe. In concert, he noted that the development of the primary ssure, the second to appear and rst in the corpus cerebelli, resulted in an anterior lobe (lobules I–V) and a posterior lobe (lobules VI–IX); the further development of additional ssures in these lobes clearly established to a fundamental plan. He postulated that this 10 lobule arrangement would prove to be applicable to a wide range of forms, a point well-taken.

In studying Larsell’s correspondence with Herrick, it is clear that he was a quiet, reserved man who was concerned about the wider impact of his life-long work. In a letter to Herrick (dated July 20, 1948), Larsell says:

I treaded on Brouwer’s and Ingvar’s toes somewhat– gently

enough I hope…, but I do not think my work will need

repeating.

Indeed, it did not merit repeating, and by the late 1950s and 1960s was adopted by giants of the day and, to the present, is the standard.

References

Angevine JB, Mancall EL, Yakolev PI (1961) The human cerebellum:

an atlas of gross topography in serial sections. Little Brown and

Company, Boston, pp1–138 Haines DE (1999) In: Garraty JA, Carnes MC (eds) American

national biography, vol 13. Oxford University Press, NewYork,

pp204–206 Holmes G (1917) The symptoms of acute cerebellar injuries due to gun-

shot. Brain 40:461–535 Holmes G (1922a) Clinical symptoms of cerebellar disease and their

interpretation, lecture I.Lancet 202:1178–1182 Holmes G (1922b) Clinical symptoms of cerebellar disease and their

interpretation, lecture II.Lancet 202:1232–1237

Holmes G (1922c) Clinical symptoms of cerebellar disease and their

interpretation, lecture III.Lancet 203:59–65

Holmes G (1922d) Clinical symptoms of cerebellar disease and their

interpretation, lecture IV.Lancet 203:111–115

Koehler PJ, Bruyn GW, Pearce JMS (2000) Neurological eponyms.

Oxford University Press, Oxford, pp172–178

Larsell O (1920) The cerebellum of amblystoma. J Comp Neurol

31:259–282 Larsell O (1923) The cerebellum of the frog. J Comp Neurol 36:89–112 Larsell O (1925) The development of the cerebellum in the frog (Hyla

regilla) in relation to the vestibular and lateral-line systems. J Comp

Neurol 39:249–289 Larsell O (1926) The cerebellum of reptiles: lizards and snake. J Comp

Neurol 41:59–94 Larsell O (1931) The cerebellum of Triturus torosus. J Comp Neurol

53:1–54 Larsell O (1932a) The cerebellum of reptiles: chelonians and alligator.

J Comp Neurol 56:299–345 Larsell O (1932b) The development of the cerebellum in amblystoma. J

Comp Neurol 54:357–435 Larsell O (1934) Morphogenesis and evolution of the cerebellum. Arch

Neurol Psychiatry (Chicago) 31:373–395 Larsell O (1935) The development and morphology of the cerebellum

in the opossum. Part I.Early development. J Comp Neurol 63:65–94 Larsell O (1936a) The development and morphology of the cerebel-

lum in the opossum. Part II.Later development and adult. J Comp

Neurol 63:251–291 Larsell O (1936b) Cerebellum and corpus pontobulbare of the bat

(Myotis). J Comp Neurol 64:275–302 Larsell O (1937) The cerebellum: a review and interpretation. Arch

Neurol Psychiatry (Chicago) 38:580–607 Larsell O (1945) Comparative neurology and present knowledge of the

cerebellum. Bull Minn Med Found 5:73–85 Larsell O (1947a) The cerebellum of myxinoids and petro-myzonts,

including developmental stages in the lampreys. J Comp Neurol

86:395–445 Larsell O (1947b) The development of the cerebellum in man in rela-

tion to its comparative anatomy. J Comp Neurol 87:85–129 Larsell O (1948) The development and subdivisions of the cerebellum

of birds. J Comp Neurol 89:123–189 Larsell O (1952) The morphogenesis and adult pattern of the lobules

and ssures of the cerebellum of the white rat. J Comp Neurol

97:281–356 Larsell O (1953a) The cerebellum of the cat and the monkey. J Comp

Neurol 99:135–199 Larsell O (1953b) The anterior lobe of the mammalian and the human

cerebellum. Anat Rec 115:341 Larsell O (1954) The development of the cerebellum of the pig. Anat

Rec 118:73–107 Larsell O, Dow RS (1939) The cerebellum: a new interpretation. West J

Surg Obstet Gynaecol 47:256–263 Larsell O, Jansen J (1967) The comparative anatomy and histology

of the cerebellum from myxinoid through birds. The University of

Minnesota Press, Minneapolis, pp1–291 Larsell O, Jansen J (1970) The comparative anatomy and histology of

the cerebellum from monotremes through apes. The University of

Minnesota Press, Minneapolis, pp1–269 Larsell O, Jansen J (1973) The comparative anatomy and histology of

the cerebellum: the human cerebellum, cerebellar connections, and

cerebellar cortex. The University of Minnesota Press, Minneapolis,

pp1–268 Larsell O, Whitlock DG (1952) Further observations on the cerebellum

of birds. J Comp Neurol 97:545–566

Part II

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Anatomy and Histology of the Cerebellum

Gross Anatomy oftheCerebellum

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JanVoogd andEnricoMarani

Abstract

1776) many different nomenclatures have been proposed for the gross anatomy of the cerebellum (Angevine Jr etal. The human cerebellum, Little Brown and Company, Boston, 1961). Here we will consider the classical nomenclature of the human cerebellum and the comparative anatomical nomenclatures of Bolk (Das cerebellum der säugetiere, Fischer, Haarlem, 1906), Larsell (J Comp Neurol 97:281–356, 1952), and Larsell and Jansen (The comparative anatomy and histology of the cerebellum. III. The human cerebellum, cerebellar connections, and cerebellar cortex, University of Minnesota Press, Minneapolis, 1972) and their application to the human cerebellum, and to the small cerebellum of the mouse.

Keywords

Vermis · Hemisphere · Fissures · Lobules · Folal cains Mouse cerebellum · Human cerebellum

J. Voogd (*) Department of Neuroscience, Erasmus Medical Center Rotterdam, Rotterdam, The Netherlands e-mail: janvoogd@bart.nl

E. Marani MIRA Institute for Biomedical Engineering and Technical Medicine, Department of Electrical Engineering, Mathematics and Computer Science, Biomedical Signals and Systems Group, University of Twente, Enschede, The Netherlands

After the rst description of the cerebellar foliation by Vincenzo Malacarne (1744–1816) in his “Vera struttura del cervelletto umano” (the genuine structure of the human cerebellum, 1776) many different nomenclatures have been proposed for the gross anatomy of the cerebellum (Angevine Jr etal. 1961). Here we will consider the classical nomenclature of the human cerebellum and the comparative anatomical nomenclatures of Bolk (1906), Larsell (1952), and Larsell and Jansen (1972) and their application to the human cerebellum, and to the small cerebellum of the mouse.

In the classical nomenclature of the human cerebellum vermis and hemispheres, separated by the paramedian sulcus, are distinguished (Figs.4.1, right panel and 4.2). The paramedian sulcus is shallow in the anterior cerebellum but is a deep cleft posterior to the posterior superior sulcus. Here, the cortex can be interrupted, with white matter appearing at the surface. In the antero-posterior subdivision, the cerebellum is divided into anterior and posterior lobes, separated by the primary fissure, the deepest fissure on a midsagittal section of the cerebellum. Names of the lobules are derived from their shape or their resemblance to particular structures (Malacarne

1776; Glickstein etal. 2009).

Bolk (1906) based his nomenclature on the comparison of numerous species of mammals. Bolk considered the vermis and the hemispheres as folial chains (Figs.4.1, left panel and

4.2e). The cortex within a chain is always continuous, in the

paramedian sulcus the cortex, or more precisely, the parallel bers in the molecular layer may be interrupted. In the anterior lobe and in the simplex lobule, located immediately caudal to the primary ssure, the folial chains of the vermis and hemisphere are aligned and the transverse ssures continue uninterruptedly from the vermis into the hemisphere. Caudal to the simplex lobule, the folial chain of the hemisphere makes two loops, the ansiform lobule and the paraocculus. The most caudal lobule of the folial chain of the hemisphere, the occulus, is reected upon the distal part of the paraocculus. The cortex in the center of the ansiform lobule, lateral

© The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 D. L. Gruol et al. (eds.), Essentials of Cerebellum and Cerebellar Disorders, https://doi.org/10.1007/978-3-031-15070-8_4

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J. Voogd and E. Marani

Fig. 4.1 Nomenclature of the cerebellum. Left panel illustrates the comparative anatomical nomenclature for the hemisphere and Larsell’s (1952) numbering system for the lobules of the vermis and hemispheres. Right panel shows the classical nomenclature of the human

to the folium/tuber (Larsell’s lobule VII) is interrupted. The rostral and caudal limbs of the folial loop of the ansiform lobule are known as the Crus I and II.The cortex is absent between the caudal vermal lobules, the uvula and the nodulus (IX and X), and the paraocculus (HIX) and the occulus (HX). The rostral and caudal limbs of the paraocculus are known as the dorsal and ventral paraocculus. At the level of the paramedian lobule, located between the ansiform lobule and the paraocculus, the folial chains of vermis and hemispheres are aligned and the paramedian sulcus is indistinct. Interlobular ssures, if present, continue uninterruptedly from the pyramis (VIII) into the paramedian lobule.

Larsell (1952) emphasized the medio-lateral continuity of the lobules of vermis and hemispheres. He distinguished 10 lobules in the vermis, indicated with the roman numerals I–X (Fig. 4.1, left panel). Their hemispheral counterparts are indicated with the prex H. From Larsell’s description, it becomes clear that the paramedian lobule consists of rostral and caudal subdivisions. Its rostral portion (lobule HVIIB, the gracile lobule) is continuous with vermal lobule VII, and

cerebellum. The homology of these lobules is indicated using the same color. Asterisks denote areas devoid of cortex in the center of folial rosettes of the ansiform lobule and the paraocculus. Cop copula pyramidis, PMV posterior medullary velum

its caudal portion (HVIII: the copula pyramidis) is continuous with lobule VIII (the pyramis).

Several MRI atlases of the human cerebellum have been published (Schmahmann etal. 2000; Dietrichsen etal. 2009). They use a mixture of the classical and comparative anatomical nomenclatures, retaining the terms Crus I and II of the ansiform lobule. In applying Larsell’s numeral system, they discarded the prex H for lobules of the hemisphere, thus introducing some confusion because it is not always clear whether lobules of vermis or hemispheres are meant.

For the homology of the paraocculus and the occulus with lobules in the human cerebellum, it is important to note that the cortex of the occulus can be subdivided into ve longitudinal Purkinje cell zones (Voogd and Barmack 2006; Schonewille etal. 2006). Two zonal pairs connect through vestibulo-oculomotor neurons with the external eye muscles. In most mammals, these occular zones extend for some distance on the ventral paraocculus. In monkeys, they occupy the entire ventral paraocculus. A narrow cortical bridge connects the ventral with the dorsal paraocculus. In the

4 Gross Anatomy oftheCerebellum

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Fig. 4.2 (a–c) Anterior, dorsal, and posterior views of the human cer- ebellum. Red lines indicate the direction of the folial chains of vermis and hemispheres. (d) Midsagittally sectioned human cerebellum. (e) Bolk (1906) diagram of the folial chains of vermis and hemispheres. (e) Dissection of the posterior cerebellum after removal of the tonsil. (f)

human cerebellum, this cortical bridge is broken. The dorsal paraocculus is represented by the tonsil and the ventral paraocculus by the accessory paraocculus. In most mammals, the folial loop of the paraocculus is directed laterally.

folial loops of the ansiform lobule and the paraocculus, Ce central lobule, Cu culmen, De declive, Fol/Tu folium and tuber vermis, N nodulus, PFLD dorsal paraocculus, PFLV ventral paraocculus, Py pyramis, Uv uvula, Vma anterior medullary velum

lobe and the simplex lobule.1 An area without cortex is present lateral to lobule VII in the center of the ansiform lobule and lateral to the rostral paramedian lobule. White matter in the paramedian sulcus separates lobules IX and

The folial loop of the tonsil, however, is directed medially (Fig.4.2f).

The cerebellum of the mouse conforms to Bolk’s general pattern (Marani and Voogd 1979). In the anterior lobe, the lobules (H) I and II and (H) IV and V are fused (Fig. 4.3). A paramedian sulcus is absent in the anterior

Because the vermis projects to the fastigial and vestibular nuclei, the lateral border of the vermis is located latral to the Purkuinje cell zone B that projects to the lateral vestibular nucleus. The location of the B zone in the anterior cerebellum and lobule VIII was established for the rat by Voogd and Ruigrok (2004) the corresponding white matter comprtment was located for the mouse by Marani (1986).

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J. Voogd and E. Marani

Fig. 4.3 The cerebellum of the mouse. (a–d) Anterior, dorsal, poste- rior, and ventral views of the cerebellum of the mouse. Interruptions of the cortex are indicated in red. (e) View of the midsagittaly sectioned molecular layer of the cerebellum of the mouse. Dotted line indicates the attachment of the roof of the fourth ventricle. (f) Lateral view of a reconstruction of the molecular layer of the cerebellum of the mouse.

Note continuity between the copula pyramidis and the paraocculus. Arrows point to regions where the cortex is interrupted [Modied from Marani and Voogd (1979)]. Drawings by Jan Tinkelenberg. ANS ansiform lobule, COP copula pyramidis, CrI, II Crus I II of the ansiform lobule, FLO occulus, PFL paraocculus, PMD paramedian lobule, SIM simplex lobule

X from the paraocculus and the occulus. The cortexless areas extend from the paramedian sulcus into the superior part of the lobules IX and X.The copula pyramidis (HVIII) lateral continues into the dorsal paraocculus. The folial loop of the paraocculus remains separated from the para-

median lobule by the white matter in the paraoccular sulcus, an extension of the white matter surrounding the cerebellum. The paraocculus is incompletely divided into dorsal and ventral limbs by the intraparaoccular sulcus on the medial side of this lobule.

4 Gross Anatomy oftheCerebellum

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References

Angevine JNB Jr, Mancall EL, Yakovlev PI (1961) The human cerebel-

lum. Little Brown and Company, Boston Bolk L (1906) Das cerebellum der säugetiere. Fischer, Haarlem Dietrichsen J, Balsters JH, Flavell J, Cussans E, Ramnani M (2009)

A probabilistic MR atlas of the human cerebellum. Neuroimage

46:39–46 Glickstein M, Strata P, Voogd J (2009) Cerebellum: history. Rev

Neurosci 162:549–559 Larsell O (1952) The morphogenesis and adult pattern of the lobules

and tissues of the cerebellum of the white rat. J Comp Neurol

97:281–356 Larsell O, Jansen J (1972) The comparative anatomy and histology

of the cerebellum. III. The human cerebellum, cerebellar con-

nections, and cerebellar cortex. University of Minnesota Press,

Minneapolis

Malacarne V (1776) Nuova esposizione della vera struttura del cervel-

letto umano. G.Briolo, Torino

Marani E (1986) Topographic histochemistry of the cerebellum. Prog

Histol Cytochem 16:1–169

Marani E, Voogd J (1979) The morphology of the mouse cerebellum.

Acata Morphol Neerl Scand 17:33–52

Schmahmann JD, Doyon D, Toga AW, Petrides M, Evans AC (2000)

MRI atlas of the human cerebellum. Academic Press, San Diego

Schonewille M, Luo G, Ruigrok TJ, Voogd J, Schmolesky MT,

Rutteman M, Hoebeek FE, de Jeu FE, de Zeeuw CI (2006) Zonal organization of the mouse occulus: physiology, input and output. J Comp Neurol 497:670–682

Voogd J, Barmack NH (2006) Oculomotor cerebellum. Prog Brain Res

151:231–268

Voogd J, Ruigrok TJ (2004) The organization of the corticonuclear and

olivocerebellar climbing ber projections to the rat cerebellar vermis: the congruence of projection zones and the zebrin pattern. J Neurocytol 33:5–21

Vascular Supply andTerritories

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oftheCerebellum

QiaoshuWang andLouisR.Caplan

Abstract

Within the posterior circulation, Caplan and colleagues

characterized brain and vascular structures as involving

the proximal, middle, and distal posterior circulation ter-

ritories. The proximal intracranial posterior circulation

territory includes regions supplied by the intracranial ver-

tebral arteries (ICVAs)– the medulla oblongata, and the

posterior inferior cerebellar arteries (PICAs) – supplied

region of the cerebellum. The ICVAs join at the medullo-

pontine junction to form the basilar artery (BA). The mid-

dle intracranial posterior circulation territory includes

the portion of the brain supplied by the BA up to its supe-

rior cerebellar artery (SCA) branches– the pons and the

anterior inferior cerebellar arteries (AICAs) – supplied

portions of the cerebellum. The BA divides to form the

two posterior cerebral arteries (PCAs) at the junction

between the pons and the midbrain, just beyond the ori-

gins of the SCAs. The distal intracranial posterior circu-

lation territory includes all of the territory supplied by the

rostral BA and its SCA, PCA, and their penetrating artery

branches– midbrain, thalamus, SCA– supplied cerebel-

lum and PCA territories.

Keywords

Cerebellum · Vertebral artery · Brainstem · Basilar artery

Cerebellar arteries

Q. Wang (*) Shanghai General Hospital, Shanghai, China

L. R. Caplan Beth Israel deaconess Medical Center, Boston, MA, USA e-mail: lcaplan@bidmc.harvard.edu

5.1 Overview

Within the posterior circulation, Caplan and colleagues characterized brain and vascular structures as involving the proximal, middle, and distal posterior circulation territories (Caplan 1996, 2000; Caplan etal. 2004, 2005; Chaves etal.

1994; Savitz and Caplan 2005). The proximal intracranial

posterior circulation territory includes regions supplied by the intracranial vertebral arteries (ICVAs) – the medulla oblongata, and the posterior inferior cerebellar arteries (PICAs) – supplied region of the cerebellum. The ICVAs join at the medullopontine junction to form the basilar artery (BA). The middle intracranial posterior circulation territory includes the portion of the brain supplied by the BA up to its superior cerebellar artery (SCA) branches, the pons, and the AICA –supplied portions of the cerebellum. The BA divides to form the two posterior cerebral arteries (PCAs) at the junction between the pons and the midbrain, just beyond the origins of the superior SCAs. The distal intracranial poste- rior circulation territory includes all of the territory supplied by the rostral BA and its SCA, PCA, and their penetrating artery branches– midbrain, thalamus, SCA– supplied cerebellum and PCA territories. This distribution is shown diagrammatically in Fig.5.1.

The three surfaces of the cerebellum are: tentorial (or superior) facing the tentorium cerebelli, petrosal facing toward the petrous bone, and suboccipital facing the suboccipital bone located between the lateral and sigmoid dural sinuses (Lister etal. 1982). The PICAs encircle the medulla and supply the suboccipital cerebellar surface; the AICAs course around the pons and supply the petrosal surface of the cerebellum, and the SCAs encircle the midbrain and supply the tentorial, superior surface of the cerebellum (Lister etal. 1982).

The arteries to the cerebellum are distributed rostrocaudally so that the PICAs arise from the ICVAs, the anterior inferior cerebellar arteries (AICAs) arise from the BA, and the most rostral arteries, the SCAs, arise near the BA bifurcation (Fig.5.2). The PICAs and the SCAs, the two largest arte-

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Q. Wang and L. R. Caplan

Fig. 5.1 Schema of the proximal, middle, and distal intracranial territories of the vertebrobasilar arterial system (Drawn by Laurel Cook-Lowe

1978, modeled after a gure in Duvernoy 1978)

5 Vascular Supply andTerritories oftheCerebellum

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Fig. 5.2 Schematic diagram of the cerebellar arteries. 1 Superior cer- ebellar artery (SCA); 2 medial branch of the SCA; 3 lateral branch of the SCA; 4 anterior inferior cerebellar artery (AICA); 5 posterior inferior cerebellar artery (PICA); 6 medial branch of PICA; 7 lateral branch of PICA; 8 basilar artery; 9 vertebral artery (From Amarenco 1991)

rial pairs have medial branches that supply mostly the vermian and paravermian portions of their respective regions of the cerebellum, and lateral branches which supply the cerebellar hemispheres. Infarcts in the cerebellum are often limited to the territory of one of these branches, e.g., medial PICA (mPICA), lateral SCA (lSCA), etc. These cerebellar branch territory infarcts correspond to functional regions such as the inferior vermis or superior lateral neocerebellum. The AICAs, in contrast, supply only a small part of the anterior inferior cerebellum and the occulus, but their major supply is to the lateral pontine tegmentum and the brachium pontis. The AICAs do not divide into medial and lateral major cerebellar branches but give off twigs to various structures.

5.2 Posterior Inferior Cerebellar Arteries (PICAs)

The PICAs usually originate from the ICVAs about 2 cm below the origin of the basilar artery, and, on average, about

8.6mm above the foramen magnum (Marinkovic etal. 1995).

The site of origin, however, varies from 14mm below the foramen magnum to 26 mm above the foramen magnum (Marinkovic etal. 1995). About 10% arise from the basilar artery (Amarenco and Hauw 1989). Size varies; the diameters varied between 0.58 and 2.10mm in one analysis (Amarenco and Hauw 1989). Some ICVAs end in PICA, and PICA can be absent in which case there usually is a large artery that arises from the proximal basilar artery that supplies both the PICA and AICA territories. Occasionally, PICA is duplicated.

After coursing laterally and downward to go around the

lateral medulla (the lateral medullary segment), the PICAs

Fig. 5.3 Sketch showing course and branching of the posterior inferior cerebellar artery (PICA). 1 PICA; 2 lateral branch of PICA; 3 medial branch of PICA; 4 cerebellar hemisphere; 5 cerebellar vermis; 6 cerebellar tonsil (Reproduced with permission from Amarenco etal. 1993)

make a cranially directed loop and ascend between the dorsal portion of the medulla and the caudal part of the cerebellar tonsil on that side (the tonsillomedullary segment) (Lister etal. 1982; Marinkovic etal. 1995). They then make a second loop above the cranial portion of the tonsil and descend along the inferior vermis coursing between the inferior medullary velum and the rostral portion of the tonsil (the telovelotonsillar segment). Finally, the artery becomes supercial and supplies branches to the tonsil, medulla, choroid plexus, and cerebellar cortex. Medial and lateral branches (mPICA, and lPICA) arise from the main trunks (Fig.5.3) at variable locations between the two PICA loops. mPICA supplies the inferior vermis including the nodulus, pyramis, uvula, tuber, and sometimes the declive and the medial portions of the semilunar lobule, gracile lobule, and the tonsil (Chaves etal. 1994; Amarenco and Hauw 1989; Amarenco etal. 1989, 1993; Amarenco 1991; Gilman et al. 1981; Duvernoy 1978). mPICA often sends a supply to the dorsal medulla. lPICA supplies the inferior twothirds of the biventer, most of the inferior portion of the semilunar and the gracile lobules, and the anterolateral portion of the tonsil (Chaves et al. 1994; Amarenco and Hauw 1989; Amarenco etal. 1989, 1993; Amarenco 1991; Gilman et al.

1981; Duvernoy 1978). Figures5.4, 5.5, and 5.6 show dia-

grammatically the supply territories of PICA, mPICA, and lPICA, respectively. The PICAs sometimes supply the deep cerebellar structures including the fastigial nuclei but usually do not supply the dentate nuclei (Amarenco and Hauw 1989).

Although many equate the Wallenberg syndrome with an occlusion of PICA causing infarction in the lateral medulla, PICA does not supply the lateral medullary tegmentum. This region is supplied by a group of parallel small arteries that originate directly from the intracranial vertebral artery and pass through the lateral medullary fossa to supply the lateral medulla (Fig.5.7) (Duvernoy 1978). Sometimes the medial

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