Anat. Embryo1.157, 35-68 (1979)
Anatomy
and Embryology 9 by Springer-Verlag 1979
The Pigment Architecture of the Human Frontal Lobe I. Precentral, Subcentral and Frontal Region Heiko Braak AnatomischesInstitutder Universit~ttKiel, Olshausenstral3e,D-2300 Kiel, Federal Republicof Germany
Summary. The precentral, subcentral, and frontal region of the human frontal lobe were examined by means of stereomicroscopical analysis using 800 gm thick pigment preparations. The precentral region can be divided into markedly externoteniate ganglionic core fields and weakly externoteniate paraganglionic belt areas. The core fields are in addition characterized by a conspicuous population of pigment-laden Betz-pyramids in layer PVb. A typical pattern of pigmentation permits their clear distinction from other pyramidal cells of the fifth layer. When passing to the paraganglionic belt areas devoid of Betz-pyramids, the uniform multiform layer splits into a strongly pigmented PVIa and a more pallid PVIb. The subcentral region at the lowermost extremity of the central sulcus displays features of both frontal and parietal areas. The frontal region is mainly formed of equoteniate areas but comprises also a tongue-shaped internoteniate territory medially and an elongated externoteniate area laterally. Extended parts of the frontal region which abut upon the paraganglionic belt are endowed with unusually large and pigmentladen IIIc-pyramids. Pyramids of this type can be rarely encountered within the human isocortex but occur in great number in circumscribed specialized regions such as the temporal magnopyramidal region which represents probably the speech centre of Wernicke. Within the frontal lobe, two magnopyramidal regions can be distinguished. The superofrontal magnopyramidal region stretches out over large parts of the superior frontal convolution whereas the inferofrontal one is small and covers mainly posterior parts of the inferior frontal gyrus. As to its location, the superofrontal magnopyramidal region includes the supplementary motor region which is known to be involved in the performance of speech. On account of its unique structure and its location, the inferofrontal magnopyramidal region is considered to represent the morphological counterpart of the speech centre of Broca. For offprints contact:
Prof. H. Braak
0340-2061/79/0157/0035/$06.80
H. Braak
36
K e y words: M a n - C e r e b r a l cortex - F r o n t a l lobe - M o t o r speech regions A r c h i t e c t o n i c s - Lipofuscin.
Introduction T h e o u t l i n i n g a n d m a p p i n g o f the v a r i o u s areas o f the h u m a n f r o n t a l lobe is still a m a t t e r o f d e b a t e . S t a n d i n g n o t o n l y in c o n t r a d i c t i o n w i t h the t h r u s t o f the t h e o r y o f Bailey a n d y o n B o n i n (1951), the existing cyto- a n d m y e l o a r c h i t e c t o n i c p a r c e l l a t i o n s are also to some extent at v a r i a n c e with each o t h e r ( B r o d m a n n 1903/04, 1908, 1909, 1912, 1914; C a m p b e l l , 1905; Smith, 1907; Vogt, 1910; v o n E c o n o m o a n d K o s k i n a s , 1925; S t r a s b u r g e r , 1937; S a r k i s s o v et al., 1955; Sanides, 1962, 1963, 1964). A r c h i t e c t o n i c studies o n the h u m a n b r a i n are greatly facilitated b y utilizing a selective p i g m e n t - s t a i n i n g t e c h n i q u e which p e r m i t s processing o f sections u p to 1,000 g m in thickness. Since the v a r i o u s types o f nerve cells w i t h i n the h u m a n b r a i n generally d i s p l a y a different a n d often highly c h a r a c t e r i s t i c p a t t e r n o f p i g m e n t a t i o n , p a r t i t i o n i n g o f the c o r t e x b e c o m e s easy a n d reliable (H. B r a a k , 1978a). The g r e a t n u m b e r o f s u p e r i m p o s e d a n d c h a r a c t e r i s t i c a l l y p i g m e n t e d nerve cells seen at a glance allows even the u n e x p e r i e n c e d o b s e r v e r to clearly d e l i n e a t e the c o r t i c a l areas. This s t u d y is a c o n t i n u a t i o n o f f o r e g o i n g p a p e r s o f the p i g m e n t a r c h i t e c t u r e o f b o t h the o c c i p i t a l a n d t e m p o r a l lobes (H. B r a a k , 1977, 1978b, 1978c). The p r o p o s e d p a r c e l l a t i o n is b a s e d on the c h a n g i n g p a t t e r n o f p i g m e n t a t i o n w h i c h is d e p i c t e d in d i a g r a m s for easy r e c o g n i t i o n o f the v a r i o u s areas.
Materials and Methods This study was done on the isocortex of adult man. Brains obtained at post mortem and free of significant pathology were fixed by immersion in formaldehyde 1:9 for several months (R 86/76 c~ aged 33, rheumatic fever; R 415/76 c~ aged 34, bronchopneumonia; R 721/75 d' aged 54, uremia; R 629/75 c~ aged 55, myocardial infarction; R 501/75 3 aged 67, peritonitis; R 69/76 3 aged 80, miliary tuberculosis; G 20/72 ~ aged 84, suffocation; R 507/75 ~ aged 85, pulmonary embolism; R 434/76 ~ aged 85, bronchopneumonia; R 79/76 ~ aged 88, pulmonary embolism, R 213/76 ~' aged 91, chronic pulmonary emphysema, cor pulmonale). Frozen sections were cut at 800 gin. Eleven gapless series of coronal sections through both the left and the right hemispheres were at our disposal. After a thorough oxidation with performic acid for about 30 min, the slices were washed under running tap-water, transferred to 70% ethanol, and stained with aldehydefuchsin (H. Braak, 1978d). After washing with 70% ethanol, the sections were carefully dehydrated, cleared with xylene, and mounted with a synthetic resin (Permount, Fisher). Some favourable parts of the thick sections were photographed, cut out and re-embedded in epoxy resin. These blocks were cut at 8-12 gm and stained with methylene-blue to reveal both the pigment-picture and the Nissl-picture in the same preparation (E. Braak, 1976b, 1977). Photographs were taken on orthochromatic emulsion (Agfa ortho 25 professional) and developed in Agfa Rodinal 1:20 for 10 min.
Terminology. The nomenclature recommended by Vogt and Vogt (1919) is applied in our architectonic descriptions. The isocortical layers are termed from the pial surface inwards: The molecular
Frontal Lobe Pigment Architecture
37
layer, the corpuscular layer, the pyramidal layer, the granular layer, the ganglionic layer, the multiform layer. Combinations such as 'magnopyramidal' field or 'gigantoganglionic' field point to a conspicuously pigmented population of large to giant pyramids in either the pyramidal layer or the ganglionic layer which may well serve to characterize the field. Besides more or less intensely stained layers, the pigment preparations display two light stripes running parallel to the cortical surface which are termed the external and internal tenia. The location of both teniae often corresponds to that of the outer and inner stripes of Baillarger, layer 4 and 5b respectively. 'Externoteniate' areas are characterized by a pronounced outer tenia, the breadth of which clearly exceeds that of the inner one. For detailed remarks on pigmentoarchitectonics the reader is referred to H. Braak (1978 a, b).
Results The frontal lobe is subdivided into four regions: the precentral 1, the subcentral, the frontal, and the orbital. This study is confined to the analysis of the former three regions.
1. The Precentral Region The precentral region contains the ganglionic core and the paraganglionic belt. Both the core and the belt areas share a more or less pronounced externoteniate characteristic which permits their clear distinction from the equoteniate or internoteniate areas of the frontal region.
1.1. The Ganglionic Core On the medial surface of the hemisphere, the core covers an extended part of the paracentral lobule bounded by a line in continuation with the central sulcus which courses down to the upturned end of the cingulate sulcus. Here it recedes into the sulcus where it curves forwards to reappear close to the anterior end of the paracentral lobule where it bends back and upwards (Fig. 1). Superolaterally the ganglionic core narrows considerably and soon becomes totally buried in the depth of the central sulcus. Its posterior boundary follows the course of the central sulcus in its whole length and can be traced along the anterior wall of the sulcus close to its floor (Campbell, 1905; Brodmann, 1908 ; Bucy, 1935 ; Sanides, 1962). The anterior boundary swings over the exposed surface of the triangular part of the precentral gyrus to follow for a longer distance the edge between its posterior wall and the crest where it gradually recedes deeper into the central sulcus. The core ends at about the level of the inferior frontal sulcus (Fig. 1). The ganglionic core fields share a markedly externoteniate characteristic and a more or less densely packed population of conspicuously pigmented Betz-pyramids in layer Vb. The breadth of the cortex is subjected to a slow 1 The designation 'precentral' refers to the fact that the central sulcus forms for the most part the posterior border of the region but does not imply its being confined to the limits of the precentral gyrus
38
H. Braak
Fig. 1 a-c. Map of the pigmentoarchitectonic areas of the human precentral, subcentral, and frontal regions and gradual decrease, as one passes f r o m the upper margin o f the hemisphere inferiorly. The core can be subdivided into a posterior dysganglionic zone, an intermediate territory o f refined core fields, and a small anterior zone o f gradual adaptation. It seems advisable to begin the discription with the gigantoganglionic area since this field displays m o s t p r o n o u n c e d l y the features of the core.
a) Area gigantoganglionaris (gig.; Figs. 3 and4). The cortex as a whole is signally b r o a d and relatively sparsely pigmented.
Frontal Lobe Pigment Architecture
gig.
magn,
dys.i,
para. i.
dys.s,
dys.p,
", ...... ?..
9
grg.
paragrg,
s
f, i,
srnp.c.p, smp.m.p.L
f.a.I,
trans,
pmp, m.p.
~
fi ii!i !i !iiIi i ! ii ! !:Ii!i!iii liiii:i:i:iii!lii!!! [c,a.
39
f,a.rn,
pmp.c.p,
pmp.c~a, pmp.mam, pmpm.a.I,
~
"
smp.m.p.m,
smpc.a,
srnp, rn.a.L smp.m.L
iti, p,
imp.c,
imp, rn.a.
imp.mi,
fo.p.
imp, in.p,
para.p,
para.a.
%~o~o':::::::::::::::::::::::~r
Anatomy
and Embryology 9 by Springer-Verlag 1979
The Pigment Architecture of the Human Frontal Lobe I. Precentral, Subcentral and Frontal Region Heiko Braak AnatomischesInstitutder Universit~ttKiel, Olshausenstral3e,D-2300 Kiel, Federal Republicof Germany
Summary. The precentral, subcentral, and frontal region of the human frontal lobe were examined by means of stereomicroscopical analysis using 800 gm thick pigment preparations. The precentral region can be divided into markedly externoteniate ganglionic core fields and weakly externoteniate paraganglionic belt areas. The core fields are in addition characterized by a conspicuous population of pigment-laden Betz-pyramids in layer PVb. A typical pattern of pigmentation permits their clear distinction from other pyramidal cells of the fifth layer. When passing to the paraganglionic belt areas devoid of Betz-pyramids, the uniform multiform layer splits into a strongly pigmented PVIa and a more pallid PVIb. The subcentral region at the lowermost extremity of the central sulcus displays features of both frontal and parietal areas. The frontal region is mainly formed of equoteniate areas but comprises also a tongue-shaped internoteniate territory medially and an elongated externoteniate area laterally. Extended parts of the frontal region which abut upon the paraganglionic belt are endowed with unusually large and pigmentladen IIIc-pyramids. Pyramids of this type can be rarely encountered within the human isocortex but occur in great number in circumscribed specialized regions such as the temporal magnopyramidal region which represents probably the speech centre of Wernicke. Within the frontal lobe, two magnopyramidal regions can be distinguished. The superofrontal magnopyramidal region stretches out over large parts of the superior frontal convolution whereas the inferofrontal one is small and covers mainly posterior parts of the inferior frontal gyrus. As to its location, the superofrontal magnopyramidal region includes the supplementary motor region which is known to be involved in the performance of speech. On account of its unique structure and its location, the inferofrontal magnopyramidal region is considered to represent the morphological counterpart of the speech centre of Broca. For offprints contact:
Prof. H. Braak
0340-2061/79/0157/0035/$06.80
H. Braak
36
K e y words: M a n - C e r e b r a l cortex - F r o n t a l lobe - M o t o r speech regions A r c h i t e c t o n i c s - Lipofuscin.
Introduction T h e o u t l i n i n g a n d m a p p i n g o f the v a r i o u s areas o f the h u m a n f r o n t a l lobe is still a m a t t e r o f d e b a t e . S t a n d i n g n o t o n l y in c o n t r a d i c t i o n w i t h the t h r u s t o f the t h e o r y o f Bailey a n d y o n B o n i n (1951), the existing cyto- a n d m y e l o a r c h i t e c t o n i c p a r c e l l a t i o n s are also to some extent at v a r i a n c e with each o t h e r ( B r o d m a n n 1903/04, 1908, 1909, 1912, 1914; C a m p b e l l , 1905; Smith, 1907; Vogt, 1910; v o n E c o n o m o a n d K o s k i n a s , 1925; S t r a s b u r g e r , 1937; S a r k i s s o v et al., 1955; Sanides, 1962, 1963, 1964). A r c h i t e c t o n i c studies o n the h u m a n b r a i n are greatly facilitated b y utilizing a selective p i g m e n t - s t a i n i n g t e c h n i q u e which p e r m i t s processing o f sections u p to 1,000 g m in thickness. Since the v a r i o u s types o f nerve cells w i t h i n the h u m a n b r a i n generally d i s p l a y a different a n d often highly c h a r a c t e r i s t i c p a t t e r n o f p i g m e n t a t i o n , p a r t i t i o n i n g o f the c o r t e x b e c o m e s easy a n d reliable (H. B r a a k , 1978a). The g r e a t n u m b e r o f s u p e r i m p o s e d a n d c h a r a c t e r i s t i c a l l y p i g m e n t e d nerve cells seen at a glance allows even the u n e x p e r i e n c e d o b s e r v e r to clearly d e l i n e a t e the c o r t i c a l areas. This s t u d y is a c o n t i n u a t i o n o f f o r e g o i n g p a p e r s o f the p i g m e n t a r c h i t e c t u r e o f b o t h the o c c i p i t a l a n d t e m p o r a l lobes (H. B r a a k , 1977, 1978b, 1978c). The p r o p o s e d p a r c e l l a t i o n is b a s e d on the c h a n g i n g p a t t e r n o f p i g m e n t a t i o n w h i c h is d e p i c t e d in d i a g r a m s for easy r e c o g n i t i o n o f the v a r i o u s areas.
Materials and Methods This study was done on the isocortex of adult man. Brains obtained at post mortem and free of significant pathology were fixed by immersion in formaldehyde 1:9 for several months (R 86/76 c~ aged 33, rheumatic fever; R 415/76 c~ aged 34, bronchopneumonia; R 721/75 d' aged 54, uremia; R 629/75 c~ aged 55, myocardial infarction; R 501/75 3 aged 67, peritonitis; R 69/76 3 aged 80, miliary tuberculosis; G 20/72 ~ aged 84, suffocation; R 507/75 ~ aged 85, pulmonary embolism; R 434/76 ~ aged 85, bronchopneumonia; R 79/76 ~ aged 88, pulmonary embolism, R 213/76 ~' aged 91, chronic pulmonary emphysema, cor pulmonale). Frozen sections were cut at 800 gin. Eleven gapless series of coronal sections through both the left and the right hemispheres were at our disposal. After a thorough oxidation with performic acid for about 30 min, the slices were washed under running tap-water, transferred to 70% ethanol, and stained with aldehydefuchsin (H. Braak, 1978d). After washing with 70% ethanol, the sections were carefully dehydrated, cleared with xylene, and mounted with a synthetic resin (Permount, Fisher). Some favourable parts of the thick sections were photographed, cut out and re-embedded in epoxy resin. These blocks were cut at 8-12 gm and stained with methylene-blue to reveal both the pigment-picture and the Nissl-picture in the same preparation (E. Braak, 1976b, 1977). Photographs were taken on orthochromatic emulsion (Agfa ortho 25 professional) and developed in Agfa Rodinal 1:20 for 10 min.
Terminology. The nomenclature recommended by Vogt and Vogt (1919) is applied in our architectonic descriptions. The isocortical layers are termed from the pial surface inwards: The molecular
Frontal Lobe Pigment Architecture
37
layer, the corpuscular layer, the pyramidal layer, the granular layer, the ganglionic layer, the multiform layer. Combinations such as 'magnopyramidal' field or 'gigantoganglionic' field point to a conspicuously pigmented population of large to giant pyramids in either the pyramidal layer or the ganglionic layer which may well serve to characterize the field. Besides more or less intensely stained layers, the pigment preparations display two light stripes running parallel to the cortical surface which are termed the external and internal tenia. The location of both teniae often corresponds to that of the outer and inner stripes of Baillarger, layer 4 and 5b respectively. 'Externoteniate' areas are characterized by a pronounced outer tenia, the breadth of which clearly exceeds that of the inner one. For detailed remarks on pigmentoarchitectonics the reader is referred to H. Braak (1978 a, b).
Results The frontal lobe is subdivided into four regions: the precentral 1, the subcentral, the frontal, and the orbital. This study is confined to the analysis of the former three regions.
1. The Precentral Region The precentral region contains the ganglionic core and the paraganglionic belt. Both the core and the belt areas share a more or less pronounced externoteniate characteristic which permits their clear distinction from the equoteniate or internoteniate areas of the frontal region.
1.1. The Ganglionic Core On the medial surface of the hemisphere, the core covers an extended part of the paracentral lobule bounded by a line in continuation with the central sulcus which courses down to the upturned end of the cingulate sulcus. Here it recedes into the sulcus where it curves forwards to reappear close to the anterior end of the paracentral lobule where it bends back and upwards (Fig. 1). Superolaterally the ganglionic core narrows considerably and soon becomes totally buried in the depth of the central sulcus. Its posterior boundary follows the course of the central sulcus in its whole length and can be traced along the anterior wall of the sulcus close to its floor (Campbell, 1905; Brodmann, 1908 ; Bucy, 1935 ; Sanides, 1962). The anterior boundary swings over the exposed surface of the triangular part of the precentral gyrus to follow for a longer distance the edge between its posterior wall and the crest where it gradually recedes deeper into the central sulcus. The core ends at about the level of the inferior frontal sulcus (Fig. 1). The ganglionic core fields share a markedly externoteniate characteristic and a more or less densely packed population of conspicuously pigmented Betz-pyramids in layer Vb. The breadth of the cortex is subjected to a slow 1 The designation 'precentral' refers to the fact that the central sulcus forms for the most part the posterior border of the region but does not imply its being confined to the limits of the precentral gyrus
38
H. Braak
Fig. 1 a-c. Map of the pigmentoarchitectonic areas of the human precentral, subcentral, and frontal regions and gradual decrease, as one passes f r o m the upper margin o f the hemisphere inferiorly. The core can be subdivided into a posterior dysganglionic zone, an intermediate territory o f refined core fields, and a small anterior zone o f gradual adaptation. It seems advisable to begin the discription with the gigantoganglionic area since this field displays m o s t p r o n o u n c e d l y the features of the core.
a) Area gigantoganglionaris (gig.; Figs. 3 and4). The cortex as a whole is signally b r o a d and relatively sparsely pigmented.
Frontal Lobe Pigment Architecture
gig.
magn,
dys.i,
para. i.
dys.s,
dys.p,
", ...... ?..
9
grg.
paragrg,
s
f, i,
srnp.c.p, smp.m.p.L
f.a.I,
trans,
pmp, m.p.
~
fi ii!i !i !iiIi i ! ii ! !:Ii!i!iii liiii:i:i:iii!lii!!! [c,a.
39
f,a.rn,
pmp.c.p,
pmp.c~a, pmp.mam, pmpm.a.I,
~
"
smp.m.p.m,
smpc.a,
srnp, rn.a.L smp.m.L
iti, p,
imp.c,
imp, rn.a.
imp.mi,
fo.p.
imp, in.p,
para.p,
para.a.
%~o~o':::::::::::::::::::::::~r
