Download INTRINSIC CONNECTIONS AND CYTOARCHITECTONIC DATA OF

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ACTA NEUROBIOL. EXP. 1988, 48: 169 192
INTRINSIC CONNECTIONS AND CYTOARCHITECTONIC DATA
OF THE FRONTAL ASSOCIATION CORTEIX IN THE DOG
Grazyna RAJKOWSKA and Anna KOSMAL
Department of Neurophysiology, Nencki Institute of Experimental Biology
Pasteura 3, 02-093 Warsaw, Poland
Key words: frontal association cortex, cytoarchitectonics, cortico-cortical connection,
HRP method
Abstract. Organization of intrinsic connections of the frontal association cortex (FAC) in dogs was studied using retrograde HRP-transport
method. For cytoarchitectonic observations and measurements of thickness of the cortex and its particular layers, additional sections stained
with Nissl method were examined. Organization of intrinsic connections
showed that within the dog's FAC two main cortical zones could be
distinguished - the dorsal and the ventral one. The dorsal zone involves dorsally situated areas on the lateral and medial aspects of the
hemisphere, which belong to the prefrontal and premotor regions. The
ventral zone consists only of prefrontal areas situated ventrally on both
aspects of the hemisphere. Each of the zones is characterized by strong
mutual intrinsic connections and weak connections with the other zone.
At the border there is a transitional area in which connections from
both dorsal and ventral zones overlap. The cytoarchitectonic observations
indicated that the dorsal and ventral zones can be distinguished in the
central and caudal, but not in the rostra1 FAC subregion. The dorsal zone
is characterized by considerable thickness of the cortex, cortical layers I11
and V, and the presence in these layers of scattered, large pyramidal
neurons. The ventral zone has thinner cortex and layers I11 and V, and
their pyramidal neurons are more uniform in size. In none of the zones
clearly defined granular layer IV was observed.
INTRODUCTION
Up to now the organisation of intrinsic connections of the frontal
association cortex (FAC) in the dog's brain has not been the subject of
separate studies. Our previous results suggest that within dog's frontal
association cortex two projection zones can be distinguished: the dorsal
and the ventral one (27, 29, 36, 37, 53). The dorsal zone includes dorsal
prefrontal and premotor areas, while the ventral FAC zone involves
only ventral prefrontal areas. Differences in pattern of subcortical (25 - 30,
52, 53) and distal cortico-cortical connections (36, 37) between both FAC
zones suggest that the zones are related to functionally different systems.
Studies on the prefrontal and premotor regions in other species like
the monkey and the cat proved that their particular subregions exhibited a characteristic pattern of cortico-cortical connections (3 - 6, 10, lL,
13, 14, 16, 21 23, 40 47, 57 59).
In the monkey it was shown that the prefrontal subregion localized
dorsally on the lateral cortical surface (part of area 46 above the principal sulcus) was connected with other dorsal prefrontal areas situated
anteriorly and caudally as well as with the premotor areas of the lateral
and medial surfaces of the hemisphere (3 - 6, 21, 43, 44). A similar pattern was observed in the subregion localized ventrally on the lateral
surface (part of area 46 below principal sulcus), as it is predominantly
connected with ventral prefrontal areas situated anteriorly and caudally on the lateral and basal surfaces of the hemisphere. These both adjacent subregions situated above and below the principal sulcus are also
reciprocally connected (21). Such distribution of intrinsic cortical connections within monkey's prefrontal cortex suggests some diversity of
connectional pattern of its dorsal and ventral subregions. Lately, connectional differences between dorsal and ventral parts have also been
observed in monkey's premotor area 6 (6).
Among carnivores, which differ from primates in a picture of sulci
and the extent of corresponding cortical areas in the frontal lobe, intrinsic connections of the FAC have been described only in the cat (34).
Within cat's prefrontal cortex four sectors have been lately distinguished,
namely dorsolateral, dorsornedial, ventral and rostral (10). Strong connections have been observed between cortical areas situated within
each prefrointal sector. Moreover, the dorsolateral sector is strongly
connected with the dorsomedial one, while "the rostral sector receivces
principally intraprefrontal connections from all other sectors" (10). Previous researches on the cat proved that the dorsal sectors of the prefrontal cortex also were connected with the area believed to be the premotor
cortex (7, 23, 42, 59).
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The differences in the pattern of connections between dorsal and
ventral subregions in the monkey and cat are to some extent confirmed
by results of the cytoarchitectonic observations of the prefrontal and
premotor cortices. It was shown that in the two species the areas situated dorsally or ventrally exhibited certain differences in the thickness
and distinctness of the particular cortical layers, as well as in the neuronal arrangement within these layers (5, 6, 12,' 47, 50). Some of the
cytoarchitectonic differences in the prefrontal region refer also to the
structure of layer IV. 1; primates the presence of well-defined granular
layer IV is one of the criteria of separation of the prefrontal cortex
from the premotor one (2, 8, 58). In the cat and dog the problem of the
presence of distinct layer IV in the prefrontal cortex is still under
discussion. According to some authors in the dog's prefrontal cortex
there are small subregions in which layer IV can be distinctly separated
from adjacent cortical layers (24, 31, 55). Others, however, imply that it
is not possible to distinguish this layer (1, 48). Other cytoarchitectonic
features of particular subregions of the dog's FAC have not been satisfactorily described so far. Therefore, in the present study we tried to
complete the cytoarchitectonic observations of FAC regions, ,and to
support these data by some quantitative analysis. We also aimed at elucidating the intrinsic connections of the FAC unknown before, as well
as at explaining whether differently localized subregions vary as to the
pattern of connections and cytoarchitectonics. Moreover, it is interesting
to know whether duality of the FAC area, visualized in the distal cortico-cortical and the subcortical connections, is preserved in the organization of intrinsic connections. If such duality occurs, it is also interesting to know the way the zones are linked.
MATERIAL AND METHODS
Thirty two young dogs weighing 8 - 13 kg were used in this study.
Six of them were used to study FAC cytoarchitectonics,
twenty five *
to determine the cortico-cortical connections.
Cytoarchitectonic study of the FAC. For the microscopic observations
of cytoarchitecture of the FAC, 10 and 20 Km paraffine - celloidine
sections stained by standard Nissl procedure were used (9). In four dogs
the sections were cut in the coronal, and in two dogs in the horizontal
plane.
For measurements the thickness of the cortex and its layers we used
the sections that were the material of cytoarchitectonic observations.
The measurements were carried out in particular FAC areas situated on
flat surfaces, as well as on the convexity of thy gyri in the bottoms of
the sulci (Fig. 1 and Table I). However, the statistical analysis included
only those measurements which were taken from flat cortical surfaces
in both the dorsal and ventral FAC zones (Table 11). The measurements
were takeq with a micrometric ocular in the so-called measurement
segments similarly located in all the dogs. In each FAC area 2 - 3 segments were measured (Fig. 1). In all segments the thickness of the whole
cortey and the thickness of its layers were measured perpendicularly to
the cortical surface. The number of measurements in segments of one
FAC area of 'each dog was amounted 3 to 9. For each segment the
means of the thickness of the cortex and its layers was calculated separately for each dog, then mean values were calculated in all the dogs.
The obtained data were compared using a two-way analysis of variance
followed by Duncan test.
Study of intrinsic connections of the FAC. Multiple unilateral injections of 30 50°/a HRP solution in saline (HRP Sigma Type VI or Boehringer grade I) were made into various FAC areas according to Kreiner's division (31 - 33). In each limited area 3 - 8 injections in neighboring points were made in such way to cover completely the investigated
area. The total volume of HRP solution in one area was about 1 p1.
The needle of Hamilton syringe was inserted at a depth of 2 mm from
the cortical surface. Subsequently histochemical procedure according
to Mesulam prescription was applied (38, 39).
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RESULTS
Localization of the FAC in the dog
The extent of the FAC discussed in the present results was defined
following the cytoarchitectonic (1, 20, 24, 51), myeloarchitectonic (31 - 33,
54) and connectional studies (27, 29, 36, 37).
The FAC occupies the most rostral part of the brain and lies on
both the lateral and medial aspects of the hemisphere (Fig. 2). Dorsocaudally, th;! FAC adjoihs the cruciate sulcus (sCr) and borders with
the MI1 and MI motor areas defined in electrophysiological studies (18).
Ventrally, the FAC is delineated by anterior parts of the limbic cortex. Our previous results strongly suggest that FAC involves two cortical regions, namely the prefrontal cortex and the premotor cortex.
The prefrontal cortex occupies a large extent of the most rostral
part of the frontal lobe (Fig. 2, vertical stripes). On the lateral aspect
of the hemisphere its caudal border runs in the depth of the presylvian
fissure (fPs), including the medial.rp.ral1 cortex and the bottom of this
*
Fig. 1. Schematic illustration of location of measurement segments on coronal sections of the dog's FAC from rostra1
(1) to caudal (4) direction. For the names used see the abbreviation list.
Fig. 2. Schematic illustration of the extent of the FAC in the dog's brain. A, lateral surface of the hemisphere; B,
medial surface; C, coronal sections from rostra1 (1) to caudal (4) direction; vertical stripes, the extent of the prefrontal
region squared area, the extent of the premotor region. For the names used see the abbreviation list.
A
B
C
Fig. 3. Brightfield photomicrographs of the c~toarchitectonicsof the dorsal FAC areas. A, prefrontal PRL area of the central
subregion; B, prefrontal PORd area of the caudal subregion; C, premotor XC area of the caudal subregion. Arrows indicate
single, large pyramidal cells in layers V and 111.
Fig. 4. Brightfield photomicrographs of the cytoarchitectonics !of the ventral FAC
areas. A, prefrontal SPR area of the central subregion; B, prefrontal SG area of
the caudal subregion.
fissure. On the medial aspect of the hemisphere this region lies anteriorly to the genual sulcus (sG). The prefrontal region comprises the
(areas and gyri listed below (Fig. 2C), the names of which are taken
from Kreiner's myeloarchitectonic division (31 - 33), since we consider
this division to be the most detailed one:
- on the area of frontal pole - pole area (POL);
- on the dorsal aspect of the hemisphere - the proreal gyrus (PR);
- on the lateral aspect - the proreal lateral (PRL) area, the orbital
gyrus (ORB), the paraorlbital dorsal (PORd) area of the medial presylvian
fissure wall, the subproreal lateral (SPRL) area as well as paraorbital
ventral (PORv) area of the lateral wall of the anterior rhinal sulcus;
- on the ventral aspect - the subproreal gyrus (SPR);
- on the medial aspect - the pregenual area with its dorsal (PGd) and
ventral (PGv) subareas as well as subgenual (SG) and precruciate medial (XM) areas.
The premotor cortex occupies the area between prefrontal cortex
(rostrally) and motor cortex (caudally) (Fig. 2, squared area). It is
smaller than the prefrontal one and restricted only the dorso-lateral
and dorso-medial surfaces of the hemisphere. It involves also the cortex
of the lateral presylvian fissure wall and anterior cruciate sulcus wall.
Dorsally, the premotor region occupies the most caudal part of the proreal gyrus (XC), laterally - the composite anterior (CA) and composite
internal (CJ) areas, while medially - the precruciate posterior (XJ?),
and precruciate lateral (XL) areas (Fig. 2C).
Cytoarchitectonic data
Following present cytoarchitectonic observations it was concluded
that dog's FAC is a five-layer structure which lacks a well defined granular layer IV (Figs. 3 and 4). Moreover, it is possible to divide further
layers 111, V and VI into two sublayers. The mean thickness of the cortex on the whole FAC area is 1.47 k 0.25 mm, except for the anterior
area and the tops of the gyri where it is thickest and exceeds 2.0
0.39
mm as well as the bottoms of the sulci where the cortex is thinnest
and 1.13 0.10 mm thick (Table I). The thickest among cortical layers
are: layer I11 (mean thickness of 0.90 -j- 0.11 mm) and layer V (0.41 0.13
mm); layer I1 is 'thinnest (0.12
0.03 mm). Layers I (0.27 0.11 mm)
and VI (0.28 0.10 mm) reach medium values (Table I). It should be
added that the thickness of the two extremely located cortical layers,
i.e. I and VI depends mainly on the fact whether it is measured on the
[gyrus top, flat surface or the bottom of the sulcus. Layer I is the
thickest in the sulcus bottoms and the thinnest on the gyrus tops (Table
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Mean values of the thickness of &e whole cortex and its particular layers in the FAC in four dogs
Name of
measurement
segment
Mean thickness (mm)
Whole
cortex
POL
PRa
SPRa
ORBa
PR
PRL
PORd
SORB
ORB
PORv
SRha
SPRL
SPR
FPS
PGv
SG
SPG
PGd
XMV
XMd
CJ
XC
1
I
0.22h0.04
0.33h0.11
0.25h0.05
0.24h0.08
0.24&0.05
0.26k0.11
0.26h0.05
0.44k0.20
0.25k0.15
0.25h0.07
0.46k0.10
0.23h0.06
0.20h0.04
0.50h0.17
0.21h0.03
0.22A0.08
0.41h0.10
0.21h0.04
0.20k0.04
0.23k0.06
0.23k0.20
0.22f0.06
1.18*0.27
2,561.0.58
2.13h0.49
2.33k0.39
1.72h0.36
1.60k0.29
1.26h0.19
1.24k0.26
1.65h0.24
1.3510.22
1.22h0.27
1.03k0.14
1.56h0.19
1.22k0.29
1.11hO.10
1.19h0.20
1.03k0.13
1,3610.15
1.3010.31
1.3810.16
1.41h0.12
1.5OhO.18
CS
1.20h0.33 0.20h0.24
SC
1.00&0.16 0.20k0.04
The whole
area of
1.47k0.25 0.27h0.11
the FAC
1
'
1
Cortical layers
1 1 1 1
I
1 1 1
0.11k0.03
0.13k0.03
0.14h0.03
0.16h0.07
0.12h0.03
0.14h0.06
0.11h0.02
0.12k0.04
0.14k0.13
0.13h0.02
0.14h0.02
0.12h0.06
0.12f 0.02
0.12h0.04
0.12h0.05
0.11k0.02
0.11h0.02
0.11h0.04
0.10f0.02
0.12k0.03
0.1Oh0,Ol
0.1 1k0.02
1
'
0.34k0.09
0.66h0.19
0.53h0.19
0.63h0.27
0.46h0.19
0.49h0.15
0.37k0.10
0.28h0.08
0.55h0.13
0.35k0.09
0.28&0.09
0.2810.05
0.37k0.11
0.26h0.08
0.31h0.08
0.34k0.10
0.22h0.09
0.44f0.12
0.39k0.07
0.37k0.12
0.36h0.10
0.35kO.M
0.10k0.02 0.36k0.08
0.09k0.01 0.2410.06
0.12k0.03
a
.
1
0.4010.11
v
1
1 0.33h0.09
1
VI
Number
of measure
ments
0.72h0.25
0.67k0.20
0.76h0.24
0.57h0.14
0.48k0.18
0.48h0.57
0.2410.09
0.49k0.15
0.39h0.13
0.2310.04
0.27h0.06
0.49&0.11
0.25k0.10
0.2810.06
0.33h0.11
0.18h0.07
0.38h0.05
0.41k0.12
0.39k0.10
0.4310.06
0.46h0.12
0.2210.08
0.76h0.26
0.58h0.19
0.62h0.27
0.36h0.15
0.24h0.08
0.1910.07
0.15h0.07
0.30f0.18
0.23A0.17
0.14&0.05
0.19h0.19
0.41h0.14
0.15h0.04
0.18Zt0.04
0.17Zt0.05
0.11&0.03
0.22k0.05
0.25Zt0.07
0.2350.07
0.21 k0.05
0.34~t0.10
24
15
15
14
24
16
21
20
26
19
23
22
23
17
16
16
19
16
18
21
12
12
0.3910.06
0.2910.05
0.21+0.04
0.2310.06
12
12
0.41 h0.13
1
0.28k0.10
1
The order of measurement segments is in accordance with their localization in the FAC from
rostra1 to caudal direction.
I compares measurement segments FPS, SPG, SRHa and PR, ORB, SPR).
\On the contrary, the layer VI is the thickest on gyrus tops and the
thinnest in sulcus bottoms (Table I compares measurement segments
PR, ORB, SPR and FPS, SRHa, SPG). The analysis of the thickness of
intermediate layers I11 and V proved that their thickness depended not
only on the curvature of the cortical surface but also on whether they belonged to the dorsal or ventral part of the FAC (Table 11). The thickness
differences of layers I11 and V, as well as the analysis of the cellular
structure revealed principal differences between cortical areas situated
rostrally, centrally and caudally, while the differences among central
and caudal areas account for differences between dorsal and ventral
areas. On the basis of this we distinguished in the FAC three main cytoarchitectonic subregions: rostral, central and caudal. The latter two
subregions can be further divided into dorsal and ventral zones.
Mean values of the thickness of the whole cortex and its particular layers in the dorsal and
ventral FAC areas, in four dogs
Namcs of 1
me=u=e _ment
Whole
segment
cortex
Dorsal FAC
Prefrontal
PRL
PGd
PORd
XMd
Premotor
CJ
XC
The whole
dorsal
FAC zone
Ventral
PAC
Prefrontal
PORv
PGv
SG
XMV
The whole
ventral
FAC zone
Mean thickness (mm)
I
I
I
.
I1
Cortical layer
111
I
I
I
I
v
I
I
VI
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Number
of measurement
--
I
1.6010.29
1.3650.15
1.2610.19
1.3810.16
1.4110.12
1.5010.18
1.43*0.19
--
1.35*0.22
1.1110.10
1.1950.20
1.3040.31
1.2140.16
The differences in the thickness of the cortex and its layers 111 and V between dorsal and ventral
FAC areas are statistically significant (P< 0.001).
The rostral cytoarchitectonic subregion. This subregion is situated
on the rostral pole of the brain and involves POL area as well as the
most anterior parts of the three gyri: proreus, orbitalis and subproreus,
which we named PRa, ORBa, SPRa, respectively (Figs. 1 and 3). There
the cortex is the thickest (above 2 mm, p < 0.001) than in central and
caudal FAC subregions (Table I). The rostral subregion is characterized
by thin layer I (0.26 0.09 mm) and very thick layers 111, (0.54 0.18
mm), V (0.62 -I- 0.17 mm) and VI (0.55 0.18 mm). The borders between
layers and underlying white matter are poorly visible due to a sparse
arrangement of neurons and their similar sizes.
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Dorsal zone of the central and caudal cytoarchitectonic segments.
This zone contains the areas of the prefrontal cortex localized on both
the dorso-lateral (PR, PRL, ORB, PORd, FPS) and the dorso-medial
surface of the hemisphere (PR, PGd, SPG, XM), as well as the areas
of the premotor cortex (XC, CA, CJ, XP, XL) (Fig. 2). The areas of the
dorsal zone have a thick cortex (1.43 f 0.19 mm), and thick cortical
layers I11 (0.42 4- 0.11 mm) and V (0.46 -I- 0.17 mm) (Table 11). The
borders between the two layers are barely visible due to a sparse arrangement of neurons there (Figs. 3A, B and C). Also the border with
underlying white matter is indistinct. The characteristic feature of the
cortex in this zone is the presence in layer V and sublayer IIIb of
scattered, large, pyramidal neurons (Fig. 3, arrows). Their number
and size increase from central to caudal FAC subregions, i.e. from the
Fig. 5. Schematic illustration of the localization of large pyramidal neurons of
layer V in the dog's frontal lobe cortex which is presented on the horizontal
section. Note the increase in number and sizes of these neurons from the rostral
(prefrontal) to the caudal (motor) direction. Sizes and densities of black triangles
correspond to sizes and densities of large pyramidal cells in layer V; broken lines
indicate borders between prefrontal (XM, PORd), premotor (XP, CA, CJ) and
motor (MI, MII) frontal areas.
POL
1
8
oR.3,
SPR.
Fig. 6. Schematic illustration of the thickness differences in layer I11 between
dorsal and ventral FAC areas. Black circles indicate areas, in which layer I11 is
thickest; white circles indicate areas, in which layer I11 is thinnest. Such differences are statistically significant ( P 0.001). Black-white circles indicate areas, in
which layer I11 exceeds medium values. For the names used see the abbreviation list.
<
Fig. 7. Macroscopic photographs of coronal sections with examples of the FAC
injections. A, dorsal group injection into the CA area; B, ventral group injection
into the ORBv area.
DORSAL
GROUP
I?,:.
D1
D3
D4
Fig. 8. Localization of dorsal FAC injections presented on the schemes of the (a)
lateral and (b) medial surfaces of the frontal lobe. The black areas indicate the
site of injections; broken lines show the extent of enzyme diffusion. For the names
used see thc abbreviation list.
prefrontal to motor areas (Fig. 5). This gradient is particularly clearly
visible in the cortex, of the depth of the presylvian fissure what was
described in details in our previous paper (29).
Ventral zone of the central and caudal cytoarchitectonic subregions.
This zone contains areas situated in the ventral part of the prefrontal
cortex on both the ventro-lateral (SPR, SPRL, SRHa, PORv) and ventromedial surfaces (SPR, PGv, SG) (Fig. 2). The cortex of the ventral zone
is thinner (1.21 0.16 mm) than the cortex of the dorsal ones and is
characterized by thinner layers I11 (0.33 0.09 mm) and V (0.33 0.09
mm) (P < 0.001) (for comparison see Figs. 3 and 4 as well as Table I1
and Fig. 6). It is worth emphasizing that layers 111 and V in the ventral
zone have the same thickness, while in the dorsal zone layer V is thicker than layer I11 (P < 0.01). The size of cells in layers I11 and V is
more uniform than in respective layers of the dorsal zone, as we have
not observed here, large pyramidal neurons (Fig. 4). Moreover, these
layers are more compact, what results in more distinct borders between
them and white matter than in the dorsal zone. Areas of the ventral
zone in the caudal FAC subregion have a characteristic structure of
sublayer VJa which contains densely packed neurons oriented horizontally (Fig. 4B).
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Study of connections
Localization of injections. For investigating the distribution of mutual
intrinsic connections of the frontal association cortex small single injections of HRP were made in different places of this cortex. The sites
of injections were localized in areas of dorsal and ventral zones of the
FAC and usually limited to one of them (Fig. 7). All cases of injections
here digded into two groups: dorsal and ventral. In each group the
arrangement of the injections was in accordance with their localization
in dorso-ventral and rostro-caudal directions. The sites of injections are
schematically presented on Figs. 8 and 9.
Dorsal group included cases Dl-Dl7 in which injections covered cortical areas situated on the dorsal surface of the hemisphere as well as
dorso-lateral and dorso-medial surfaces (Fig. 8). Seven of these injections were localized most dorsally and caudally in the FAC, and they
belonged to the premotor (Dl-D4) and prefrontal regions (D5-D7), (Fig.
8, Dl-D7). The nex$ ten injections were placed more ventrally and anteriorly (Fig. 8, D8-D17). They covered the prefrontal PR area (D8 and
D9), as well as ORB area situated below, on the lateral surface (D10D14) and XM area, on the medial surface (D15-D17).
VENTRAL GROUP
Fig. 9. Localization of ventral FAC injections. Denotations as in Fig. 8.
/
Ventral group involved cases D18-D26 with injections into prefrontal
areas located on the ventral as well as ventro-lateral and ventro-medial
surfaces of hemisphere (Fig. 9). The first two injections were located
most ventrally and covered anterior part of the SPR area (Fig. 9, Dl8
and D19). The next injections were localized more caudally and except
for SPR area they included adjacent ventro-lateral SPRL, ORBv areas
(D20) and ventro-medial PGv, SG areas (021). The next five injections
were situated more dorsally than the previous ones and they covered
three areas: the PGv and PGd on the medial surface (D22) and ventral
ORB part on the lateral surface (D24-D26).
Distribution of labeled neurons. The dorsal group. The results obtained with this group are illustrated by four chosen cases, with each dog
representing a series of similar injections and patterns of the distribution of labeled cells (Fig. 10).
QOKSAL GROUP
Fig. 10. Scheme of distributions of labeled neurons (illustrated with dots) following dorsal FAC injections (black areas).
A, lateral surface of the frontal lobe; B, medial surface; C, coronal sections from the rostra1 (1) to the caudal (6) direc-
tion. One dot on the scheme stands for two labeled cells. For the names used see the abbreviation list.
Dog D5 represents the cases of dorso-caudal injections. In this subject injection was placed in the caudal part of the proreal gyrus (XC)
and in the fundus and small part of the medial wall (PORd) of the
presylvian fissure (Fig. 10 upper picture). In this case the largest number
of labeled neurons was found in neighboring caudal areas, FPS and PPRd
of the prefrontal region and in CA area of the premotor region (Fig.
10, D5 A and C). Additional cell labeling was observed in the prefrontal
XM area and premotor XP, XL areas of the medial surface of the hemisphere (Fig. 5, D5 B and C). A small number of labeled cells was found
in the central and rostra1 prefrontal areas, namely, PRL, ORBd and
PGd. It is worth mentioning that in the cases where injections were
restricted only to the premotor cortex areas, additional labeled neurons
were observed in other premotor areas (Fig. 11) and even in the areas of
the primary motor cortex.
Dog D9 represents the cases of more rostrally placed injections covering the proreal gyrus (PR) of the prefrontal cortex. The D9 injection
involved only the medial part of this gyrus (Fig. 10, D9). After this
injection the largest accumulation of labeled neurons was found in centrally located prefrontal PGd and XM areas of the dorso-medial surface
(Fig. 10, D9 B and C). Quite a large number of neurons was observed
also in the dorsal PRL, PORd, ORB areas of the lateral surface (Fig. 10,
D9 A and C). Occurrence of such cells seems to be interesting since the
injection did not extend on the cortex of the lateral surface. A small
number of HRP positive cells was detected in the caudal prefrontal XM,
PORd and premotor XP areas of both surfaces. Only sporadic labeled
neurons were found in the ventral half of the frontal lobe namely, in
ORBV, PORv, and SRHa areas.
Dog Dl3 was injected more ventrally than the prevjous cases and
the injection involved antero-dorsal part of ORB area situated centrally
on the lateral surface of the hemisphere (Fig. 10, D13). HRP-positive
neurons were found almost exclusively in the neigboring prefrontal
areas of the lateral surface. Most frequently they appeared in dorsal
areas such as the PORd, ORBd, and POL, but they were also found in
the SPR, PORv, SPRL prefrontal areas situated ventrally (Fig. 10, Dl3
A, B and C). Thus, unlike in previous cases we observed here additional
labeling in the ventral prefrontal areas. Moreover, in the most dorsal
prefrontal PR area as well as premotor XC and XP areas only single
labeled cells were found.
Dog Dl7 represents the cases of centrally situated XM field injections of the medial cortical surface (Fig. 10, bottom picture). The largest
number of labeled neurons was present in the prefrontal PGd, PGv, SG
areas of the medial surface located in the close vicinity of the injection
site (Fig. 10, Dl7 B and C). Additionally, single HRP-positive cells were
Fig. 11. Microphotographs of labeled cells in the CA premotor area following XC
premotor injections.
VENTRAL
GROUP
Fig. 12. Schematic illustration of distributions of labeled neurons following ventral FAC injections. Denotations as in Fig. 10.
observed in the dorso-lateral POL, PR, PRL, PORd and ORBd areas as
well as in the premotor XP field (Fig. 10, Dl7 A and C). Unlike in dog
Dl3 they were not found in the most ventral areas of the frontal association cortexc
The ventral group. The results obtained on this group are illustrated
by three representative cases (Fig. 12).
Dog Dl8 represents most ventral FAC injections located in the anterior part of the prefrontal subproreus gyrus (SPR) of both aspects
of the hemisphere. (Fig. 12, D18). In this case dense cell labeling was
observed in neighboring areas of the ventro-lateral prefrontal cortex SPRL, SRHa, PORv, and ORBv (Fig. 12 Dl8 A and C) as well as in the
ventro-medial prefrontal cortex - POL, PGv, SG (Fig. 12 Dl8 B and C).
A small number of HRP-positive cells was found also in the dorso-lateral PRL, PORd, ORBd and dorso-medial PGd, XM prefrontal areas.
Only single labeled cells were detected in the most dorsally situated
prefrontal PR and premotor XC areas.
Dog D22 represents a series of injections localized more dorsally than
in the previous cases and restricted only to the medial prefrontal surface. In the case D22 the injection covered the PGv and PGd areas, on
both sides of the pregenual sulcus (Fig. 12, D22). After this injection
the HRP-positive cells were found in the neighboring medio-dorsal XJU
area and medio-ventral SG area of the prefrontal cortex (Fig. 12, D22
B and C). Less intensive labeling extended also on the dorsal PR area
and the ventral SPR area involving the latero-ventral SPRL area (Fig.
12, D22 A and C).
Dog D25 represents a series of injections placed ventro-caudally on
the lateral surface in the ORBv prefrontal area (Fig. 12, D25). In this
case labeled neurons were localized only in few neighboring cortical
areas and they were restricted to the ventral half of the lateral prefrontal surface. The HRP-positive neurons were present in the SPRL, PORV,
SRHa and SPR areas (Fig. 12, D25 A and C). Thus, in this case labeled
cells were found neither in the medial surface of the prefrontal region
cortex nor in the premotor region.
Organization of intrinsic FAC connections. In the present material
it was generally observed that the majority of labeled neurons was found
in the cortical FAC areas adjacent to injection sites, significantly less
intensive labeling was observed in more distal FAC areas. However,
following dorsal FAC injections the main 'aggregation of labeled cells
was found predominantly in the dorsally localized FAC areas of both
the prefrontal and premotor regions forming short cortical connections
between them. This fact strongly supports a concept of the dorsal FAC
zone as a separable entity. The ventral injections unlike the dorsal ones
caused labeling of cells mainly in the adjacent ventral prefrontal areas.
It should be stressed that in the two groups of injections, dorsal and
ventral, aggregations of labeled neurons were observ,ed on both lateral
and medial surfaces of the hemisphere.
m
DORSAL FAC ZONE
Fig. 13. Schemes of organization of intrinsic connections of the dorsal FAC zone
presented on the (A) lateral and (B) medial surface of the frontal lobe. Thick
arrows indicate strong connections; thin arrows, weak connections.
Fig. 14. Schemes of organization of intrinsic connections of the ventral FAC zone.
Denotations as in Fig. 13.
Taking into account the distribution of intrinsic connections, the
existence within the dog's FAC of two main cortical zones, dorsal and
ventral can be considered (Figs. 13 - 15). The dorsal zone involves dorsally
situated areas on the lateral and medial aspects of both the prefrontal
and premotor regions (Fig. 13). This zone is characterized by strong
mutual connections linking adjacent areas (Fig. 13 thick arrow) and
a small number of connections with the ventral zone areas (Fig. 13 thin
arrows). The ventral zone, which comprises the ventrally situated prefrontal areas of both aspects of the hemisphere has strong intrinsic
mutual connections (Fig. 14 thick arrow) and only weak connections
with the dorsal zone areas (Fig. 14 thin arrows). However, there is no
sharp border between the dorsal and ventral zones. In the area where
connections from both of -them overlap, a transitional zone. can be dis-
DORSAL
FAC L O N E
....
VENTRAL
FAC
ZONE
Fig. 15. Schemes of the extent of dorsal and ventral FAC zones, and the transitional dorso-ventral area. A, lateral surface of the frontal lobe; B, medial surface;
C , coronal sections from rostra1 (1) to caudal (3) direction.
tinguished (Fig. 15 area with overlapping symbols - lines and dots).
The transitional zone is formed on the lateral surface by POL area,
antero-dorsal part of ORB and ventral part of PORd areas, while on
the medial surface by the POL area, parts of PGd and PGv subareas
situated close to the pregenual sulcus and part of XM area (Fig. 15B).
It should be added that according to the general rule of strong connections between neighboring areas, some differentiation in rostro-caudal direction was observed. The areas of the premotor cortex situated
most caudally in the FAC have strong connections with caudal prefrontal areas, weak connections with central prefrontal areas and no connections with the most rostral ones. It is worth mentioning that the
premotor region receives also connections from the caudally situated
primary motor cortex.
Summary of cytoarchitectonic observations. Diversity of some FAC
areas which is e ~ p r e s s e dby their differing pattern of connections is
also related to their cytoarchitectonic features. It was observed that the
most rostrally localized FAC areas differed in their cytoarchitecture from
&he central and caudal areas. The areas of the rostral subregion are
characterized by thick cortex and its layers, indistinct borders between
the layers and uniform sizes of neurons. In areas of the central and
caudal FAC subregions cytoarchitectonic features are differentiated in
dorso-ventral direction. The dorsal areas of the central and caudal subregions are characterized by thick layers I11 and V without distinct borders between them. Moreover, in dorsal areas of the caudal subregion
there appear in these layers more numerous large pyramidal cells. The
ventral areas of the central and caudal FAC subregions in comparison
to the dorsal ones possess thinner layers I11 and V with more distinct
border between them and more uniform sizes of their pyramidal neurons. The ventral areas of the caudal subregion are additionally characterized by compact structure of layer VI.
DISCUSSION
On the basis of the present data on cytoarchitectonics and a pattern
of intrinsic collnections, the idea of existence in the dog's frontal association cortex of two main zones, dorsal and ventral was supported.
The dorsal zone includes two previously identified regions, the prefrontal and premotor one. However, the problem of the course of caudal
border of the area called in this paper the frontal association cortex in
various mammalian species is still under discussion. The majority of
researchers identify the term "frontal association cortex" with prefron-
tal region and they believe that in primates it is situated rostrally to
cytoarchitectonic area 6 and 8 (2, 22, 41, 58). According to other authors
the frontal association cortex involves also premotor area 6 (35, 45, 47).
In primates cytoarchitectonics is the criterion to determine regions of
the frontal lobe cortex. In this cortex the granular prefrontal region
and the agranular motor region can be easily distinguished (2, 6, 8,
56 - 58). The premotor cortex is characterized by a small degree of
granulation. However, this criterion cannot be used for subprimates,
including carnivores in which the whole frontal lobe cortex is rather
agranular (1, 48, 49). Our cytoarchitectonic observations (present paper)
confirm the above view, since in the dog we did not succeed in determining dictinct cortical layer IV, either in the prefrontal region or the
premotor one. However, some researchers separate layer IV in some
prefrontal areas, while in other areas this layer is difficult or even
impossible to identify (24, 31, 55). We observed also that layers I11 and
were developed better than other ones. Differences in their structure
can help to distinguish the frontal association cortex from the located
caudally motor cortex. It is believed that the primary motor cortex is
identified by the presence of gigantic pyramidal neurons in layer V
(19). Layers Vi and I11 of the premotor and dorso-caudal prefrontal cortex also contain large pyramidal neurons, although not as gigantic and
numerous as the ones in the motor cortex. The size and density of such
neurons decrease in the direction from the motor to the prefrontal cortex. Gradual change in size and density of pyramidal cells in the whole
area situated rostrally to the motor cortex gives no evidence to separate premotor cortex from the prefrontal one and suggests that the
FAC can be considered as separable entity. Therefore the prefrontal
and premotor regions were defined here as one separate zone and named the dorsal FAC zone. Moreover, the obtained results let us point
out that this zone differs from the ventral FAC zone also in the thickness and distinctness of cortical layers, as well as their neuronal density. Some cytoarchitectonic differences between dorsal and ventral parts
of the prefrontal cortex were observed in the monkey and cat (5, 12).
In these species the differences are explained by a later onto- and
phylogenetic development of the dorsal part of the prefrontal cortex as
compared to the ventral part (15, 17, 47, 50).
The results we obtained in dogs indicated that dorsal and ventral
zones of the frontal association cortex differed also in a connectional
pattern of their intrinsic cortical connections. The cortical areas localized within each of the zones strongly link with one another by short
cortico-cortical connections, but are very weakly connected with the
areas of the other zone. In the cortex where the two zones overlap, the
connections from them overlap as well, forming thus the transitional
zone. Thus, the'most intensive contact between dorsal and ventral zones
was observed in their transitional zone, while the extremely located
areas on the dorsal and ventral surfaces of the hemisphere are connected rather weakly with one another. Similar relations were described
in the monkey, though the description does not clearly identify the
zones (3 - 6, 21). In the monkey morphologists identified strong connections within the dorsal or ventral subregions of the prefrontal cortex
situated above and below principal sulcus, respectively. Moreover, these
two subregions are mainly linked within the principal sulcus cortex
(21). Comparing the results obtained in the two species, it can be suggested that the dog's orbital gyrus cortex situated on the lateral surface of the bemisphere is an analog of the monkey's cortex of the
principal sulcus region.
In the cat four sectors were identified in the prefrontal cortex on
the basis of the organization of cortico-cortical connections (10). However, both dorsal sectors are strongly connected with one another and
with the premotor cortex, which resembles the connectional pattern in
the dog.
The division of the dog's FAC into dorsal and ventral zones presented
here closely correlates with the results obtained earlier in our laboratory
concerning the organisation of distal cortico-cortical (36, 37) and subcortical (25 - 28, 30, 52, 53) connections of this cortex. This division
of the FAC can be justified by the fact that the entire dorsal zone (i.e.
the prefrontal and premotor regions) was connected with the subcortical
structures and cortical areas, related to the regulation of the motor activity and processing of the sensory information. On the contrary, the
ventral FAC zone is connected with structures and cortices usually assigned to the limbic system. It is of interest that all results we obtained
suggest approximately the same borders of the zones in the frontal association cortex of the dog's brain.
This investigation was supported by Project CPBP 0401 of the Polish Academy
of Sciences.
ABBERVIATIONS
CA
CJ
CX
f
fPs
FPS
area composita anterior
area composita interna
area composita precruciata
fissura
fissura presylvia
area of the bottom of the presylvian fissure
FAC
G
HRP
MI
MI1
ORB
ORBa
ORBd
ORBV
PFC
PG
PGd
PGv
PM
POL
PORd
PORv
PK.
PRa
PRL
s
sA
sCor
sCr
sG
spg
SPG
sRha
SRHa
SG
SPR
SPRa
SPRL
XC
XL
XM
XP
frontal association cortex
area genualis
horseradish peroxidase
primary motor cortex
secondary motor cortex
gyrus orbitalis
gyrus orbitalis pars anterior
gyrus orbitalis pars dorsalis
gyrus orbitalis pars ventralis
prefr'ontal cortex
area pregenualis
area pregenualis pars dorsalis
area pregenualis pars ventralis
premotor cortex
area polaris
area paraorbitalis dorsalis
area paraorbitalis ventralis
gyrus proreus
gyrus proreus pars anterior
area prorea lateralis
sulcus
sulcus ansatus
sulcus coronalis
sulcus cruciatus
sulcus genualis
sulcus pregenualis
area of the bottom of the pregenual sulcus
sulcus rhinalis anterior
area of the bottom of the anterior rhinal sulcus
area subgenualis
gyrus subproreus
gyrus subproreus pars anterior
gyrus subproreus lateralis
area precruciata centralis
area precruciata lateralis
area precruciata medialis
area precruciata posterior
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Accepted 20 January 1988