Download ORGANIZATION OF CORTICAL AFFERENTS TO THE FRONTAL

ACTA
NEUROBIOL. EXP.
1987, 47: 137-161
ORGANIZATION OF CORTICAL AFFERENTS TO THE FRONTAL
ASSOCIATION CORTEX IN DOGS
Grazyna MARKOW-RAJKOWSKA and Anna KOSMAL
Department of Neurophysiology, Nencki Institute of Experimental Biology
Pasteura 3, 02-093 Warsaw, Poland
Key words: dog's frontal as,sociation cortex, cortical afferents, HRP method
Abstract. The source of cortical frontal association cortex (FAC) afferents and their terminal distribution in the dog's brain was determined
by the HRP tracing method. It was shown that the sources of ipsilateral
FAC afferents are limbic and paralimbic areas of allo- and mesocortex
and parasensory areas of the neocortex. Most of these areas with the
exception of the piriform olfactory cortex could be characterized as cortical association fields. The terminal distribution of FAC afferents gave
evidence to distinguish dorsal and ventral FAC zones. The dorsal FAC
zone which includes the premotor and dorsal prefrontal regions is supplied by afferents originating in the temporal, parietal, occipital, perirhinal and parahippocampal cortical areas. In contrast, the ventral FAC
zone, involving the ventral part of the prefrontal cortex, receives characteristic projections from the subcallosal area and from the anterior
parts of the piriform cortex. However, both FAC zones receive intensive projections from the cingular and insular cortices. The organization
of FAC afferents in the dog was discussed in comparison with ather
species.
INTRODUCTION
Previous research on the dog's frontal association cortex (FAC) based
on behavioral effects of lesions (9, 10, 25, 32, 33, 40, 63, 64) as well as
cyto- (1, 19, 24, 61) and myeloarchitectonic (34) studies have shown mor-
pho-functional heterogeneity of this cortical region. Recent results show
the diversification in afferent projections into particular FAC parts coming from thalamic and also from extrathalamic structures (26-30, 51,
65, 67, 68). It is particularly well expressed by the distribution of indirect FAC afferents passing via mediodorsalnucleus (MD), which is
known to be precisely and topographically connected with this cortex
(65). Since MD afferents were determined, it seems justifiable to distinguish within FAC two principal regions, namely the dorsolateral and
medioventral. The dorsolateral FAC region is via the lateral MD segment
predominantly related to structures involved in the regulation of motor
activity, such as motor cortex, nigro-striatal system and cerebellar nuclei (65). In contrast, the medioventral FAC region via the medial MD
segment is related to the structures of the limbic system i.e., the cingular and insular cortices, amygdaloid complex, septum, nucleus of diagonal band, anterior olfactory nucleus and olfactory tubercle (65).
Cortical ipsilateral afferents and their distribution within the FAC
region in the dog are unknown, while in other species they are generally
less known than the subcortical ones. Previous investigations in various
species have shown that they originate in the cortex which can be determined as "nonprimary" or parasensory, as well as in paralimbic (3-8,
11, 12, 15, 16, 21, 22, 41, 43, 44, 50, 52-56, 58-60, 72). Among the mammalian species the cortico-frontal connections are the richest and best
organized in primates. The results obtained from Rhesus monkeys showed the existence of abundant projections from the association parasensory areas of the temporal, parietal and occipital neocortex reaching
predominantly the dorsolateral fields of the frontal association cortex
(3, 4, 15, 21, 22, 41, 52, 54). On the other hand, the frontal orbital surface receives connections mainly from limbic and paralimbic mesocortical areas like the cingular, subcallosal, temporal pole, perirhinal, parahippocampal areas, as well as from the entorhinal, subicular and presubicular limbic allocortical areas (2, 52, 53, 72). The authors, studying cortical connections in the monkey (52) and in the cat (60) divide the dorsolateral convexity of the frontal association cortex into prefrontal and
premotor regions. This division was made on the basis of differences in
the terminal distribution of the connections originating in the first and
second order parasensory areas. The first-order (proximal) parasensory
areas send afferents to the premotor region, whereas the second-order
(distal) areas reach the prefrontal region. Up to now, only the premotor
region apart from its characteristic connections, has been distinguished
in the monkey from the point of view of its electrophysiological features. As for other features, the presence of the movement-related neurons
was defined (71) as active due to the occurrence of some sensory signals.
However, similar neurons were also found in the caudal region of the
dorsolateral prefrontal cortex (13, 14). Such results could suggest the
lack of a sharp border between the prefrontal and premotor regions. In
other species, like the bush baby (56), cat (6-8, 20, 43, 44, 59, 60), guinea
pig (55), hamster (58) and rat (5, 11, 50), the FAC connections originating in most of the above mentioned cortical regions were detected, although the patterns of their organization differ to some extent. Among
subprimates the dog's brain is characterized by the relatively well developed frontal association cortex which occupies about 7O/o of the entire
neocortex (12).
Up to now, little has been known about the morphology of the cortex in the dog's brain, particularly about the localization of association
areas. According to the results obtained from monkeys and other species, most of the association cortical areas can be defined by their relation to the frontal association cortex. Thus, in the present study $we
intend do determine the sources of cortical FAC afferents and their terminal differentiation. We would like to find out whether the distribution of particular cortical projections provides additional arguments for
a division of the FAC area in the dog into dorsal and ventral zones, as
was suggested by the analysis of subcortical afferents topography. Moreover, we would like t~ discuss the extent to which the division of FAC
into prefrontal and premotor regions is justified from the point of view
of their afferent connections.
METHODS
Twenty-two young dogs were used to determine the distal intrahemispheric cortical FAC connections. Each animal was under nembutal
anesthesia 35 mglkg of body weight and received unilateral injections
of HRP (Sigma, Type VI or Boehringer Grade I). Particular FAC fields
were multiply injected in 8-12 points with 30-50°/o HRP solution with
total amount about 2 pl at a depth of 2-3 mm from the cortical surface.
The dogs survived for 48-72 h, then they were deeply anesthetized and
perfused with Mc Evans saline followed by fixative solution at pH = 7.4.
The removed brains were kept for 48 h in the fixative mixture with
30°/o sucrose and then frozen 40 pm sections were cut.
In order to reveal the reactive HRP in accordance with the procedures of Mesulam every 10th section was incubated in a medium containing benzidine dihydrochloride or tetramethyl benzidine (46, 47). The
sections were brightly counterstained with cresyl violet or neutral red.
Microscopic observations of HRP labeled cells were made with light and
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- Acta Neurobiol.
Exp. 4i87
dark field illumination. To determine the cortical regions in which labeled neurons were found, Kreiner's division of the dog's cortex (37)
was used.
RESULTS
The localization of injections. To investigate cortical intrahemispheric FAC afferents, particular HRP injections covered the entire surface
of the cortex. The injection sites, together with zones of their diffusion
are schematically shown in Figs. 1 and 2. The results are presented in
two groups, following the characteristic distribution of the frontal afferents.
GROUP I
Fig. 1. Diagramatic illustration of HRP injections in Group I (dorsal FAC cases)
presented on the schemes of the lateral ( A ) and medial (B) surfaces of the frontal
lobe. The black area indicate the site of injections; broken lines show the extent
of enzyme diffusion. For the names used, see Abbreviations.
GROUP I1
Fig. 2. Diagramatic illustration of HRP injections in Group I1 (ventral FAC cases).
Denotations as in Fig. 1.
Group I involved dorsal injections made in dogs 1-12 (Fig. 1) and
covering dorsal, dorsolateral and dorsomedial fields of the FAC. Three
injections were placed in the premotor cortex (dogs D 1-3), whereas nine
others were injected in various fields of the prefrontal cortex (dogs D
4-12). Particular injections were arranged on the basis of their localization - namely, from posterior to anterior as well as from dorsal to
ventral directions. Group I1 included ventral injections made in dogs
D 13-21 (Fig. 2), which were placed in the ventral, ventrolateral or ventromedial fields of the FAC involving the prefrontal cortex. only.
Sources of cortical afferents to FAC. The results presented in this
paper refer to the distribution of the retrograde labeled cells situated in
cortical fields of the entire ipsilateral hemisphere. The cortical projections from the contralateral hemisphere as well as the intrinsic FAC
connections wiil be described in separate papers.
Distribution of labeled cells after dorsal injections (Group I ) . The
most representative distribution of labeled cells was found in dog 7 (Fig.
3). In this case, a large injection was placed in the dorsal FAC zone, involving mainly the caudal prefrontal and partly the premotor cortices.
A high concentration of reaction product was found on the dorsolateral
surface of the caudal proreal gyrus (PR), the central precruciate area
(XC) and a part of the dorsal paraorbital area (PORd), which is situated
on the medial wall of the presylvian fissure (Figs. 1 and 3A). However,
on the medial surface of the hemisphere its noticeable concentrations
were also found predominantly in the dorsal parts of the medial precruciate (XM) and dorsal pregenual (PGd) areas (Figs. 1 and 3B). A striking aggregation of labeled cells was observed in the two vast cortical
areas, on the medial surface in the cingular gyrus, while on the lateral
surface it was observed in the regions of sylvian (sS), ectosylvian (sEs)
and rhinal (sRh) sulci (Fig. 3A, B and C).
In the cingular gyrus, labeled cells were distributed through the entire length: frontally from the area around the callosal genu (G), and
caudally to the area of callosal splenium (RSPL) (Fig. 3B and C1-6). Labeled cells were found in the cortex of the surface of this gyrus, as well
as in the depth of the splenial sulcus (sSpl), which borders dorsally with
the cingular gyrus. The most extensive aggregation seemed to involve
the medial part of this gyrus (CN), whereas in its anterior part above
the corpus callosum labeled cells were fairly less numerous. I n the area
frontal to the genu as well as in retrosplenial and parahippocampal areas lying behind the spleniurp of the corpus callosum only single cells
were found (G, RSPL, PH in Fig. 3B, C1 and C6).
The cortex of the cingular region in which the labeled cells were
found correspond to fields: 32, 24, 23, 31, 30, 29 of Klempin's (24) and
Gurewitsch's (19) cytoarchitectonic maps of the dog's cerebral cortex, and
to area limbica prima (L,) and secunda (Lz) according to Adrianov's division (1). The same cortical fields were named as follows according to
the myeloarchitectonic division of Kreiner (35): area genualis - G, area
limbica anterior - LA, media - LM and posterior - LP. Thus, the
main projection to FAC originates from fields 23 and 24 of Klempin's
and Gurewitsch's division, based on the Brodman's nomenclature. ,The
ventral edge of the splenial sulcus, where labeled cells were also present
is usually regarded as a part of the cingular cortex (19, 24, 35), whereas
the dorsal edge and the bottom of the same sulcus belong to different
cortical regions (19, 24, 38, 39). Its anterior part is considered to be
parietal cytoarchitectonic fields 5 and 7, while the caudal part belongs to
fields 18 and 19 of the occipital cortex.
On the lateral surface, labeled cells were found in a vast region of
the cortex, and they covered a few cortical areas (Fig. 3A). Anteriorly,
labeled cells were situated along the rhinal sulcus (sRh), (Fig. 3A and
Fig. 3. Distribution of labeled neurons in different regions of the cerebral cortex after injection into the dorsal prefrontal and premotor FAC fields in the case of Dog. D7; A, lateral surface of the hemisphere; B, medial surface; C , frontal
sections from anterior (1) to the posterior (7). Black color is used for the places with the highest enzyme concentration;
broken lines, a region of enzyme diffusion; crosses, localization of labeled neurons of the surface of gyri; dots, i n the depth
of the sulci. Due to a large number of the labeled cells found in this case, each symbol (cross or dat) represents three labeled cells. For names used, see Abbreviations.
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P
W
C1-6). It should be emphasized that they also occuppied the most caudal
part of the orbital gyrus (ORB), between the presylvian (fPs) and the
anterior rhinal (sRha) sulci. This aggregation of labeled cell was continued more caudally around the sylvian sulcus (sS). But in the depth of
sylvian sulcus, as well as on the surface of the anterior part of sylvian
gyrus (S), the cells were most densely packed. The cortical region situated close to the rhinal and sylvian sulci is believed to belong to the insular cortex, but is named differently by the above mentioned authors.
According to the investigators of cytoarchitectonic, these are fields 13,
14 (18) or area insularis prima - I (I), while it is named area orbitalis
tertia (ORB 111) and area sylvia interna (SI) according the myeloarchitectonic division (34, 36). However, the cortex of the anterior sylvian
gyms is regarded as the insular (1) or temporal area (36).
The projection area described above continued dorsocaudally in the
medial and posterior parts of the sylvian gyrus, as well as in the depth
of the ectosylvian sulcus (S, sEs; Fig. 3A and C4-6). On the surface of
the ectosylvian gyrus (ES), labeled cells were less numerous (Fig. 3A and
C2-6). The terminology of the cortex of the medial and posterior sylvian
gyms is also inconsistent. Some authors include this cortex in the parainsular (I), but the others include it in the temporal region (36, 45).
According to Gurewitsch and Klempin, it corresponds to cytoarchitectonic field 52 (19, 24). The depth of the ectosylvian sulcus and ectosylvian
gyrus, however, has consistently been considered as temporal cortex (19,
24, 36). The cortex of the anterior and posterior ectosylvian sulci and of
the ectosylvian gyrus has been defined as fields 50, 22 and 20 respectively (19, 24). It should be stressed that the places in which labeled cells
appeared were localized outside the primary auditory cortex (66, 69, 70),
so they belong to its association area. The main projection group of cells
in the insulo-temporal region was surrounded by scattered labeled cells
(Fig. 3A). They were localized in the depth of medial and posterior suprasylvian sulci (sSs), caudal suprasylvian gyrus (SS) and posterior rhinal sulcus (sRhp), often named the perirhinal cortex (Fig. 3A and C
4-6). In the medial part of the suprasylvian sulcus, cytoarchitectonic
fields 5 and 7 are localized, while in its posterior part, field 21 is localized (19, 24). The caudal suprasylvian gyrus corresponds to field 20 (19,
24) or area TE (1) and area composita lateralis - CPL (36) of the above
cited divisions. In this case described labeled cells in parietal and occipital cortices form separate groups on the lateral or medial surface of
the hemisphere. The groups are a continuation of main projection zones,
but they do not overlap one another.
The second case of the FAC of dorsal injections group is represented
by dog D2 in which the injection was restricted to the premotor cortex
Fig. 4. Distribution of labeled neurons in different regions of the cerebral cortex after injection into the FAC premotor
region in the case of Dog D2. One symbol (cross or dot) stands for two cells. Other denotations as in Fig. 3.
-
P
V1
and placed in the anterior composite area (CA) of the lateral presylvian
wall (Fig. 4), thus more caudally than in the previous dog. Such a small
injection caused the labeling of a much smaller amount of cells: Their
distribution, however, seems to be very significant. The cells appeared
in the same cortical areas as in the previous subject, but their accumulation was observed in the upper parts of the projection zones.
On the medial surface the main aggregation of labeled cells was observed in the dorsal part of the cingular gyrus and in the dephh of splenial sulcus (CN, sSpl; Fig. 4B and C 1-5). They were significantly less
numerous in the ventral and caudal parts of this gyrus. In contrast to
the previous subject, labeled cells appeared additionally on the dorsally
neighboring cortex of the splenial gyrus (SPL), in the depth of suprasplenial sulcus (sSspl) and some single cells, in the marginal gyrus (MA;
Fig. 4B and ;C2-4). Thus, they occupied the upper parts of the cytoarchitectonic fields 5 and 7 of the parietal cortex (19, 24).
On the lateral surface of the hemisphere, labeled cells were mainly
aggregated in the anterior and medial parts of the ectosylvian sulcus,
predominantly in its depth, but also in thq neighboring dorsal part of
the ectosylvian gyrus (sES Es; Fig. 4A and C1-5). So, the main projection
to the premotor cortex originates from the anterior part of the temporal
cortex, i.e. from the region constituting the dorsal part of the projection
zone in the previous case.
Labeled cells in the insular cortex prevailed in the depth of the sylvian sulcus, whereas on the surface of the same gyrus as well as along
the rhinal sulcus such cells were less numerous (sS, S, sRhp; Fig. 4 A
and C2-4).
In the cortex of the lateral surface, similar to the cortex of the medial one, labeled cells also appeared more dorsally to the main projection area. Fairly numerous cells were found in the depth of the suprasylvian sulcus (sSs), as well as on the surface of the suprasylvian gyrus
(SS) and in the depth of the lateral sulcus (sL; Fig 4A and C3-5).
According to cytoarchitectonic maps these newly appeared cells could
be localized in fields 5 and 7 of the parietal cortex and the most anterior parts of the occipital cortex (19, 24, 39).
Distribution of labeled cells after ventral injections (Group 11). This
group is represented by two subjects D20 (Fig. 5) and Dl3 (Fig. 6). Injection in D20 covered the medioventral prefrontal fields: the ventral pregenual area (PGv), the subgenual area (SG) and a small part of the subproreal gyrus (SPR; Figs. 2 and 5). Following injection, labeled cells were
found mainly in two cortical areas: the cingular cortex of the medial surface and the insular cortex of the lateral one. In the cingular cortex, labeled cells were situated in the anterior and middle parts of this gyrus (G,
20
ORB
A
1 1
I
664
1
1
1
821
Fig. 5. Distribution of labeled neurons in different regions of the cerebral cortex after injection into the ventromedial
prefrontal FAC fields in the case of dog. D20. Denotations as in Fig. 3,
CN; Fig. 5B and C). Anteriorly, they were localized around the callosal
genu, while caudally they extended to the medial part of gyms, occupying approximately 2/3 of its length. The most caudal (retrosplenial)
part of the cingular gyrus was free of labeled cells. It is interesting to
mention that the main aggregationof cells was found only In the ventral
part of this gyms. Thus, in comparison with the distribution of labeled
cells in those cases with dorsal injections, the source of projection to the
ventral FAC covers exclusively the ventral part of the previous projection zone.
On the lateral surface of the hemisphere, labeled cells were distributed from the caudal part of the orbital gyrus, along the whole length
the anterior rhinal sulcus and both walls of the sylvian gyms [ORB,
sRha, S; Fig. 5A and C). They were mainly localized in the depths
of these sulci and only single cells - in the convexity of the orbital
and sylvian gyri. Single cells that appeared in, this case, slightly dorsal,
above the ectosylvian sulcus, seem to be caused by some spreading of
the injection into the dorsal FAC zone. In the case of other medioventral injections, labeled cells above the close vicinity of sylvian pulcus
cortex were never found. So unlike the cases of dorsal injections, labeled cells were not found outside the restricted region of the insular cortex.
Apart from the above mentioned cortical areas, labeled cells were
also observed in the subcallosal area (SC; Fig. 5B, and ,C1). The labeled
cells in this cortical field were never observed after any dorsal injection.
Thus, SC seems a specific source of projection to the ventral FAC zone.
This cortex is defined as field 25 of Klempin's cytoarchitectonic map
(24) and area subcallosa I (sCI) and I1 (SC 11) of the limbic cortex according to Kreiner's myeloarchitectonic division (35).
In the second case of the ventral group (dog D13), a small injection
involved the anterior part of the subproreal gyrus (SPR), predominantly
its lateral surface (Figs. 2 and 6 ) . Generally, less numerous labeled cells
were present in the same parts of the cingular, subcallosal and insular
cortices. However, some differences in the distribution of these cells were
observed. On the lateral surface of the hemi$phere, the main aggregation of labeled cells was found in the most anterior part of the insular
cortex involving the caudal orbital and anterior sylvian gyri (ORB, S;
Fig. 6A). This group uf cells was continued ventrally in the anterior piriform cortex (Ppir., Pamg; Fig. 6A, B and C1-4). The piriform cortex
seems to be specific source of projection into the most antero-ventral
prefrontal cortex. This cortex in various cytoarchitectonic maps of the
dog's brain is generally considered part of the limbic allocortex (1, 19,
24). Additionally, in the cases of ventrolateral injections, single labeled
Rspl
Fig. 6. Distribution of labeled neurons in different regions of the cerebral cortex after injection into the antero-ventral
prefrontal FAC fields in the case of Dog D13. Denotations as in Fig. 3.
cells appeared neighboring the insular parts of the temporal cortex (Fig.
6A - pluses in S).
In all cases of injections labeled neurons were mainly localized in
cortical layer I11 while fewer were found in layers 11, V, VI (Figs. 7 and
8). Most often they were pyramidal cells of medium size, although some
oval and stellate small neurons were also observed. Often they had
a tendency to aggregate into small groups.
Organization of cortico-frontal projections. Table I summarises the
results of all injections into FAC which caused the labeling of cells in
the following cortical areas: the piriform, cingular, subcallosal, parahippocampal, perirhinal, insular, temporal, parietal and occipital. In the cingular and insular cortices, numerous labeled cells were observed in all
cases of injections. Both mesocortical areas gave rise to the most abundant and significant projections to the entire FAC. However, we would
like to stress some differentiation of cingular afferents. The medial part
of the cingular gyrus (CN) sends more abundant connections to the dorsal FAC, whereas its anterior part (G) sends more to the ventral FAC.
In the remaining cortical areas, labeled cells appeared following either
dorsal or ventral injections (Table I).
The dorsal FAC is provided with afferents originating in the parahippocampal and perirhinal mesocortical areas, as well as the temporal,
parietal and occipital neocortical regions. In contrast, the ventral FAC
receives afferents from the subcallosal area of the mesocortex and the
piriform area of the allocortex. The only exception is the temporal cortex which, apart from the main projection to the dorsal, also sends some
afferents to the ventrolateral FAC.
The arrangement of particular cortical areas giving rise to frontal
projections and their terminal distribution is graphically presented in
Fig. 9. The cortical areas of the insular cortex (INS) and the cingular
gyrus (G, CN, RSPL), (dense vertical lines in Fig. 9A), which give rise to
strong projections into the entire FAC (sparse vertical lines in Fig. $4
occupy) the central position of both lateral and medial surfaces of the
hemisphere. The cortical areas such as parahippocampal (PH), perirhinal
(PRH), temporal (TE), parietal (PA), occipital (OC) which are the sources
of projections into the dorsal FAC (sparse slanting lines in Fig. 9B) constitute an outer ring of the cerebral cortex (dense slanting lines in Fig.
9B). The areas which send specific projection to the premotor cortex of
the dorsal FAC (sparse lines slanting to the right in Fig. 9B) occupy the
most dorsal position in the same outer ring of the cortex (dense lines
slanting to the right in Fig. 9B). However, the subcallosal (SC) and piriform (PIR) cortices, supplying the ventral FAC zone (sparse horizontal
lines in Fig. 9C) are localized most ventrally in the inner ring of the
Fig. 7. Microphotograph of HRP labeled neurons in the central part of the cingular gyrus following dorsal FAC injection
dog D5; A, in a light field; B, in a dark field. Arrows indicate groups of labeled cells.
Fig. 8. Microphotograph of HRP labeled neurons; A, in the dorsal wall of the ectosylvian sulcus following dorsal FAC injection
in the case of dog D 7. The labeled neurons are set in a smallgroups, often in vertical rows (arrows); B, the labeled neurons
in the upper bank of the splenial sulcus following dorsal FAC injection in case of dog D5.
Cortical regions containing the labeled neurons following FAC injection
Localization j
of injection
-
1
Allocortex
1
Gyrus cinguli
G
-1
2
I
+
-
Area
subcallosa
I/ ++ I
CN
RSPL
11 1 2 -
1
cortex
parahipoI campalis
cortex
perirhinalis
Cortex
insularis
Cortex
temporalis
+
+
++
++
+
+++
++
++
+++
++
+
+++
+++
+
++
+++
++
++
++
++
++
+
+++
+++
+++
+
+++
+++
++
+++
+++
+++
+
+
+
+
-t
+
+
1 -
13
,
16
17
18
19
20
21
++
+
-
+++
-
1
+
+i-+
+-
The number of plus sigus
(+)
+
+
++
++
+
+
+
+
+
++
++ I +
1
1
+
+
-+ 1 - ++
+
++
+ 1 ++
++ +++ + I ++
+++ ++ + ' +
-
'
+-
+
-
-
I
-
Neocortex
+
I
I1
--- . -.
Mesocortex
-
-
-
-
-
-
-
I
-
I
-
-
indicates a relative number of labeled cells in one section;
10 cells; -, indicate of labeled cell.
+,
-
1-5 cells; + I - ,
1
Cortex
parietalis
Cortex
I occipitalis
++
I
++
++
++
+
++
++
++ I
+-
+
-
-
-
-
-
5-10 cells;
-
+
+
+
++
+
-
l
+++,
-
-
more than
cortex (dense horizontal lines in Fig. 9C). Thus the main differences of
connectivity pattern could be attributed to the dorsal and ventral FAC
zones. The dorsal FAC is more abundantly supplied by afferents from
various fields of meso- and neocortex, while the ventral FAC is supplied
Fig. 9. General schemes of the topography of the distal intrahemispheric FAC
cortico-cortical connections shown on the lateral (1) and medial (2) surfaces of
the hemisphere. The cortical areas which are the source of afferent connections
to the FAC are illustrated by differently arranged dense lines, while the sites
of termination of these projections are indicated by the same, but sparsely arranged lines; A, the areas that are the source of strong connections to the entire
FAC are marked with vertical lines; B, cortical areas giving rise to differentiated
projection to the dorsal zone of FAC are indicated by slanting lines. Lines slanting
to the right, areas projecting to the premotor cortex; lines slanting to the left,
areas projecting to the prefrontal cortex; C, cortical areas sending differentiated
projection to the ventral zone of FAC are Indicated by horizontal lines. For the
names used see Abbreviatlons.
by afferents originating in meso- and allocortex. However, it should be
mentioned that the mesocortical areas related to dorsal or ventral FAC
zones are localized differently.
DISCUSSION
The results reported here allow recognition for the first time the
association cortical areas in the dog's brain on the basis of their relation
to the FAC area. The organization of the cortico-frontal connections is
considered from the point of view of the localizations of sources of cortical projections and their terminal distribution in the FAC area.
The insular and cingular regions of the mesocortex form a strong
ipsilateral projection reaching the entire FAC. The insular cortex, named by some authors limbic (17, 62) and by others paralimbic (48) area,
was identified in various species as a cortex situated in the depth of
sylvian sulcus as well as in the anterior sylvian gyrus (1, 17, 18, 36, 42,
57). In accordance with the data as well as with the present results it
seems justifiable to include into the insular area the cortex localized in
the anterior part of the rhinal sulcus and in the most caudal part of the
orbital gyrus. Such a point of view is consistent with the previous cytoarchitectonic and myeloarchitectonic results (1, 19, 24, 34, 36) as well
as with the distribution of the cortical MD afferents (65) in the dog.
However, the projection from these cortices seems to be differentiated
to some extent. In the dorsocaudal insular cortex originate afferents
which terminate more densely in the dorsal part of FAC zone, whereas,
the antero-ventral insular cortex is a source of connections which predominantly supply the ventral FAC zone. The studies of connectivity of
the insular cortex in other species provide further evidence for its morpho-functional heterogeneity (17, 18, 48, 49, 58). Definite differentiation
of this cortical region in the dog needs further morphological and functional examination.
The limbic cingular cortex, involving the entire region situated in
front of and above the corpus callosum, is not homogeneous in the dog
brain. On the basis of the connections presented the cingular cortex
could be divided into three parts: (i) The anterior part predominantly
supplies the ventral FAC zone which is identified as the prefrontal cortex. (ii) The medial part of the cingular cortex sends abundant 'projection
mainly to the dorsal FAC zone in which the dorsal prefrontal region
receives more intensive connections than the premotor one. (iii) A weak
projection of the posterior cingular part often named the "retrosplenial
cortex" also reaches mainly the dorsal FAC zone. The diversity between
the anterior part and the rest of the cingular cortex was presented in
previous electrophysiological studies (23) and justified by subcortical connections (65). In previous studies of other species (8, 11, 21, 43, 55-57),
the projection from the cingular cortex was detected mainly to the prefrontal cortex with the monkey only having projection to both the prefrontal and premotor regions (2, 52, 53). Usually, the projection was described as strong, but the terminal areas were differently determined.
Thus, in spite of the interpretation of the above results in the dog and
the conclusion that the both insular and cingular cortices supply the entire FAC zone, it should be emphasized that some of their parts are
closely related to the ventral, while others are related to the dorsal FAC
zone.
The cortical areas forming differentiated frontal projections terminate in either the dorsal or ventral FAC zone. The dorsal FAC zone
receives afferents from the temporal, parietal and occipital neocortical
areas, as well as from the perirhinal and parahippocampal areas of the
mesocortex. On the contrary, afferents to the ventral FAC zone come
from the subcallosal field of the mesocortex and from the anteromedial
parts of the piriform lobe which belong to the allocortex.
Among the structures which supply the dorsal FAC zone, the most
plentiful connections originate in the temporal cortex related to the depth
of the ectosylvian sulcus. Moreover, temporal afferents that supply the
premotor cortex originate from a more dorsally situated area of the projection than those supplying the prefrontal cortex. This cortex was identified with morphological (45, 66) and electrophysiological (69, 70) methods as an association auditory area. Additionally, a weak projection
originated in the posteromedial part of the suprasylvian sulcus. A corresponding source of frontal afferents was determined in the cat as an
auditory-visual association cortical area (6, 60). In the primates, like
carnivores, association fields of the temporal cortex are to source of
a strong projection to the dorsolateral prefrontal cortex (21, 22, 52).
Other neocortical areas of the parietal and occipital lobes give rise
to weaker projections that terminate exclusively in the dorsal FAC zone.
Afferents to the premotor region originate in the more dorsal part of
the outer projective ring of both cortical surfaces than to the prefrontal
one. These regions correspond to the somatosensory association cortex
(1, 19, 24, 38). Occipital afferents originate in the posterior parts of the
same projection zone and are regarded as the visual association cortex
(1, 19, 24, 39). Comparable projection8 from the association parieto-occipita1 fields are described in the cat (44, 60) and monkey (15, 22, 52, 54)
as terminating predominantly in the premotor cortex. In our material,
a n additional weak projection to the dorsal FAC 'zone may come from
the perirhinal and parahippocampal fields of the mesocortex. The perir-
hinal mesocortical field, situated between the outer neocortical and inner allocortical ring in cat, is identified as visual association cortex (6,
18, 60). The projection from the hippocampal formation and parahippocampal cortex was identified in the cat (6, 8, 20) and the monkey (16,
52); in the dog, however, it seems to be very weak.
The ventral FAC zone, unlike the dorsal zone, receives characteristic
projections from the limbic areas. They originate in the mesocortical
subcallosal field, as well as in the anterior and medial parts of the piriform cortex (allocortex). It should be stressed that the piriform cortex, as
an olfactory projective zone, is an exception in general pattern of FAC
connections. This is the only primary sensory cortex which supplies the
FAC area and can be explained by the peculiarity of the dog's behavior.
Such results agree with previous data obtained on the dog, which showed that these structures supply the ventral FAC zone indirectly also,
through the medial MD segment (65). These MD afferents also originate
from the anterior piriform cortex. Afferents from the piriform cortex to
the same FAC part were found in the rat (57) and cat (6, 7). In the monkey, however, this projection origin also involved the most caudal part
of the piriform lobe, the entorhinal cortex (16, 72). Recently it has been
shown that in the monkey, the entorhinal afferents terminate in a vast
area of the frontal cortex (16), which may correspond to both the ventral and dorsal FAC zones in the dog.
A basic pattern of the distribution of cortico-frontal connections in
various mammalian species is generally similar. Slight differences between the phylogenetically less developed rodents and more developed
primates could refer to the intensity of this projection and the extent
of the cortical regions giving rise to this projection. It seems that in carnivores and rodents, FAC connections with limbic and paralimbic areas
of the allo- and mesocortex are stronger and more scattered than with
the neocortical areas. On the contrary, in primates the connections with
neocortical parasensory areas prevail and they are more focused. Among
subprimates, the extent of the cortical regions giving rise to the frontal
projection in the dog (present results) is most similar to that observed
in the cat's brain (8). It is difficult to compare the pattern of terminal
distributions of particular projection system in lower mammals because
of significant differences in the extent of FAC. In the monkey, however,
the pattern of termination of afferents originating from the primary and
secondary parasensory areas enabled the division of the frontal lobe
association cortex into the prefrontal and premotor regions (52). In our
opinion, the present results show that in the dog the primary and secondary parasensory areas could not be clearly determined on the same
basis. The areas of termination of particular projections seem to be wider
3
- Acta Neurobiol. Exp.
4187
than i n the monkey and to a greater extent they overlap with projections from the limbic and paralimbic cortices. The premotor cortex shares the features of connectivity with the dorsal prefrontal cortex. Therefore, it would be more justified to divide the entire frontal lobe association cortex in the dog into the dorsal and ventral zones. According to
such a division, the ventral FAC zqne could be characterized by strong
connections with the limbic and paralimbic areas of the meso- and allocortex which occupy the central and inner ring of the projection zone,
whereas the dorsal FAC zone would be characterized by its relations to
the mesocortical limbic and paralimbic areas of the central projection
area, as well as to the neocortical parasensory areas that constitute the
outer projection ring.
Apart from receiving the cortical afferents from parasensory neocortical fields, the most characteristic feature of the dog's dorsal FAC zone
is its relation to the motor system. Morphological evidence supporting
such a point of view consists, on the one hand, in the existence of a chain
of short cortico-cortical connections linking the primary motor cortex
with the dorsal prefrontal fields (30) and, on the other hand, in the
connectivity with subcortical structures involved in the regulation of
motor activity (65). The most significant evidence seem to be the connections between the dorsal FAC zone and the lateral MD segment and via
it, with the primary motor cortex, as well as with the structures of the
nigrostriatal system and cerebellar nuclei (65). Moreover, the projection
from the ventral anterior thalamic nucleus, which is usually considered
as a characteristic for the premotor cortex, in the dog involves both
the premotor and dorsal prefrontal cortici, thus comprising the entire
dorsal FAC zone (28).
This investigation was supported by Project CPBP 0401 of the Polish Academy of Sciences.
ABBREVIATIONS
area
area composita anterior
area cingularis
area composita posterior
gyrus ectosylvius
firjsura
fissura presylvia
frontal association cortex
gYvs
area genualis
I
horseradish peroxidase
INS
MA
MD
OC
ORB
ORBd
ORBv
Pamg
PA
FG
'
PGd
PGv
PH
PIR
POL
PORd
PORv
Ppir
PR
PRH
PRL
RSPL
s
s
sA
sCor
sCr
sEs
sG
SL
spg
sRc
sRha
sRhp
sRspl
SS
ssp1
sss
sssp
SC
SG
SJ
SPL
SPR
SPRL
SS
TE
XC
XM
XP
cortex insularis
gyrus marginalis
nucleus medlaLis dorsalis
cortex occlpitalis
gyrus orbitalis
gyrus orbltalls pars dorsalis
gyrus orbitalis pars ventralis
cortex plriformis pars periamygdaloidea
cortex parietalis
area pregenualis
area pregenualis pars dorsalis
area pregenualls pars ventralis
area parahippocampalis
cortex piriformis
area polaris
area paraorbitalis dorsalis
area paraorbitalis ventralis
cortex piriformis pass prepisifarmis
gyrus proreus
cortex perirhinalis
area prorea lateralis
cortex retrosplenialis
sulcus
gyrus Sylvius
sulcus ansatus
sulcus coronalis
sulcus cruciatus
sulcus ectosylvius
sulcus genualis
sulcus lateralis
sulcus pregenualis
sulcus recurens
sulcus rhinalis anterior
sulcus rhinalis posterior
sulcus retrosplenialis
sulcus sylvius
sulcus splenialis
sulcus suprasylvius
sulcus suprasplenialis
area subcallosa
area subgenualis
area sylvia insularis
gyrus splenialis
gyrus subproreus
gyrus subproreus lateralis
gyrus suprasylvius
cortex temporalis
area precruciata centralis
area precruciata medialis
area precruciata posterior
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