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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). - - - 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). - 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 + + + + + + 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 / 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. + + + 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). + + + 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 REFERENCES 1. ADRIANOV, 0. S. and MERING, T. A. 1959. 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