The Cingulate Bridge between Allocortex, lsocortex and Thalamus ERVIN W. POWELL Department ofAnatomy, College of Medicine, University ofArkansas for Medical Sciences, Little Rock, Arkansas 72201 ABSTRACT The Fink-Heimer silver impregnation and the autoradiographic methods were used to study the fiber projections of the cingulate cortex in the squirrel monkey. I t was found t h a t this cortex provides inputs to the striatum, thalamus and several areas of isocortex. Evidence was found for a number of fiber projections (1) Fibers from the anterior limbic area were traced to the central part of the head of the caudate nucleus, putamen, septum, dorsomedial nucleus of the thalamus, anterior hypothalamus and lateral basal nucleus of the amygdala. (2) Projections from the cingulate area were traced to the lateral part of the head of the caudate nucleus, putamen, and to t h e centromedian, anterior, lateral dorsal, and lateral ventral thalamic nuclei and to medial nuclei of the base of the pons. (3) There were projections from t h e retrosplenial area of the anterior, latera l dorsal, dorsomedial, and posterior thalamic nuclei and lateral nuclei of the pons. These results indicate t h a t most of the cingulate gyrus is a n intermediate structure between the thalamus and overlying cortex. The anterior limbic area forms a bridge between the thalamus and other areas of the cingulate gyrus and the frontal cortex. (4) The retrosplenial area and the posterior part of the cingulate area bridge the adjacent visual sensory association cortex and pelvic areas of the sensory motor cortex, respectively. These areas of the cingulate gyrus project directly to the striatum as well as to the thalamus, structurally providing limbic system input to subcortical motor structures. The cingulate gyrus has been considered a n important cortical component of the limbic system since Papez ('37) proposed a n anatomical system of emotion. Although projections of the cingulate gyrus have been studied in the rat and cat, knowledge of the role and connections of the cingulate gyrus as applicable to primates is not yet adequate (Adey and Meyer, '52; Showers, '59; Kreig, '63; Siegel et al., '73). The anterior thalamic nuclei have been described as receiving most of the topographi c a l p r o j e c t i o n s of t h e c i n g u l a t e g y r u s (Gerebtschoff and Wauters, '41-'43; Kreig, '63; Siegel et al., '73; Powell et al., '74). On t h e other hand, some studies have suggested the absence of cingulothalamic projections (Cragg and Hamlyn, '59; Powell and Cowan, '64). Other workers have reported a large number of connections from the cingulate gyrus to extracingulate cortical gyri in the cat (Airapetyants and Sotnichenko, '67; Powell et al., '74). The purpose of this study is to investiANAT. REC. (1978) 190: 783-794. gate the projections from the cingulate gyrus and to discern what are the major nuclei of termination of those projections in a primate, the squirrel monkey. If, as implied above, cingulothalamic projections are sparse, and cingulocortical projections are more numerous than subcortical ones, then the cingulate gyrus may be a n important limbic system link between the thalamus and isocortex. MATERIALS AND METHODS Adult squirrel monkeys of both sexes weighing a t least 500 g were used in these studies. Anesthesia was induced by ketamine hydrochloride, 25 mg/kg intramuscularly, supplemented as needed. Prior to stereotaxic surgery, analgesia of the scalp was produced locally with 2%Xylocaine containing epinephrine. Electrolytic lesions were produced in 22 aniReceived July 25, '77. Accepted Oct. 31, '77 783 784 ERVIN W. POWELL mals, unilaterally, in one of three loci (fig. 1): (a1 anterior limbic region Brodmann's areas 24, 25, 32 (A 15-23, L 0.25, H 10.0); (b) cingulate region Brodmann's area 23 (A 6-12, L 0.25, H 10.5); and (c) retrosplenial region Brodmann's areas 29, 30 (P 1-A 2, L 0.25, H 810) according to Emmers and Akert ('63). The lesions were produced by 2 ma of current acting for 15 seconds, using a 0.3-mm calibre electrode as the anodal pole. After allowing six days for the development of maximal argyrophilia of degenerating axons, preterminals and terminals (Powell and Schnurr, '721, the animals were perfused with 10% formalin in 0.9% saline while deeply anesthetized; and the brains were treated subsequently essentially as described by these authors. The brains were immersed in 30% sucrose solution for three days prior to cutting frozen coronal sections. Selected sections were impregnated with silver a s described by Fink and Heimer ('67) and modified by Powell and Brown ('75). Additional sections were counterstained with cresyl violet to localize the lesion and the nuclei of the brain stem. Tritiated leucine was used in eight other monkeys to label the fast protein anterograde component in loci corresponding to those in which lesions had been placed. The same procedures were followed except a 26-gauge needle (attached to a 10-pl Hamilton syringe), instead of an electrode, was placed stereotaxically using the same coordinates (fig. 1). Aliquots (0.2 pl) of L-(4,5-3H-)leucine in normal saline were injected a t 1-minuteintervals until five injections had been made (1 p l total). The needle was left in place another five minutes to minimize reflux and dispersion of the solution. The labeled leucine (New England Nuclear) had a specific activity of 5 Ci/mmole and was concentrated to 10 Ci/pl. The animals were allowed a period of 24 to 26 hours for translocation of the labeled fast protein component (Lasek, '701, and then were sacrificed and prepared as described above. Rather than frozen sections, however, 8-pm paraffin sections were cut and every twentieth section from genu to splenium of the carpus callosum was selected. The sections were mounted on slides, processed for autoradiographic study, and counter-stained with cresyl violet according to the procedure described by Cowan e t al. ('72). Silver grains were resolved satisfactorily at a magnification of 1,000 x microscopically, and counts per 1,000 pm2 were made with the aid of a square grid ocular reticule. Background counts were obtained from blank slides similarly processed, and from contralateral neutral areas of sections such as isocortex, pons, and ventral lateral nucleus of the hypothalamus. RESULTS Both methods produced evidence of projections to cingulate cortex and to isocortical areas overlying the cingulate gyrus. Other cortical areas receiving projections were the superior frontal gyrus, the parietal operculum and the hippocampal gyrus (figs. 2-41. All of the described projections were observed to be most abundant on the side of the lesion or injection site and therefore the ipsilateral projections only were studied in detail. Differences in the topography of projection appear in the results between the two methods used and may be explained on several different bases: 1. The silver method as opposed to the autoradiographic method, destroys overlying cortical and fiber projections in addition to those of the cingulate gyrus and cingulum due to penetration of the electrode. This destruction results in argyrophilia which could account for projections seen using the silver method and which were not seen using autoradiographic methods. 2. Some topographic differences could be attributed to slight differences of size and location of foci since none could be expected to be exactly identical from one brain to the next, e.g., anterior nuclei (SM-70) vs. those for (SM-85). 3. The different staining chemistry of the two methods could account for some seeming indiscrepancies, i.e., the chemistry of silver impregnation of a degenerating axon is different than that of incorporating radioactive amino acids into neuronal protein constituents. In the case of the latter, possibly, only the larger functional ones are successfully labeled. In the case of using silver impregnation methods, possibly certain terminals are less tenaciously impregnated. This is most often attributed to their small size rather than to their metabolic state. The negative data of either method used in this study is not helpful. My opinion after using both is that the silver impregnation methods usually reveal degeneration that is not clearly relevant to the anatomical system being studied and the autoradiographic method is reluctant to label all of 785 CINGULATE PROJECTIONS A bbreuiations Ac, Anterior commissure Ag, Silver impregnation method Ah, Anterior hypothalamus Al, Anterior limbic area Am, Anteromedial nucleus of thalamus Av, Anteroventral nucleus of thalamus B, Background grain count11.000 pm* Cb, Cerebellum Cc, Corpus callosum Cd, Caudate Cg, Cingulate gyrus Cm, Centromedian nucleus of thalamus Cn, Cingulate area Cp, Cerebral peduncle Cr, Corona radiata Dm, Dorsomedial nucleus of thalamus Ec, External capsule Fb, Fornixbody Fc, Fornix column Gp, Globus pallidus 3H, Autoradiographic method Hg, Hippocampus gyrus Hp, Hippocampus Ic, Internal capsule In, Insular cortex Ip, Interpeduncular nucleus Lb, Basal lateral nucleus of amygdala Ld, Lateral dorsal nucleus of thalamus Lg, Lateral geniculate body Lp, Lateral posterior nucleus of thalamus Mb, Mammillary body Oc, Optic chiasma Ot, Optic tract Pg, Periaqueductal gray Pn, Pons Ps, Presubiculum Pt, Pretectum Pu, Putamen Pv, Pulvinar Re, Retrospinal area Sb, Subiculum Sc, Superior colliculus Se, Septum Sf, Superior frontal gyrus Sm, Squirrel monkey (case number follows) Sn, Substantia nigra So, Supraoptic nucleus Sp, Superior cerebellar peduncle Su, Subthalamus Th, Thalamus V, Ventricle Va, Ventral anterior nucleus of thalamus V1, Ventral lateral nucleus of thalamus Vp, Ventral posterior nucleus of thalamus Cb Fig. 1 Foci for three representative pairs of cases. Three cases illustrate t h e results obtained using the silver impregnation method in this study (SM-71,SM-60 and SM-70). and three were selected to illustrate the results obtained using the autoradiographic method (SM-84, SM-80 and SM-85). The cytoarchitectural areas of the medial hemisphere are indicated by Brodmann’s numbers. The cytoarchitecture of the cingulate gyrus for lesions anterior to SM-60 and SM-80 was agranular cortex typical of the anterior limbic area, while for SM-60and SM-80 and lesions posterior to them it was granular cortex, found in cingulate and retrosplenial areas. SM-84 'H SM-71 Ag Fig. 2 Degeneration (SM-71) and grain (SM-84) patterns observed as projecting from the anterior limbic area. Grain counts for the most dense 1,000/*m' are shown for the main structures. B = 6 indicates the background level. The count for the cingulate gyrus was taken 3 mm posterior to the injection focus. The A-P stereotaxic coordinates for diagrams from left to right are: A,51(note lesion and injection foci), A,,, A,,,, and A,,, respectively (Emmers and Akert, '63). CINGULATE PROJECTIONS TABLE 1 Grain counts obtainedl1,OOO pn' Structure SM-84 cg Sh Pu Cd Lh 12 7 so 133 92 v1 Av Am Ld Dm LP Cm Pv Ah Pt Pn Background 23 21 20 8 s7 6 8 7 38 8 6 6 ' SM-80 SM-85 138 12 43 86 cil 75 14 43 91 19 20 17 25 73 18 20 12 17 8 12 159 133 - 155 158 Is2 8 71 16 53 e 43 10 8 ' Only the counts underlined are considered t o represent targets above background counts. the reported known anatomy of the system being studied. Anterior limbic area Degenerated fibers of passage, as impregnated by t h e Fink-Heimer I method, were consistently traced across the cingulum and corona radiata into the internal capsule (fig. 2: SM-71). Collateral branches were traced to t h e central part of t h e head of the caudate nucleus and putamen where argyrophilia representative of preterminals and terminals was observed. Most of the axons traced through t h e internal capsule coursed to the thalamus via the dorsal thalamic peduncle (fig. 2). Argyrophilia, which included terminal and preterminal degeneration, was observed in lateral thalamic nuclei, dorsomedial nucleus, subthalamus, and dorsal hypothalamus (figs. 2, 5). A number of fibers were traced posteriorly in the medial part of the cerebral peduncle to degeneration in the ipsilateral medial nuclei of t h e basis pontis. Some fine argyrophilia was seen in t h e dorsal periaqueductal gray. No axons or terminals were impregnated in t h e anteroventral and anteromedial nuclei of the thalamus from this area of the cingulate gyrus. I t would be i n t e r e s t i n g t o know whether or not t h e density in the number of argyrophilic deposits representing axonal de- 787 generation in a target nucleus is indicative of the number of preterminal and terminal fibers in t h a t structure. Results using the autoradiographic method also revealed t h e central part of the caudate and putamen to be targets of projections from this area of t h e cingulate gyrus (fig. 2: SM-84; table 1). There was some spread of leucine to cells in t h e ventromedial part of the superior frontal gyrus in this case. Dark grains, representing transported 3H-leucine,were observed in the septum, lateral part of the dorsomedial nucleus of t h e thalamus, anterior hypothalamus (level not shown), and in the basal lateral amygdaloid nucleus. No grains above background levels were observed in other amygdaloid, thalamic, or hypothalamic nuclei, subthalamus, base of pons, or periaqueductal gray. Cingulate area Degenerated axons impregnated by use of t h e Fink-Heimer method were traced laterally across the cingulum to the corona radiata and internal capsule (fig. 3: SM-60). Degeneration in target nuclei, including associated terminals and preterminals hereafter referred to as terminal degeneration, was observed in the dorsolateral head of the caudate nucleus and dorsolateral part of t h e putamen (fig. 3 , 5 ) . Degenerating fibers of passage were traced from the internal capsule into the dorsal thalamic peduncle to terminal degeneration in the anteroventral nucleus of the thalamus. Terminal degeneration was also seen in the lateral part of t h e centromedian and lateral thalamic nuclei. Other fibers were traced from t h e internal capsule into the subthalamus, dorsal hypothalamus and substantia nigra via the lenticular and thalamic fascicles. Degenerating terminals were observed in t h e ipsilatera1 medial nuclei of the base of the pons. A few fibers in the external capsule were continuous with coarse terminals in the hippocampal gyrus. Silver grains developed using autoradiography were obvious in the dorsal lateral part of t h e head of t h e caudate nucleus, in the dorsal lateral part of the putamen, and in the centromedian nucleus of the thalamus (figs. 3, 5:SM-80). Silver grains indicating target nuclei were observed over the ventral lateral, medial part of the ventral posterior, and anteroventral, thalamic nuclei, and the medial nuclei of t h e base of the pons (fig. 3; table 1).No grain counts above background levels 788 ERVIN W. POWELL 789 CINGULATE PROJECTIONS TABLE 2 Comparison of results obtained usingsilver and autoradiographic methods Limbic Cingulate Retrosplenial Structure cg Sb Pu Cd Lb v1 Av Am Ld Dm LP Cm Pv Ah Pt pg Pn Ag 3n Ag 3n Ag w + 0 + + + + + 0 0 0 + + + + 0 + + + 0 + 0 0 0 0 (0 +) 0 (0 +) (0 0 0 0 0 + + 0 (0 + + + + + + + )' 0 0 0 0 + 0 0 +) + 0 0 0 + + + + + 0 + + + + 0 0 + + 0 0 0 0 + 0 0 0 0 + + + + + 0 (0 0 (0 + + 0 + + + + 0 +) 0 +) 0 + ' Data in parentheses represent areas positive for grain counts but negative in similar silver-impregnated cases. These differences appear to be due to the differences between the two techniques (fibers of passage and cell soma) and to the larger area of the injection site, especially for the retrosplenial area. were observed in the hippocampus, lateral part of the ventral posterior nuclei of the thalamus, subthalamus, hypothalamus, substantia nigra or interpeduncular nucleus. Retrosplenial area Degenerated fibers of passage were traced from the lesion through the corona radiata to the white matter of the hippocampal gyrus and subiculum and anteriorly in the cingulum to more rostra1 areas of isocortex (fig. 4: SM70). Some coarse degeneration was followed through the subiculum to the lacunar layer of the hippocampus. The main bundle of degenerated fibers, however, was traced anteriorly through the corona radiata to the dorsal thalamic peduncle where they entered the thalamus. Degenerated terminals were seen in the lateral posterior, lateral dorsal and dorsomedial nuclei. A few were observed in the ventral part of the anteromedial nucleus, medial part of the head of the caudate nucleus, periaqueductal gray, and lateral nuclei of the base of the pons. None were found in the putamen. Silver grains developed using autoradiography were seen in the medial part of the head of the caudate nucleus, the anteroventral, anteromedial, lateral dorsal, dorsomedial, lateral posterior and pulvinar thalamic nuclei as well as in the pretectum and lateral nuclei of the base of the pons (figs. 4, 5; table 1:SM-85). Grain counts slightly above background were observed in the presubiculum (table 1) and prestriatal cortex. No grains were seen in the hippocampus or periaqueductal gray in contrast to the degenerated fibers seen using the Fink-Heimer method (table 2). DISCUSSION The results support previous studies in the abundance and in the specificities of projections found (Adey and Meyer, '52; Airapetyants and Sotnichenko, '67; Powell et al., '74). The cingulate gyrus has been suggested as forming a link between allocortex and isocortex (Sanides, '70;Chronister and White, '75). The proposal by Papez ('37) and the data from retrograde studies of thalamic nuclei show that the cingulate gyrus receives many connections from anterior thalamic nuclei. The anterior thalamic nuclei are structures where there is convergence of anatomical projections from the hippocampus, septum, mammillary body, and parts of the cingulate gyrus (Powell, '73; Powell e t al., '74; this study). Data from this anterograde study (cingulothalamic projections) and data from retrograde (thalamocingulate projections) studies of others (Cowan and Powell, '54; Yakovlev e t al., '60; Powell and Cowan, '64) imply that there are more thalamocingulate projections than there are cingulothalamic ones. Our observations also indicated that anterior parts of the cingulate gyrus have many connections 790 ERVIN W. POWELL CINGULATE PROJE CTIONS 791 Fig. 5 Top half, comparison of silver-impregnated sections (Ag) and grain PH)densities using autoradiographic methods in the anteroventral nucleus (Av) none from the anterior limbic area (SM-71and SM-841, the cingulate area (SM-60 and SM-80) and the retrosplenial area (SM-70 and SM-85). Bottom half, comparison of silver-impregnated sections (Ag) from SM-60 with the grain density, using autoradiographic methods, from SM-80 in caudate (Cd),putamen (Pu),and centromedian (Cm) from the cingulate area. The possible reasons for differences in amounts of projection shown by the two methods are stated on page 784. These photographs represent the quantitative comparisons made on the basis of counts given in table 1 and the impressions gained from a continuous study of the silver impregnated material. The calibration mark applies for all photographs in each row. 792 ERVIN W. POWELL ISOCORTEX Frontal Cortex tl' ALLOCORTEX CINGULATE BRIDGE Fig. 6 Diagram of cingulate bridge between allocortex, isocortex and thalamus as proposed in this paper. posteriorly while posterior areas of the cingulate gyrus have many projections anteriorly via the cingulum. Therefore, the cingulate gyrus provides an anatomical bridge between the thalamus and isocortex as well as between the allocortex and proisocortex and isocortex as suggested by Chronister and White ('75). This structural bridge for the anterior limbic area would be primarily from the anterior nuclei to the frontal lobes. These connections might account for the short latency responses recorded by Desiraju ('76) in the frontal cortex following stimulation of the anterior limbic area. This study shows cingulate connections to the centromedian nucleus of the thalamus. Functional and anatomical relations between the centromedian nucleus and the striatum have been reported (Powell and Cowan, '56; Krauthamer and Bagshaw, '63; Bowsher, '66). Projections from frontal and cingulate cortex to the centromedian nucleus provide a structural basis for interal activation (selective?) a t the revel of the caudate nucleus. Bowsher ('66) found that stimulation of the centromedian nucleus inhibited unit firing in the caudate nucleus in the monkey. Talairach et al. ('73) reported that stimulation of the anterior limbic area produced patterns of sucking, palpation, or nibbling accompanied by EEG rhythms of 3-8 c/sec. Such effects on motor activity would be in addition to primary motor regulation from the cerebellum through ventrolateral and centromedian nuclei. This study supports claims (Adey and Meyer, '62; Raisman et al., '65; Airapetyants and Sotnichenko, '67; Pandya et al., '73) that fibers of the retrosplenial area of the cingulate gyrus terminate in the hippocampal gyrus and presubiculum but do not terminate in Ammon's horn. Argyrophilia seen in layers of Ammon's horn was probably due to damage of fibers other than cingulofugal ones contained in the angular bundle, since no terminals were found nearer to the hippocampus than the presubiculum in any of the sections studied using the autoradiographic method. Connections of the cingulate gyrus to cortical association areas, i.e., limbic area to frontal cortex, cingulate area to somatosensory cortex, and retrosplenial area to visual association cortex, as well as those to sensory association nuclei of the thalamus (Locke and Kerr, '73; Granier e t al., '70; Yakovlev and Locke, '611, form pathways which could provide sensory information to limbic structures of the temporal lobe and insula. 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