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Limbic Areas Have Been Quantitatively Stud­ Tex: an Outer Layer of Small Granular Type Cells, An CHAPTER 15 Development of the Limbic Cortical Areas 15.1 Neurogenetic Gradients in the Lateral Limbic 15.2.3 The Retrosplenial Area, 195 Areas, 187 15.2.4 Gradients Between Areas, 197 15.1.1 Radial and Transverse Neurogenetic 15.3 Neurogenetic Gradients in- the Orbital Cortex, Gradients, 188 197 15.1.2 Unique Longitudinal Neurogenetic 15.4 Correlations Between Neurogenetic Gradients Gradients, 188 and Anatomical Connections in the Limbic 15.2 Neurogenetic Gradients in the Medial Limbic Cortex, 198 Areas, 191 15.4.1 Connections of the Anterior Thalamic 15.2.1 The Dorsal Peduncular and Infralimbic Nuclear Complex with the Medial Limbic Areas, 191 Cortex, 198 15.2.2 The Cingulate Areas, 193 15.4.2 Thalamocortical Connections of the Gustatory Cortex, 198 As early as 1664, Thomas Willis wrote that the cortex hypothesis and named the interconnected cortical and on the borders of the cerebral hemispheres had unique subcortical structures the limbic system. Since then, anatomical features resembling a "hem" or "limbus." anatomical and functional links in the limbic system in In his 1878 paper, Broca called that area the "grande general and the medial limbic cortex in particular have lobe limbique" (reviewed in White, 1965). In rats as been widely studied in relation to behavior (Isaacson, well as in man, the limbic lobe is a continuous cortical 1974) and support has been provided for Papez' orig­ band encircling the neocortex. In this chapter, we use inal hypothesis. The participation of the lateral limbic the term limbic cortex to include parts of Broca's cortex in other circuits involved with emotional be­ limbic lobe that have been traditionally considered havior was' emphasized by Livingston and Escobar neocortex by some (Papez, 1937; MacLean, 1952; (1971). Indeed, the limbic cortex has unique anatom­ Isaacson, 1974), and variously called allocortex, ical connections when compared to the neocortex. For peripaleocortex, periarchicortex, and proisocortex by example, the mediodorsal thalamic nucleus projects specialists in cytoarchitectonics (Abbie 1940, 1942; exclusively to the limbic cortex (Leonard, 1972; Kret­ Sanides, 1969). The major components of the lateral tek and Price, 1974, 1977; Siegel et aI., 1977; Divac et limbic cortex are the insular, perirhinal, and gustatory aI., 1978; Beckstead, 1979; Sarter and Markowitsch, areas above and in the rhinal sulcus. The major com­ 1983; Groenewegen, 1988), and dopamine innervation ponents of the medial limbic cortex are the dorsal pe­ is more extensive in both the medial and lateral limbic duncular, infralimbic, cingulate, and retrosplenial areas than in the neocortex (Descarries et aL, 1987; areas in the medial wall. The two join in the orbital Kalsbeek et al., 1988). areas below the frontal pole. In contrast to the wealth of functional and anatom­ In 1937, Papez (1937) proposed that a group of in­ ical literature dealing with the limbic cortex, there are terconnected telencephalic and diencephalic struc­ only a few eH]thymidine autoradiographic studies of tures mediates emotional behavior. The cingulate and neurogenesis in the medial limbic cortex, all based on retrosplenial areas in the medial wall of the cerebral pulse labeling after single injections. Fernandez (1969) cortex were important parts of the "Papez circuit." questioned whether times of neuron origin in the cin­ Some years later, MacLean (1952) popularized Papez' gulate cortex in rabbits were linked with those in the 186 THE LIMBIC CORTICAL AREAS / 187 anterior thalamic nuclei; he concluded that develop­ riorly, the ventral agranular insular (AIV, Fig. 15-1) mental patterns between the two structures appeared in the rhinal sulcus and the dorsal agranular insular to be unrelated. In a detailed series of papers, Richter (AID, Fig. 15-l)just above AIV in the lateral cortical and Kranz (1978, 1979a, 1979b, 1979c, 1980) investi­ wall. The insular cortex continues posteriorly in the gated the kinetics of cell proliferation and cell migra­ rhinal sulcus as area AlP (posterior agranular insular tion in the cingulate gyrus in rats and found that ventral area). AIV and AlP correspond to Krieg's (1946a, superficial cells have earlier birthdays than dorsal su­ 1946b) area 13, while AlD corresponds to a more cir­ perficial cells, but they did not link that pattern to other cumscribed part of Krieg's area 14. Krieg (1946b) de­ developmental events in the cortex. Although some of scribes three cortical layers throughout the insular cor­ the lateral limbic areas have been quantitatively stud­ tex: an outer layer of small granular type cells, an. ied (Bayer, 1986), a complete neurogenetic timetable intermediate layer of pyramidal cells, and a deep layer has only recently been presented (Bayer, 1990a, with horizontally flattened cells. All areas of the in­ 1980b). sular cortex are situated above the claustrum, which The main goal of this chapter is to present quanti­ makes this area homologous to the human insular cor­ tative timetables of neurogenesis in the lateral and me­ tex (Krieg, 1946b). The gustatory cortex (GU, Zilles, dial limbic areas and in the orbital cortex. The major 1985, Fig. 15-1) is defined by its reciprocal connec­ findings are that the limbic cortex has neurogenetic tions with the taste area in the medial part of the tha­ gradients in both the transverse and longitudinal di­ lamic ventromedial nucleus (Wolf, 1968; Leonard, rections that differ from the global gradients found in 1969; Reep and Winans, 1982a, 1982b; Saper, 1982; the neocortex. We also show that the neurogenetic gra­ Shipley and Geinisman, 1984; Kosar et aI., 1986; Cech­ dients found in the limbic cortex correlate with the etto and Saper, 1987). GU forms the dorsal border of pattern of its thalamic innervation. AID and is incorporated into Krieg's (1946a, 1946b) area 14. The cellular layers are more distinct in GU, 15.1 NEUROGENETIC GRADIENTS IN THE and a sparse but definite layer IV can be distinguished, LATERAL LIMBIC AREAS similar to that seen in the secondary somatasensory area (Zilles and Wree, 1985). Posterior to the insular The insular cortex forms the dorsal border of the pir­ cortex, the perirhinal cortex (PR, Zilles and Wree, iform cortex. Zilles (1985) describes two areas ante­ 1985; area 35, Krieg 1946a, 1946b) lies in the rhinal "A"'~ ., . ... ,;... .. ~ ." ". .. , . , .. , ... '"' 'j '1 - • . .' ,":. r. "'. ~ ... ,.... .'. c~.:..' . 'j. >/. , .~,: ., I. , .. , . \ .:. AIV··. .~.. , ..' I . e· -:~ ..... 'il '. FIG. 15-1. Photomicrographs of the lateral cortical wall at level A8.2 in an animal exposed to [3H]thymidine on E18 and E19 and killed on P60. (A) low-magnification view showing the increase in the depth of labeled cells progressing from the ventral agranular insular cortex (AIV) through the dorsal agranular insular cortex (AID) and into the gustatory cortex (GU). The areas encircled with dashed lines are shown in higher magnification in Band C. (6 fLm paraffin section, he­ matoxylin/eosin stain.) From Bayer (1990a). 188 / CHAPTER 15 sulcus just below the auditory cortex and above the neurons originate on or before E16 in AIV but only entorhinal cortex. The cortical layers are thinner, and 26% of these neurons originate during this time in GU. the horizontally oriented cells in layer VI are especially In layer V (left column of graphs, Fig. 15-2), neuro­ prominent. For quantitative analysis, coronal sections genesis occurs earlier in AIV than in AID (P < 0.0001) were selected at nine anteroposterior levels (A9.2 to and earlier in AID than in GU (P < 0.0001). Again, A1.2; drawings, Fig. 15-3). there are sharp differences between AIV and GU. For example, 75% of the layer V neurons originate on or before E15 in AIV, while only 47% of these neurons 15.1.1 Radial and Transverse Neurogenetic Gradients originate during the same time period in GU. Layer VI neurogenesis occurs mainly on E14 (16%) and E15 When eH]thymidine injections are given on E18 and (65%) simultaneously in GU, AID, and AIV (all com­ E19, cell labeling patterns in the lateral cortical wall parisons P > 0.05; data are not shown). In the deep at level A8.2 (Fig. 15-1) indicate that only a thin band parts of AIV and AID, fewer neurons are generated of superficial cells are labeled in AIV in the rhinal sul­ on E14 and more on E15 than would be expected by cus (Fig. 15-1C), while the dorsally located GU (Fig. the pattern seen in GU. Possibly some of the oldest 15-1 B) has a considerably thicker band of superficial deep neurons are missing in AID and AIV. That cir­ labeled cells. These photomicrographs illustrate the cumstance is most likely due to the presence of the two neurogenetic gradients seen in all other neocort­ claustrum, which lies beneath the deep neurons in AIV ical areas: (1) a radial gradient (deep cells are older and AID. Claustral neurons originate mainly on E15 than superficial cells) and (2) a transverse gradient and E16 (in preparation). (ventral cells are older than dorsal cells). Since the transverse gradient is found throughout the entire ros­ trocaudal expanse of AIV, AID, and GU, only the data 15.1.2 Unique Longitudinal Neurogenetic Gradients for level A8.2 (drawing, Fig. 15-2) are illustrated. In layers II-IV (right column of graphs, Fig. 15-2), neu­ Unlike the neocortex, where there is an older-anterior rogenesis occurs earlier in AIV than in AID (P < to younger-posterior longitudinal gradient in nearly all 0.0001) and earlier in AID than in GU (P < 0.0001). areas, the lateral limbic cortex shows either a sandwich When AIV and GU are directly compared, 59% of the pattern, where older neurons are flanked anteriorly % GU "'Sl 40 30 20 % IT-TIl GUl40 10 ~ 30 ., 20 10 40 10 30 20 0 I )1fJffI/L 60 ffffPdb, Jw AIV 40 40 30 20 10 E13 14 .
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