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4 Bayer Exp Neurol 107 1 EXPERIMENTALNEUROLOGY 107,11&131(1990) Development of the Lateral and Medial Limbic Cortices in the Rat in Relation to Cortical Phylogeny SHIRLEY A. BAYER Department of Biology, Indiana-Purdue University, Indianapolis, Indiana 46205 limbique” (as reviewed in Ref. (45)). In rats and in man, [‘H]Thymidine autoradiography was used to investi- the limbic lobe is a continuous cortical band encircling gate neurogenesis of the lateral limbic cortex and mor- the neocortex. Phylogenetic relationships within the phogenesis of the medial and lateral limbic cortices in limbic lobe and with the neocortex were often the sub- adult and embryonic rat brains. Ontogenetic patterns jects of contradicting opinions and confusing terminol- in the limbic cortex are unique because some neuroge- ogy in the classical neuroanatomical literature (1,2,22, netic gradients are linked to those in neocortex, others 40). None of the hypotheses has found general accep- are linked to those in paleocortex. These findings are tance, and interest in the topic of evolutionary origin has related to hypotheses of cortical phylogeny. The experi- waned in recent years. Since ontogenetic patterns are mental animals used for neurogenesis were the off- important clues to phylogenetic links, a comprehensive spring of pregnant females injected with [‘Hlthymidine developmental study of the limbic lobe as a whole would on 2 consecutive days: Embryonic Day (E)13-E14, shed new light on old controversies. In 1974, Bayer and E14-E15, . E21-E22, respectively. On Postnatal Altman (10) started using the comprehensive labeling Day (P)60, the proportion of neurons originating dur- method of [3H]thymidine autoradiography to quantita- ing 24-h periods were quantified at nine anteroposte- tively determine timetables of neuronal birthdays rior levels and one sagittal level. Similar to neocortex, deep cells are generated earlier than superficial cells throughout the rat nervous system. With data presented throughout the lateral limbic cortex: layer VI mainly on in a companion paper (S), our forthcoming book on neo- E14-15, layer V on ElB-E16, and layers IV-II on cortical development (13), previous work on the hippo- E16-El6 There is a ventral/older to dorsal/younger campal region (6, 10) and primary olfactory cortex (8), neurogenetic gradient between the ventral agranular quantitative developmental analyses of the entire telen- insular, dorsal agranular insular, and gustatory corti- cephalic cortical mantle are complete. These studies cal areas and between ventral and dorsal orbital areas show that each major cortical “system” has characteris- beneath the frontal pole. Similar to paleocortex below tic neurogenetic timetables and gradients. the rhinal sulcus, limbic cortex in the rhinal sulcus has The developmental patterns in the limbic cortex are a “sandwich” gradient: the older posterior agranular unique in that they are linked on the one hand to the insular area is sandwiched by anterior and posterior neocortex and on the other to the paleocortex (piriform younger areas (ventral agranular insular and perirhi- and entorhinal areas) and archicortex (hippocampus). nal). To study morphogenesis, pregnant females were Consequently, the first goal of this paper is to discuss given single injections of [‘Hlthymidine during gesta- overall ontogenetic patterns in the entire cortex in rela- tion and embryos were removed in successive 24-h in- tion to hypotheses of phylogenetic origins. The second tervals (sequential-survival). Neurogenesis finishes goal is to present quantitative timetables of neurogen- first in ventral limbic areas, later in dorsal limbic areas, esis in the insular, perirhinal, and gustatory cortices. Al- and latest in neocortical areas. The cortical plate in the though some of these areas have been quantitatively region of the medial and lateral limbic cortices does not studied (8), a complete neurogenetic timetable has not have a separate subplate layer as is found in the region been done. The third goal is to examine the embryonic of the neocortex. Instead, layer VI in the limbic cortices development of the cortex, focusing on differences be- has unusually older cells that are generated simulta- tween center and edges. The unique location of unusu- neously with subplate cells. o 1990 Academic PEW, I~C. ally older deep cells in the medial and lateral extremes of the cortical plate may be linked to the distribution of dopamine axon terminals in the cortex. INTRODUCTION MATERIALS AND METHODS As early as 1664, Thomas Willis wrote that the cortex on the borders of the cerebral hemispheres had unique Long Survival 13HlThymidine Autoradiography anatomical features resembling a “hem” or “limbus.” In The experimental animals were the offspring of his 1878 paper, Broca called that area the “grande lobe Purdue-Wistar timed-pregnant rats given two subcuta- 0014-4&36/90 $3.00 118 Copyright 0 1990 by Academic Press, Inc. -3 LIMBIC CORTEX DEVELOPMENT 119 neous injections of [ 3H]thymidine (Schwarz-Mann; sp TABLE 1 act, 6.0 Ci/mM; 5 &i/g body wt) to ensure that cells Neurogenesis of the Layer V Cells in the Perirhinal Cortex” originating after the onset of the injections will be de- tected as labeled (comprehensive labeling). The injec- Injection % Labeled cells Day of % Cells tions (given between 8:30 and 9:00 AM) to an individual group N (mean + SD) origin originating animal were separated by 24 h. Two or more pregnant E13-El4 8 (A) lOOk El3 0.49 (A-B) females made up each injection group. The onset of the E14-El5 7 (B) 99.51 + 0.33 El4 4.75 (B-C) [3H]thymidine injections was progressively delayed by 1 E15-El6 6 (C) 94.75 * 1.29 El5 63.31 (C-D) day between groups (E13-E14, E14-E15, . .E21-E22) E16-El7 12 (D) 31.44 zk 7.65 El6 23.72 (D-E) so that the amount of neurogenesis could be determined E17-El8 9 (E) 7.72 + 2.41 El7 4.31 (E-F) within a single 24-h period. The day the females were E18-El9 6 (F) 3.41 + 1.01 El8 3.41 (F-G) E19-E20 6 Ok0 El9 0 sperm positive was designated Embryonic Day 1 (El). (G) Normally, births occur on E23, which is also designated ’ The data for the deep cells in the perirhinal cortex are given as an as Postnatal Day 0 (PO). All animals were perfused example of how they are derived for presentation in the bar graphs through the heart with 10% neutral (pH 7.4) formalin used throughout the paper. N refers to the number of animals analyzed on P60. The brains were kept for 24 h in Bouin’s fixative in each injection group. The percentage labeled cells for each injection group gives the group means + the standard deviation for the raw data and then were transferred to 10% neutral formalin until counts (percentage of labeled ceils to total cells in individual animals). they were embedded in paraffin, The brains of at least The standard deviations are typical of the variability seen throughout six animals from each injection group were blocked coro- data collection. The percentage cells originating column lists the data nally according to the stereotaxic angle of Pellegrino et that are presented in the bar graph (Fig. 3, bottom). To get the height aZ.‘s (33) atlas. Every 15th section (6 pm) through the of the bar on E15, for example, the proportion of labeled cells in injec- tion group E16-El7 (entry D, column 3) is subtracted from the propor- cerebral cortex was saved. The brains of some animals tion labeled cells in injection group E15-El6 (entry C, column 3) to in each injection group were also sectioned in the sagittal get the proportion of cells originating during the day on El5 (63.31%). plane (every 15th was saved) to examine the cortex in the vicinity of the frontal pole. Slides were coated with Kodak NTB-3 emulsion, exposed for 12 weeks, devel- ing nonmitotic neurons. By analyzing the rate of decline oped in Kodak D-19, and poststained with hematoxylin in labeled neurons, one can determine the proportion of and eosin. neurons originating over blocks of days (or single days) Coronal sections were selected for quantitative analy- during development. Table 1 shows the data and calcula- sis at nine anteroposterior levels (A9.2 to A1.2; draw- tions for the layer V cells in the perirhinal cortex at lev- ings, Fig. 3), and sagittal sections at 1.5 mm lateral to the els A4.2-Al.2 (bottom graph, Fig. 3). midline. Cells were counted microscopically at X312.5 in Throughout the quantitative analysis, it was noted unit areas set off by a 10 X 10 ocular grid (0.085 mm2 per that even slight trends in cell labeling within animals section). For quantification, all neurons within a desig- were very consistent. In the dorsal agranular insular cor- nated area were assigned to one of two groups, labeled or tex, for example, the layer VI cells at levels A8.2-A7.2 nonlabeled. Cells with silver grains overlying the nu- tended to have a lower percentage of labeled cells than cleus in densities above background levels were consid- those at level A9.2 during the peak period of neurogen- ered labeled. In our material, background noise is very esis. That indicates that at least some posterior cells low (approximately 2-4 grains per grid square), and a have birthdays earlier than those of anterior cells. Para- cluster of 6-12 silver grains over a nucleus (approxi- metric statistical tests, such as a nonnested analysis of mately 3X background) was enough to identify a labeled variance, look only at the degree of divergence between cell. However, due to the comprehensive labeling and the groups, and slight consistent differences within animals long exposure period, only a slight proportion of the neu- are disregarded.
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