The time of origin of neurons in the hippocampal region of the rhesus monkey

Abstract

The time of origin of neurons in the hippocampal region was determined in a series of rhesus monkeys, each of which had been exposed to a pulse of tritiated thymidine (3H-TdR) at a different time during ontogeny and sacrificed between the second and fifth month after birth. No heavily labeled cells were found in the hippocampal region of animals exposed to 3H-TdR before embryonic day 33 (E33). Exposure to 3H-TdR given at E36 labels a few neurons in the deepest layers of the entorhinal area, and 3H-TdR given at E38 labels a small number of neurons in all hippocampal subdivisions. Although the first neurons are generated almost simultaneously throughout the hippocampal region, the proliferation ceases at a different time in each subdivision. The last neurons destined for the entorhinal area and presubiculum are generated between E70 and E75, whereas the last parasubicular neurons are generated between E75 and E80. The production of neurons that form the subiculum ends about two weeks earlier, between E56 and E65. Within the hippocampus, genesis of pyramidal cells ends between E70 and E80 in area CA1, between E56 and E65 in area CA2, between E65 and E80 in area CA1, between E56 and E65 in area CA2, between E65 and E70 in area CA3, and between E75 and E80 in area CA4. In contrast, the genesis of granule cells of the fascia dentata is considerably prolonged. It continues throughout the second half of gestation, declines steadily in the course of the first postnatal month, and tapers off during the next 2 months. There is a distinct inside-to-outside spatiotemporal gradient in the parahippocampal formation and in the stratum pyramidale of both the subiculum and hippocampus. In contrast, the spatiotemporal pattern of granule cell origin in the dentate gyrus is outside-to-inside. Furthermore, granule cells generated between E36 and E80 are distributed in a distinct suprapyramidal-to-infrapyramidal gradient, whereas those generated at later ages are distributed evenly throughout the fascia dentata. Correlation of the present findings with histological data on hippocampal neurogenesis in the human brain demonstrates that the timing and sequence of developmental events as well as spatiotemporal gradients are similar in both primate species.

SLC25A12 expression is associated with neurite outgrowth and is upregulated in the prefrontal cortex of autistic subjects

“…The hippocampus matures postnatally in rodents, whereas it develops prenatally in primates. [38][39][40] We observed Slc25a12 expression in postnatal mouse hippocampus (P21), whereas the Slc25a12 transcript was not detected in the 23 weeks human hippocampus (Supplementary Figure S5b), consistent with the relative developmental periods. In addition, no molecular gradient of Slc25a12 expression was observed in the mouse brain.…”

Neonatal Nonhandling andIn UteroPrenatal Stress Reduce the Density of NADPH-Diaphorase-Reactive Neurons in the Fascia Dentata and Ammon’s Horn of Rats

“…This has been observed in various species (mouse: Angevine, 1965; monkey: Rakic and Nowakowski, 1981;rat: Altman and Das, 1965;cat: Purpura and Pappas, 1968), including human. On the basis of their analysis of the Yakovlev collection, Kretschmann et al (1986) concluded that the maximum rate of growth of the human hippocampal formation occurs at approximately 2 months postnatally.…”

Translating developmental time across mammalian species

“…For example, ideally we would assign`starts',`peaks' and`ends' for neurogenesis dates that are consistent across studies. However, while some investigators publish histograms for which we can use consistent numerical criteria (Rakic, 1977;Bayer, 1980;Rakic and Nowakowski, 1981;Bayer andAltman, 1987, 1990), others report only onset or o¡set of neurogenesis, that is, the ¢rst or last day any neurons were generated (Robinson and Dreher, 1990). When possible, we counted as`start' the day on which 5% of the neurons of a given structure were generated, and`end' similarly, but this criterion is impossible to apply uniformly without some loss of data.…”

“…The nature of ¢ber tract data derived from human embryos and fetuses would suggest that observational error, rather than`real' variability, could account for the larger error of estimate. A crown to rump length is often used to`age' a human fetus, but this measurement can be confusing between studies (Humphrey, 1968;Rakic and Yakovlev, 1968) and variable even within studies (Rakic and Yakovlev, 1968). The`delay' factor is likely to be unusually large for human observations, as intervals between ages used in an individual developmental study may be relatively large (Hewitt, 1961;Zilles et al, 1986;Mojsilovic and Zecevic, 1991;Arnold and Trojanowski, 1996).…”