Cross-species analyses of the cortical GABAergic and subplate neural populations

Abstract

Cortical GABAergic (gamma-aminobutyric acidergic) neurons include a recently identified subset whose projections extend over relatively long distances in adult rodents and primates. A number of these inhibitory projection neurons are located in and above the conventionally identified white matter, suggesting their persistence from, or a correspondence with, the developmental subplate. GABAergic and subplate neurons share some unique properties unlike those of the more prevalent pyramidal neurons. To better understand the GABAergic and subplate populations, we constructed a database of neural developmental events common to the three species most frequently used in experimental studies: rat, mouse, and macaque, using data from the online database www.translatingtime.net as well as GABAergic and subplate developmental data from the empirical literature. We used a general linear model to test for similarities and differences, a valid approach because the sequence of most neurodevelopmental events is remarkably conserved across mammalian species. Similarities between the two rodent populations are striking, permitting us to identify developmental dates for GABAergic and subplate neural events in rats that were previously identified only in mice, as well as the timing in mouse development for events previously identified in rats. Primate comparative data are also compelling, although slight variability in statistical error measurement indicates differences in primate GABAergic and subplate events when compared to rodents. Although human extrapolations are challenging because fewer empirical data points are available, and because human data display more variability, we also produce estimates of dates for GABAergic and subplate neural events that have not yet been, or cannot be, determined empirically in humans.

Keywords: GABA; cross-species correlations; human development; layer VIb; persisting subplate neurons; rodent development; statistical analysis; white matter neurons.

Figure 1

(A) Schematic of a dorsal view of an adult rat brain produced from serial sections using Neurolucida (Version 8; MicroBrightField, Williston, VT, USA). Persisting subplate cells (blue) lie above the white matter (solid white). The brain outline is depicted in shadow. (B) The same brain with the infracortical stria, a fiber tract above the persisting subplate cells, shown in transparent white. The white, dashed line represents the continuity, but decreasing thickness, of the infracortical stria in posterior brain regions. (C) Overlapping coronal serial sections depicting the location of the persisting subplate cells (blue) with the conventional white matter outlined (white). Scale bar = approximately 1.0 mm. Abbreviations: ant (anterior); post (posterior).

Figure 2

The predicted (black) and empirical values (red) of the post-conceptional days in the log-scale, i. e. log(PC days), of the 38 common events excluding GABAergic and subplate events across mice, rats and macaques are shown in (A), (B) and (C) respectively. The rat and macaque events are in the same chronological order as that of mouse events. The confidence limits (log-scale) about the predicted values and the sum of absolute error (e) between the empirical and the predicted values are also shown in (A), (B) and (C). The correlation coefficient (r) between the predicted and the empirical values for mice, rats and macaques are shown in (D), (E) and (F) respectively. The names of the events are included in Table 2 at the end of this review.

Figure 3

The predicted (black) and empirical values (red) of the post-conceptional days in the log-scale, i. e. log(PC days), of the 46 common events including GABAergic and subplate events across mice, rats and macaques are shown in (A), (B) and (C) respectively. The rat and macaque events are in the same chronological order as the mouse events. The confidence limits (log-scale) for the predicted values and the sum of absolute error (e) between the empirical and the predicted values are also shown in (A), (B) and (C). The correlation coefficient (r) between the predicted and the empirical values for mice, rats and macaques are shown in (D), (E) and (F) respectively. The specific events are included in Table 3 at the end of this review.