The significance of the subplate for evolution and developmental plasticity of the human brain

Abstract

The human life-history is characterized by long development and introduction of new developmental stages, such as childhood and adolescence. The developing brain had important role in these life-history changes because it is expensive tissue which uses up to 80% of resting metabolic rate (RMR) in the newborn and continues to use almost 50% of it during the first 5 postnatal years. Our hominid ancestors managed to lift-up metabolic constraints to increase in brain size by several interrelated ecological, behavioral and social adaptations, such as dietary change, invention of cooking, creation of family-bonded reproductive units, and life-history changes. This opened new vistas for the developing brain, because it became possible to metabolically support transient patterns of brain organization as well as developmental brain plasticity for much longer period and with much greater number of neurons and connectivity combinations in comparison to apes. This included the shaping of cortical connections through the interaction with infant's social environment, which probably enhanced typically human evolution of language, cognition and self-awareness. In this review, we propose that the transient subplate zone and its postnatal remnant (interstitial neurons of the gyral white matter) probably served as the main playground for evolution of these developmental shifts, and describe various features that makes human subplate uniquely positioned to have such a role in comparison with other primates.

Keywords: cerebral cortex; life-history; metabolic cost; neuron number; subplate zone.

Figure 1

Laminar development of human telencephalon from 10 postconceptional weeks (PCW) to newborn. The layers are transient and their appearance changes with changes in neurogenetic events. The subplate starts to develop around 13 PCW, reaches the peak of its development between 22 and 24 PCW, and starts to resolve around 34 PCW. In the newborn brain, the subplate remains during the first year, when the subplate disappears as a zone but its neurons become incorporated into the subcortical white matter as so-called interstitial neurons. cp, cortical plate; sp, subplate zone; iz, intermediate zone; svz, subventricular zone; vz, ventricular zone. Bar = 100 μm (A), 250 μm (B), 1 mm (C–E).

Figure 2

Lamination of frontal (A), mid-central (B) and occipital (C) region of human telencephalon at the peak of subplate development (22–24 PCW), as revealed by Nissl staining and acetylcholinesterase (AChE) histochemistry. At the peak of subplate development (22–24 PCW), subplate zone is the largest compartment of the human telencephalon. It is the place of intense synaptic activity and “waiting” compartment for the thalamocortical fibers (dark band below cp). Note that there are regional differences in the lamination between frontal and occipital region. cp, cortical plate; sp, subplate zone; iz, intermediate zone; svz, subventricular zone; vz, ventricular zone. Bar = 1 mm.

Figure 3

Although the resolution of the subplate zone starts after 34 PCW, the subplate remains visible as a major component of the telecephalic wall (asterisk in A,D). In the human telencephalon, cortico-cortical connections are still not developed (B) or myelinated (C) at 33 PCW, while at 40 PCW substantial development and myelination of cortico-cortical fiber can be observed (arrow in E,F). A–C 34 PCW, D–F 40 PCW.

Figure 4

Subplate and white matter interstitial neurons stained for NOS (NADPH-diaphorase-stained neurons in A–D), MAP2 (E,G) and NeuN (F) are visible throughout the subplate (A,B) and the white matter (C–G). Note that subplate/white matter interstitial neurons are numerous even after the first year of life, when subplate zone disappears. (A), 37 PCW; (B), 13 days; (C), 12 years; (D), 57 years; (E,G), 13 months; (F), 51 years. Bar = 1 mm.

Figure 5

Higher magnification view of subplate and white matter interstitial neurons displayed in panels A–F of the Figure 4 and stained for NOS (NADPH-diaphorase-stained neurons in A–D), MAP2 (E) and NeuN (F). Note that dendritic arborizations of subplate/interstitial neurons continue to grow and develop even after the disapearance of the subplate zone during the first year of life (compare (A and B with C). (A), 37 PCW; (B), 13 days; (C), 12 years; (D), 57 years; (E), 13 months; (F), 51 years. Bar = 0.5 mm.