Patterns of Vertebrate Neurogenesis and the Paths of Vertebrate Evolution

Abstract

Any substantial change in brain size requires a change in the number of neurons and their supporting elements in the brain, which in turn requires an alteration in either the rate, or the duration of neurogenesis. The schedule of neurogenesis is surprisingly stable in mammalian brains, and increases in the duration of neurogenesis have predictable outcomes: late-generated structures become disproportionately large. The olfactory bulb and associated limbic structures may deviate in some species from this general brain enlargement: in the rhesus monkey, reduction of limbic system size appears to be produced by an advance in the onset of terminal neurogenesis in limbic system structures. Not only neurogenesis but also many other features of neural maturation such as process extension and retraction, follow the same schedule with the same predictability. Although the underlying order of event onset remains the same for all of the mammals we have yet studied, changes in overall rate of neural maturation distinguish related subclasses, such as marsupial and placental mammals, and changes in duration of neurodevelopment distinguish species within subclasses. A substantial part of the regularity of event sequence in neurogenesis can be related directly to the two dimensions of the neuraxis in a recently proposed prosomeric segmentation of the forebrain [Rubenstein et al., Science, 266: 578, 1994]. Both the spatial and temporal organization of development have been highly conserved in mammalian brain evolution, showing strong constraint on the types of brain adaptations possible. The neural mechanisms for integrative behaviors may become localized to those locations that have enough plasticity in neuron number to support them.

Extrapolating brain development from experimental species to humans

“…Rodent/primate comparisons raise a question about the presumption of comparable rates of development across all regions of the brain. The premise that brain regions develop at similar rates across species does not take into account disparities in relative sizes of mature primate limbic and cortical regions which indicate that these regions develop on a somewhat different timetable in primates, as discussed below Finlay et al, 1998;West, 1990).…”

“…Although the authors make no attempt to directly translate development across species, this study is an example of the manner with which the conservation of developmental sequences across species is presumed -the human study simply makes use of non-human data to "fill in" gaps. This assumption is possible because close similarities in the manner in which mammalian brains develop are well documented (Finlay and Darlington, 1995;Finlay et al, 2001;Finlay et al, 1998;Striedter, 1999;Striedter, 2005) and, when properly considered, can be used to equate developmental time across mammalian species with confidence (Clancy, 2006;Clancy et al, 2000;Clancy et al, 2001;Clancy et al, 2006;Verley, 1977). Some studies have been directly prompted by evolution-based questions.…”

Mapping behavioural evolution onto brain evolution: the strategic roles of conserved organization in individuals and species

“…Furthermore, the duration of neurogenesis maps onto an axis in the conserved embryonic brain plan in vertebrates such that the medially located, 'basal' cell groups in brain segments ('segments' here are spinal cord segments, rhombomeres and prosomeres) cease precursor generation early. Laterally located, 'alar' groups stop last, or in the case of hippocampus and olfactory bulb continue into adulthood [38].…”

“…Changes in the duration of growth (of genetic, but possibly environmental origin as well) do not produce isometric changes in all brain parts, but allocate volume changes preferentially to the structures produced over the longest embryonic duration. In neural development, the basal-to-alar axis of repeating brain segments (the embryonic medial-to-lateral direction) is the axis in which increasing duration of neurogenesis is roughly represented [35,38]. While this conserved axis could be argued to be a 'developmental constraint' on brain structure, we have presented arguments here that a brain axis in which duration of neuron production systematically varies may be essential to a useful brain architecture, one that scales gracefully and is robust to damage.…”

Humanity from African Naissance to Coming Millennia

“…There are some examples of disproportionate growth of specific brain structures, which can be related to active growth (Pirlot, 1987;Stephan et al, 1991;Barton et al, 1995;Aboitiz, 1996; Rilling & Insell, 1998: Barton, 1998). However, in many cases the observed species differences in relative size of the distinct brain parts are not too dramatic, and some methodological problems in statistics have been claimed (for details, see Finlay et al, 1998). Further studies are needed to determine more precisely to what extent and in which instances the distinct brain parts may grow independently of one another if they do.…”