Fossil skulls reveal that blood flow rate to the brain increased faster than brain volume during human evolution

Abstract

The evolution of human cognition has been inferred from anthropological discoveries and estimates of brain size from fossil skulls. A more direct measure of cognition would be cerebral metabolic rate, which is proportional to cerebral blood flow rate (perfusion). The hominin cerebrum is supplied almost exclusively by the internal carotid arteries. The sizes of the foramina that transmitted these vessels in life can be measured in hominin fossil skulls and used to calculate cerebral perfusion rate. Perfusion in 11 species of hominin ancestors, from Australopithecus to archaic Homo sapiens, increases disproportionately when scaled against brain volume (the allometric exponent is 1.41). The high exponent indicates an increase in the metabolic intensity of cerebral tissue in later Homo species, rather than remaining constant (1.0) as expected by a linear increase in neuron number, or decreasing according to Kleiber's Law (0.75). During 3 Myr of hominin evolution, cerebral tissue perfusion increased 1.7-fold, which, when multiplied by a 3.5-fold increase in brain size, indicates a 6.0-fold increase in total cerebral blood flow rate. This is probably associated with increased interneuron connectivity, synaptic activity and cognitive function, which all ultimately depend on cerebral metabolic rate.

Keywords: brain perfusion; cerebral cortex; cognition; evolution; hominin.

Figure 1.

Internal carotid foramina in selected hominin species: (a) Australopithecus africanus, (b) Homo neanderthalensis (cast) and (c) archaic Homo sapiens. All photographs are the same scale (increments in b and c are 0.5 mm) and thus illustrate the increase in foramen size across hominin evolution.

Figure 2.

Allometric relationships derived for the brains of 12 species of hominins: (a) mean endocranial volume (V_br) plotted against body mass (M_b), where $V_{\mathrm{br}}=37.9M_{\mathrm{b}}{\hspace{0.17em}}^{0.76}$. (b) Mean lumen radius (r) of internal carotid arteries in relation to endocranial volume (V_br), where $r=4.79\times {10}^{-3}\hspace{0.17em}{V}_{\mathrm{br}}{\hspace{0.17em}}^{0.52}$. (c) Cerebral blood flow rate (${\dot{Q}}_{\mathrm{ICA}}$), calculated from the size of the internal carotid foramina, in relation to endocranial volume (V_br), where $\dot{Q}{\hspace{0.17em}}_{\mathrm{ICA}}=2.10\times {10}^{-4}\hspace{0.17em}{V}_{\mathrm{br}}{\hspace{0.17em}}^{1.41}$. Allometric power regressions (solid curves) with 95% confidence bands (dashed curves) are presented on arithmetic axes, but were calculated on log-transformed data.

Figure 3.

Cerebral blood flow rate (${\dot{Q}}_{\mathrm{ICA}}$) in relation to estimated geological age (A) in 12 hominin species, where ${\dot{Q}}_{\mathrm{ICA}}=0.677A^2-3.69A+6.52$. Homo floresiensis is excluded from the regression.