What can volumes reveal about human brain evolution? A framework for bridging behavioral, histometric, and volumetric perspectives

Abstract

An overall relationship between brain size and cognitive ability exists across primates. Can more specific information about neural function be gleaned from cortical area volumes? Numerous studies have found significant relationships between brain structures and behaviors. However, few studies have speculated about brain structure-function relationships from the microanatomical to the macroanatomical level. Here we address this problem in comparative neuroanatomy, where the functional relevance of overall brain size and the sizes of cortical regions have been poorly understood, by considering comparative psychology, with measures of visual acuity and the perception of visual illusions. We outline a model where the macroscopic size (volume or surface area) of a cortical region (such as the primary visual cortex, V1) is related to the microstructure of discrete brain regions. The hypothesis developed here is that an absolutely larger V1 can process more information with greater fidelity due to having more neurons to represent a field of space. This is the first time that the necessary comparative neuroanatomical research at the microstructural level has been brought to bear on the issue. The evidence suggests that as the size of V1 increases: the number of neurons increases, the neuron density decreases, and the density of neuronal connections increases. Thus, we describe how information about gross neuromorphology, using V1 as a model for the study of other cortical areas, may permit interpretations of cortical function.

Keywords: brain evolution; brain volume; cognitive evolution; histology; illusions; primates; visual cortex.

Figure 1

Examples of four size illusions. The two horizontal lines are the same size in the Müller-Lyer and Ponzo illusions. The running person is the same size in each part of the corridor illusion. The central discs are the same size in the Ebbinghaus illusion.

Figure 2

Total number of V1 neurons increase as a function of V1 volume (r₂₈ = 0.95); the plot also provides the reduced major axis (RMA) regression of the base 10 logged species mean data (y = 1.073x + 5.134, R² = 0.899, p < 0.001). Total neuron number estimated from V1 layer II–VI neuron density times V1 volume in mm³ (gray matter only, Frahm et al., ; Bush and Allman, ; de Sousa et al., ; Lewitus et al., 2012b). (Note that because layer I was not included in the neuron density estimate, these should be considered to be overestimates of total V1 neuron number, but this overestimation is consistent for the whole sample). This figure also depicts visual illusion strength in the context of V1 volume and neuron numbers. Red shows the greatest size illusion experience, followed by orange, yellow, and green as the weakest size illusion experience; the size of the colored Müller-Lyer data points also corresponds to the size of the illusion experience (greater to weakest).

Figure 3

The size of the visual field represented by a neuron is inversely related to the size of the cortical region. A larger cortical area has more neurons, although neuronal soma size does not increase much. Modified from Elston et al. (1996).

Figure 4

Visual acuity increases as a function of V1 volume in both diurnal and nocturnal primates. Log-log (base 10) RMA plot of V1 volume (mm³, as above: Frahm et al., ; Bush and Allman, ; de Sousa et al., ; Lewitus et al., 2012b) as a function of visual acuity (y = 0.761x − 1.106, R² = 0.770, p < 0.001). The species' visual acuity was estimated based on the maximum visual acuity value (c/deg) out of all values listed for behavioral and anatomical visual acuity (Kirk and Kay, 2004).