Combining diffusion magnetic resonance tractography with stereology highlights increased cross‐cortical integration in primates

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Primates possess an expanded isocortex and more isocortical neurons compared with many other mammals, but the implications for cortical structure, connectivity patterns, and function remain poorly understood (Finlay and Darlington, 1995; Barton and Harvey, 2000; Herculano‐Houzel, 2012). How connectivity patterns and cross‐cortical integration evolved with the expansion of the primate isocortex is a fundamental question in evolutionary neuroscience.
Across the depth of the isocortex, neurons exhibit stereotypical and conserved projection patterns (Gilbert et al., 1975; Barbas, 1986; Nudo and Masterton, 1990). Generally, upper‐layer neurons (i.e., layers II–IV) form connections with other cortical neurons. Many lower‐layer pyramidal neurons (i.e., layers V–VI) form connections with subcortical structures (Gilbert et al., 1975; Barbas, 1986; Nudo and Masterton, 1990), and some lower‐layer neurons project cross‐cortically (Kennedy and Bullier 1985; Callaway, 1998; Sincich et al., 2010). Layer IV neurons are locally projecting, whereas layer III pyramidal neuron preferentially project over longer distances. Given that neurons generally exhibit conserved stereotypical patterns of projections, a greater number of upper‐layer neurons would suggest increased cross‐cortical integration.
Comparing connectivity patterns between species has traditionally been challenging because differences arising from noninvasive methods (e.g., diffusion MR imaging) can be difficult to interpret (Jones et al., 2013) and tract‐tracing methods can be problematic for quantitative comparison across species (Nudo and Masterton, 1990). For these reasons, the present study combines stereological counts of neuron numbers across cortical layers with comparative analyses of diffusion MRI tractography to assess whether primates exhibit evidence of increased intracortical connectivity relative to other mammals.
For the present study, we collected data on upper‐layer (i.e., layers II–IV) and lower‐layer (i.e., layers V–VI) neuron numbers of primate and nonprimate species. Many layer IV neurons project locally, whereas many layer II–III neurons form synapses with other cortical neurons. A comparative analysis of layer II–IV neuron numbers yields insights into evolutionary changes in cortical neuron numbers that modulate incoming (e.g., thalamocortical input) and cross‐cortical information (Frost and Caviness, 1980). We also assessed evolutionary changes in long‐range cross‐cortical connectivity patterns between primate and nonprimate species with the use of high‐angular resolution diffusion and diffusion spectrum MR tractography. Our analyses show that primates possess disproportionately more isocortical neurons, more upper‐layer neurons, and increased long‐range‐projecting intracortical tracts coursing across the anterior–posterior axis compared with other mammals. Collectively, these findings demonstrate that primates show evidence of increased cross‐cortical integration relative to the other mammals studied.

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