Human Association Cortex: Expanded, Untethered, Neotenous, and Plastic

The expansion of distributed regions of association cortex over human development and evolution may confer different connectional tendencies to these zones relative to conserved primary sensory areas. Here, we review some of the core constraints that pattern mammalian neocortex and give rise to conserved properties of corticocortical connectivity. Beyond these conserved properties, primates and particularly humans have increased ipsilateral corticocortical connectivity that connects distributed regions of association cortex together. We offer a framework for thinking about how the massive scaling of the human neocortex may have untethered portions of cortex from evolutionarily conserved patterning centers that serve as anchors to the developing cortical plate. Activity-dependent input from the thalamus sculpts the connectional organization in primary sensory areas that then shapes properties of adjacent cortical regions. Association cortex may expand to fill regions interposed between areas patterned by sensory cascades. Absent the strong bottom-up anchor of sensory activity, association regions may be biased to connect to the other widely distributed association zones forming long-range networks. We discuss implications of this organization for cortical function as well as current gaps in our understanding of the developmental constraints that allow such an organization to emerge.