Invariant Synapse Density and Neuronal Connectivity Scaling in Primate Neocortical Evolution

Author:

Sherwood Chet C1,Miller Sarah B2,Karl Molly1,Stimpson Cheryl D1,Phillips Kimberley A3,Jacobs Bob4,Hof Patrick R5,Raghanti Mary Ann6,Smaers Jeroen B78

Affiliation:

1. Department of Anthropology, Center for the Advanced Study of Human Paleobiology, The George Washington University, Washington, DC 20052, USA

2. Department of Psychological and Brain Sciences, Dartmouth College, Hanover, NH 03755, USA

3. Department of Psychology, Trinity University, San Antonio, TX 78212, USA

4. Department of Psychology, Laboratory of Quantitative Neuromorphology, Colorado College, Colorado Springs, CO 80946, USA

5. Nash Family Department of Neuroscience, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA

6. Department of Anthropology, School of Biomedical Sciences, Brain Health Research Institute, Kent State University, Kent, OH 44242, USA

7. Department of Anthropology, Stony Brook University, Stony Brook, NY 11794, USA

8. Division of Anthropology, American Museum of Natural History, New York, NY 10024, USA

Abstract

Abstract Synapses are involved in the communication of information from one neuron to another. However, a systematic analysis of synapse density in the neocortex from a diversity of species is lacking, limiting what can be understood about the evolution of this fundamental aspect of brain structure. To address this, we quantified synapse density in supragranular layers II–III and infragranular layers V–VI from primary visual cortex and inferior temporal cortex in a sample of 25 species of primates, including humans. We found that synapse densities were relatively constant across these levels of the cortical visual processing hierarchy and did not significantly differ with brain mass, varying by only 1.9-fold across species. We also found that neuron densities decreased in relation to brain enlargement. Consequently, these data show that the number of synapses per neuron significantly rises as a function of brain expansion in these neocortical areas of primates. Humans displayed the highest number of synapses per neuron, but these values were generally within expectations based on brain size. The metabolic and biophysical constraints that regulate uniformity of synapse density, therefore, likely underlie a key principle of neuronal connectivity scaling in primate neocortical evolution.

Funder

NSF INSPIRE

James S. McDonnell Foundation

Publisher

Oxford University Press (OUP)

Subject

Cellular and Molecular Neuroscience,Cognitive Neuroscience

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