Wiring Economy of Pyramidal Cells in the Juvenile Rat Somatosensory Cortex

• Published in: PloS one Vol. 11; no. 11; p. e0165915
• Main Authors: Anton-Sanchez, Laura, Bielza, Concha, Larrañaga, Pedro, DeFelipe, Javier
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 10.11.2016; Public Library of Science (PLoS)
• Subjects: Animals; Bifurcations; Biology; Biology and Life Sciences; Brain; Brain architecture; Cerebral cortex; Computer Simulation; Cortex (somatosensory); Dendrites - physiology; Dendritic branching; Dendritic structure; Economic aspects; Evolution; Evolutionary computation; Genetic algorithms; Graph theory; Models, Neurological; Morphology; Nerve Net - cytology; Nerve Net - physiology; Neural networks; Neurons; Neurosciences; Optimization; Physical Sciences; Pyramidal cells; Pyramidal Cells - cytology; Pyramidal Cells - physiology; Rats; Rats, Wistar; Research and Analysis Methods; Rodents; Somatosensory Cortex - anatomy & histology; Somatosensory Cortex - physiology; Studies; Wiring; Spain
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0165915

Ever since Cajal hypothesized that the structure of neurons is designed in such a way as to save space, time and matter, numerous researchers have analyzed wiring properties at different scales of brain organization. Here we test the hypothesis that individual pyramidal cells, the most abundant type of neuron in the cerebral cortex, optimize brain connectivity in terms of wiring length. In this study, we analyze the neuronal wiring of complete basal arborizations of pyramidal neurons in layer II, III, IV, Va, Vb and VI of the hindlimb somatosensory cortical region of postnatal day 14 rats. For each cell, we search for the optimal basal arborization and compare its length with the length of the real dendritic structure. Here the optimal arborization is defined as the arborization that has the shortest total wiring length provided that all neuron bifurcations are respected and the extent of the dendritic arborizations remain unchanged. We use graph theory and evolutionary computation techniques to search for the minimal wiring arborizations. Despite morphological differences between pyramidal neurons located in different cortical layers, we found that the neuronal wiring is near-optimal in all cases (the biggest difference between the shortest synthetic wiring found for a dendritic arborization and the length of its real wiring was less than 5%). We found, however, that the real neuronal wiring was significantly closer to the best solution found in layers II, III and IV. Our studies show that the wiring economy of cortical neurons is related not to the type of neurons or their morphological complexities but to general wiring economy principles.