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The Journal of Neuroscience, June 17, 2009, 29(24):7917-7928; doi:10.1523/JNEUROSCI.5200-08.2009

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Behavioral/Systems/Cognitive
How the Optic Nerve Allocates Space, Energy Capacity, and Information

János A. Perge,¹ Kristin Koch,¹ Robert Miller,³ Peter Sterling,¹ and Vijay Balasubramanian²

Departments of ¹Neuroscience and ²Physics, University of Pennsylvania, Philadelphia, Pennsylvania 19104, and ³Department of Neuroscience, University of Minnesota, Minneapolis, Minnesota 55455

Correspondence should be addressed to János A. Perge at the above address. Email: jperge{at}gmail.com

Fiber tracts should use space and energy efficiently, because both resources constrain neural computation. We found for a myelinated tract (optic nerve) that astrocytes use nearly 30% of the space and >70% of the mitochondria, establishing the significance of astrocytes for the brain's space and energy budgets. Axons are mostly thin with a skewed distribution peaking at 0.7 µm, near the lower limit set by channel noise. This distribution is matched closely by the distribution of mean firing rates measured under naturalistic conditions, suggesting that firing rate increases proportionally with axon diameter. In axons thicker than 0.7 µm, mitochondria occupy a constant fraction of axonal volume—thus, mitochondrial volumes rise as the diameter squared. These results imply a law of diminishing returns: twice the information rate requires more than twice the space and energy capacity. We conclude that the optic nerve conserves space and energy by sending most information at low rates over fine axons with small terminal arbors and sending some information at higher rates over thicker axons with larger terminal arbors but only where more bits per second are needed for a specific purpose. Thicker axons seem to be needed, not for their greater conduction velocity (nor other intrinsic electrophysiological purpose), but instead to support larger terminal arbors and more active zones that transfer information synaptically at higher rates.

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Received Oct. 27, 2008; revised May 7, 2009; accepted May 12, 2009.

Correspondence should be addressed to János A. Perge at the above address. Email: jperge{at}gmail.com

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