Input timing for spatial processing is precisely tuned via constant synaptic delays and myelination patterns in the auditory brainstem

Precise timing of synaptic inputs is a fundamental principle of neural circuit processing. The temporal precision of postsynaptic input integration is known to vary with the computational requirements of a circuit, yet how the timing of action potentials is tuned presynaptically to match these proce...

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Bibliographic Details
Published in:Proceedings of the National Academy of Sciences - PNAS 2017-06, Vol.114 (24), p.E4851-E4858
Main Authors: Stange-Marten, Annette, Nabel, Alisha L., Sinclair, James L., Fischl, Matthew, Alexandrova, Olga, Wohlfrom, Hilde, Kopp-Scheinpflug, Conny, Pecka, Michael, Grothe, Benedikt
Format: Article
Language:English
Subjects:
Action potential
Adaptation
Animals
Auditory Pathways - physiology
Axons
Biological Sciences
Brain
Brain stem
Brain Stem - physiology
Circuits
Cochlear Nucleus - physiology
Cognition & reasoning
Computational neuroscience
Conduction
Female
Gerbillinae
Humans
Information processing
Integration
Invariants
Localization
Male
Mice
Mice, Inbred CBA
Myelin Sheath - physiology
Myelination
Neural Conduction - physiology
Optimization
PNAS Plus
Sound
Sound localization
Sound Localization - physiology
Spatial Processing - physiology
Structure-function relationships
Synaptic transmission
Synaptic Transmission - physiology
Time Factors
Time measurement
Trapezoid Body - physiology
Velocity
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Summary:Precise timing of synaptic inputs is a fundamental principle of neural circuit processing. The temporal precision of postsynaptic input integration is known to vary with the computational requirements of a circuit, yet how the timing of action potentials is tuned presynaptically to match these processing demands is not well understood. In particular, action potential timing is shaped by the axonal conduction velocity and the duration of synaptic transmission delays within a pathway. However, it is not known to what extent these factors are adapted to the functional constraints of the respective circuit. Here,we report the finding of activity-invariant synaptic transmission delays as a functional adaptation for input timing adjustment in a brainstem sound localization circuit. We compared axonal and synaptic properties of the same pathway between two species with dissimilar timing requirements (gerbil and mouse): In gerbils (like humans), neuronal processing of sound source location requires exceptionally high input precision in the range of microseconds, but not in mice. Activity-invariant synaptic transmission and conduction delays were present exclusively in fast conducting axons of gerbils that also exhibited unusual structural adaptations in axon myelination for increased conduction velocity. In contrast, synaptic transmission delays in mice varied depending on activity levels, and axonal myelination and conduction velocity exhibited no adaptations. Thus, the specializations in gerbils and their absence in mice suggest an optimization of axonal and synaptic properties to the specific demands of sound localization. These findings significantly advance our understanding of structural and functional adaptations for circuit processing.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.1702290114