Abstract
SummaryThe architecture of computational devices is shaped by their energy consumption. Energetic constraints are used to design silicon-based computers but are poorly understood for neural computation. In the brain, most energy is used to reverse ion influxes generating excitatory postsynaptic currents (EPSCs) and action potentials. Thus, EPSCs should be small to minimize energy use, but not so small as to impair information transmission. We quantified information flow through the retinothalamic synapse in the visual pathway in brain slices, with cortical and inhibitory input to the postsynaptic cell blocked. Altering EPSC size with dynamic clamp, we found that a larger-than-normal EPSC increased information flow through the synapse. Thus, the evolutionarily selected EPSC size does not maximize retinal information flow to the cortex. By assessing the energy used on postsynaptic ion pumping and action potentials, we show that, instead, the EPSC size optimizes the ratio of retinal information transmitted to energy consumed. These data suggest maximization of information transmission per energy used as a synaptic design principle.
Highlights
The geometry of excitatory synapses is subject to competing constraints
We studied the lateral geniculate nucleus relay synapse in the visual system to investigate whether postsynaptic currents are large, to transmit to the cortex as much as possible of the information arriving from the retina, or smaller, to save energy
The results presented below extend this concept to postsynaptic terminals, the largest consumers of energy in the brain, and are consistent with energy use profoundly constraining the operation of the CNS
Summary
The geometry of excitatory synapses is subject to competing constraints. Synapse diameter needs to be small, first so that a neuronal dendrite can receive a large number of synaptic inputs and second because if synapses are too large in diameter glutamate clearance by diffusion to surrounding astrocytes will be too slow, limiting the maximum rate of information transfer through the synapse [1]. If synapses are too small and possess only a few glutamate receptors, variability in the opening of postsynaptic ion channels creates noise in the postsynaptic signal [2, 3]. Because most brain energy is used to pump out ions that enter through postsynaptic receptors [4, 5], the number of receptors per synapse should be kept small to minimize energy use, but if it is too small, the postsynaptic effect of the input will be negligible. Analysis of the energetic cost of the postsynaptic ion pumping associated with synaptic signaling [6] revealed that synapse properties are evolutionarily selected to maximize the information transferred per energy used. Synapses do not maximize bits transmitted per second but bits transmitted per ATP molecule
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