1. Energy-efficient information transfer at thalamocortical synapses
- Author
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Harris, Julia Jade, Engl, Elisabeth, Attwell, David, and Jolivet, Renaud Blaise
- Subjects
Computer and Information Sciences ,Patch-Clamp Techniques ,QH301-705.5 ,Physiology ,Entropy ,Models, Neurological ,Information Theory ,Neurophysiology ,Action Potentials ,In Vitro Techniques ,Nervous System ,Membrane Potential ,Synaptic Transmission ,Rats, Sprague-Dawley ,Nerve Fibers ,Thalamus ,Animal Cells ,Medicine and Health Sciences ,Animals ,Computer Simulation ,Visual Pathways ,Biology (General) ,Visual Cortex ,Neurons ,Physics ,Biology and Life Sciences ,Computational Biology ,Excitatory Postsynaptic Potentials ,Cell Biology ,Neuronal Dendrites ,Axons ,Rats ,Electrophysiology ,Cellular Neuroscience ,Synapses ,Physical Sciences ,Thermodynamics ,Anatomy ,Cellular Types ,Energy Metabolism ,Information Entropy ,Research Article ,Neuroscience - Abstract
We have previously shown that the physiological size of postsynaptic currents maximises energy efficiency rather than information transfer across the retinothalamic relay synapse. Here, we investigate information transmission and postsynaptic energy use at the next synapse along the visual pathway: from relay neurons in the thalamus to spiny stellate cells in layer 4 of the primary visual cortex (L4SS). Using both multicompartment Hodgkin-Huxley-type simulations and electrophysiological recordings in rodent brain slices, we find that increasing or decreasing the postsynaptic conductance of the set of thalamocortical inputs to one L4SS cell decreases the energy efficiency of information transmission from a single thalamocortical input. This result is obtained in the presence of random background input to the L4SS cell from excitatory and inhibitory corticocortical connections, which were simulated (both excitatory and inhibitory) or injected experimentally using dynamic-clamp (excitatory only). Thus, energy efficiency is not a unique property of strong relay synapses: even at the relatively weak thalamocortical synapse, each of which contributes minimally to the output firing of the L4SS cell, evolutionarily-selected postsynaptic properties appear to maximise the information transmitted per energy used., Author summary Compared to other organs, the brain consumes a vast amount of energy for its size. Most of this energy is used to power the electrical and chemical processes that support neural computation. As the energy supply to the brain is limited, it follows that this computation should be energetically efficient. Previously, we showed that this is indeed the case for transmission of information between cells at synapses. Synapses transferring information from the retina to the brain do not maximise information transmission—some information is lost and does not reach the visual cortex. Instead, these synapses maximise the information transmitted per energy used. Here, we demonstrate that this principle of energetic efficiency also holds at the next synapse in the visual pathway, the thalamocortical synapse. This synapse is weaker and competes with hundreds of other inputs to influence the output firing of the next cell. Using detailed simulations of cortical neurons, and electrophysiological recordings in rodent brain slices, we found that this relatively weak synapse also does not maximise information transmission. Instead, it maximises the amount of information transmitted per energy used. This suggests that energy efficiency at synapses could be a common design principle in the brain.
- Published
- 2019