Local design principles at hippocampal synapses revealed by an energy-information trade-off

Abstract

Synapses across different brain regions display distinct structure-function relationships. We investigate the interplay of fundamental design principles that shape the transmission properties of the excitatory CA3-CA1 pyramidal cell connection, a prototypic synapse for studying the mechanisms of learning in the hippocampus.This small synapse is characterized by probabilistic release of transmitter, which is markedly facilitated in response to naturally occurring trains of action potentials. Based on a physiologically realistic computational model of the CA3 presynaptic terminal, we show how unreliability and short-term dynamics of vesicle release work together to regulate the trade-off of information transfer versus energy use. We propose that individual CA3-CA1 synapses are designed to operate at close to maximum possible capacity of information transfer in an efficient manner. Experimental measurements reveal a wide range of vesicle release probabilities at hippocampal synapses, which may be a necessary consequence of long-term plasticity and homeostatic mechanisms that manifest as presynaptic modifications of release probability. We show that the timescales and magnitude of short-term plasticity render synaptic information transfer nearly independent of differences in release probability. Thus, individual synapses transmit optimally while maintaining a heterogeneous distribution of presynaptic strengths indicative of synaptically-encoded memory representations. Our results support the view that organizing principles that are evident on higher scales of neural organization percolate down to the design of an individual synapse.in the freely-moving rat. Brain Res 34, 171 (1971). 26 J. E. Lisman, Bursts as a unit of neural information: making unreliable synapses reliable, Trends in neurosciences 20, 38 (1997).

Comparative performance of mutual information and transfer entropy for analyzing the balance of information flow and energy consumption at synapses

“…to be designed to maximize information flow per energy units (bits/ATP) rather than per time units (bits/sec). More recently, similar results have also been obtained at hippocampal synapses [13].…”

“…Figure 5 shows that when systematic frame shifts occur between input and output sequences, i.e. when the 13 input and output action potentials do not happen in matching time bins due to transmission delays or due to the integrative properties of the neuron under consideration, the use of TE requires a more careful examination of the detailed biophysics at play. It also becomes difficult to directly compare results obtained with I and TE.…”

“…We have recently published a series of experimental and computational works on the tradeoff between information flow and concomitant energy consumption in neurons and neural networks, in which we used either I [7][8][9] or TE [10]. This work is part of an emergent interest for energetic questions in neural information processing [13][14][15][16]. Here, we proceed to a systematic comparison of both those quantities in different biologically-relevant scenarios when comparing inputs to a synapse and the output spike train generated by the postsynaptic neuron in response, using spike train data generated from Poisson processes, or an experimentally-calibrated biophysical model of thalamic relay cells of the Hodgkin-Huxley-type [8].…”