Abstract

Artificial feedforward neural networks perform a wide variety of classification and function approximation tasks with high accuracy. Unlike their artificial counterparts, biological neural networks require a supply of adequate energy delivered to single neurons by a network of cerebral microvessels. Since energy is a limited resource, a natural question is whether the cerebrovascular network is capable of ensuring maximum performance of the neural network while consuming minimum energy? Should the cerebrovascular network also be trained, along with the neural network, to achieve such an optimum? In order to answer the above questions in a simplified modeling setting, we constructed an Artificial Neurovascular Network (ANVN) comprising a multilayered perceptron (MLP) connected to a vascular tree structure. The root node of the vascular tree structure is connected to an energy source, and the terminal nodes of the vascular tree supply energy to the hidden neurons of the MLP. The energy delivered by the terminal vascular nodes to the hidden neurons determines the biases of the hidden neurons. The “weights” on the branches of the vascular tree depict the energy distribution from the parent node to the child nodes. The vascular weights are updated by a kind of “backpropagation” of the energy demand error generated by the hidden neurons. We observed that higher performance was achieved at lower energy levels when the vascular network was also trained along with the neural network. This indicates that the vascular network needs to be trained to ensure efficient neural performance. We observed that below a certain network size, the energetic dynamics of the network in the per capita energy consumption vs. classification accuracy space approaches a fixed-point attractor for various initial conditions. Once the number of hidden neurons increases beyond a threshold, the fixed point appears to vanish, giving place to a line of attractors. The model also showed that when there is a limited resource, the energy consumption of neurons is strongly correlated to their individual contribution to the network’s performance.

Highlights

  • Energy constraints are believed to play a vital role in shaping the evolution of the b­ rain[1,2]

  • One widely accepted theory is that the glucose transported to the neurons are picked up directly by neurons and used as a substrate to carry out oxidative phosphorylation, which is the major contributor of Adenosine TriPhosphate (ATP), the energy currency used to fuel the action of ionic p­ umps[12,13,14]

  • Astrocytes convert the glucose released from the cerebral vessels to lactate and provide it to the neurons, where it is converted into pyruvate and into ATP

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Summary

Introduction

Energy constraints are believed to play a vital role in shaping the evolution of the b­ rain[1,2]. One widely accepted theory is that the glucose transported to the neurons are picked up directly by neurons and used as a substrate to carry out oxidative phosphorylation, which is the major contributor of ATP, the energy currency used to fuel the action of ionic p­ umps[12,13,14]. Another exciting study still d­ ebated[15,16,17,18,19] is the astrocyte-neuron lactate shuttle ­theory[20], which posits an important role to astrocyte in mediating neurovascular coupling. If the models of neuroenergetics at the single-unit level are so complicated, it would not be a pragmatic enterprise to extend them as they are to a network level and study neuroenergetics in an extremely detailed fashion at a network level

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