Abstract

Most organisms suffer neuronal damage throughout their lives, which can impair performance of core behaviors. Their neural circuits need to maintain function despite injury, which in particular requires preserving key system outputs. In this work, we explore whether and how certain structural and functional neuronal network motifs act as injury mitigation mechanisms. Specifically, we examine how (i) Hebbian learning, (ii) high levels of noise, and (iii) parallel inhibitory and excitatory connections contribute to the robustness of the olfactory system in the Manduca sexta moth. We simulate injuries on a detailed computational model of the moth olfactory network calibrated to data. The injuries are modeled on focal axonal swellings, a ubiquitous form of axonal pathology observed in traumatic brain injuries and other brain disorders. Axonal swellings effectively compromise spike train propagation along the axon, reducing the effective neural firing rate delivered to downstream neurons. All three of the network motifs examined significantly mitigate the effects of injury on readout neurons, either by reducing injury’s impact on readout neuron responses or by restoring these responses to pre-injury levels. These motifs may thus be partially explained by their value as adaptive mechanisms to minimize the functional effects of neural injury. More generally, robustness to injury is a vital design principle to consider when analyzing neural systems.

Highlights

  • Injuries are inevitable for most organisms, yet maintaining a satisfactory level of functionality can be decisive for their survival

  • (i) The antennae comprise the outermost region of the olfactory system and are arguably the most exposed to external environmental shocks

  • We note that the hundreds of Receptor Neuron (RN) responsive to a given odor are spread throughout the antennae, ensuring that localized damage to an antenna does not disproportionately reduce the response to a particular odor

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Summary

Introduction

Injuries are inevitable for most organisms, yet maintaining a satisfactory level of functionality can be decisive for their survival. The progressive wear of a honeybee’s wings, for example, challenges the insect to sustain its load lift or face less nourishing foraging trips [1,2]. Functional robustness is desirable for neural systems as well. While computer devices operate in a regime of near-zero tolerance for physical damage, the middle-aged human brain undergoes significant neuronal losses on a daily basis [3]. Robustness to injury is often overlooked when analyzing the purpose and function of neural structures while the transmission of maximum information, high signal-to-noise ratio, and low energy consumption are primarily considered [4]. Analyzing neural information processing in the context of these principles is certainly important, but arguably incomplete

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