Elsevier

Current Opinion in Neurobiology

Volume 41, December 2016, Pages 62-67
Current Opinion in Neurobiology

Consequences of degeneracy in network function

https://doi.org/10.1016/j.conb.2016.07.008Get rights and content

Highlights

  • More than one set of circuit parameters can produce the same network output.

  • Degeneracy is likely to make network function more robust.

  • Network degeneracy may enable the encoding of latent memories.

  • Network degeneracy may promote the ability of a network to task switch.

Often distinct elements serve similar functions within a network. However, it is unclear whether this network degeneracy is beneficial, or merely a reflection of tighter regulation of overall network performance relative to individual neuronal properties. We review circumstances where data strongly suggest that degeneracy is beneficial in that it makes network function more robust. Importantly, network degeneracy is likely to have functional consequences that are not widely appreciated. This is likely to be true when network activity is configured by modulators with persistent actions, and the history of network activity potentially impacts subsequent functioning. Data suggest that degeneracy in this context may be important for the creation of latent memories, and for state-dependent task switching.

Introduction

Biological ‘degeneracy’ is defined as the ability of elements that are structurally distinct to fulfill the same function, for example, some amino acids are specified by more than one nucleotide combination [1]. This review focuses on degeneracy at a different level, that is, at the level of a neural network. Neural networks are characterized by a set of parameters that describe the intrinsic properties of the component neurons, and the synapses that they make [2]. Degeneracy is observed when more than one set of circuit parameters produces the same (or very similar) output.

Network degeneracy has been described in a number of systems leading to speculation as to why it is observed. It could be beneficial for an organism. Alternatively it could simply reflect the need for tight regulation of network performance without a similar need to restrict specific circuit parameters. We discuss research that strongly argues that network degeneracy makes circuit function more robust. Further, we suggest that network degeneracy can have other functional consequences. We focus on situations in which network activity is configured by persistent effects of neuromodulators, and mechanisms utilized to pattern one bout of activity impact subsequent network activation.

Section snippets

Variability in membrane and synaptic currents

The potential for degeneracy in network function was strikingly illustrated in a computational study that simulated more than 20 million versions of a relatively simple, triphasic motor program generated by the crustacean stomatogastric nervous system [3]. This study clearly demonstrated that virtually indistinguishable activity patterns could arise from widely disparate sets of circuit parameters.

To determine whether degeneracy is observed in biological systems, investigators have measured

Stabilizing effects of conductance correlations

Interestingly, however, a number of studies have demonstrated that this variability can be constrained in that certain circuit parameters co-vary. Namely, the expression levels of different ion channels can be linearly correlated with one another [10, 11, 12]. For example, Schulz et al. [10] measured mRNA expression of the ion channels in each cell type in the crab stomatogastric ganglion (STG) and observed correlations in most neurons, which could be pairwise, three-way or even four-way.

Degeneracy and robustness in behavior

Although a large body of work has demonstrated that degeneracy in ionic conductances can stabilize network activity, much less is known about how this impacts behavior. What is known is primarily a result of research conducted in Caenorhabditis elegans. For instance, C. elegans thermoregulate by modifying navigation, that is, an animal that encounters a temperature higher than its cultivation temperature displays negative thermotaxis [26]. Cell ablation and rescue experiments have demonstrated

Network degeneracy and experience dependent plasticity

In addition to permitting vital behavior under a variety of conditions, degeneracy in network function has been described in other contexts [33, 34•, 35, 36, 37, 38••]. For example, surprising variability in network composition has been reported in large-scale voltage sensitive dye (VSD) imaging experiments monitoring the activity of neural networks mediating highly stereotypic behaviors in molluscs [35, 36, 37, 38••]. Even for a behavior as stereotyped as escape swimming in Tritonia, the

Conclusions

Although a priori it cannot be assumed that degeneracy in network function creates a physiological advantage, data are emerging that suggest that in many cases it does. It is likely that it makes behavior more robust. Further, data suggest that it may be important for the induction of latent memories, and that it may create the potential for increased behavioral flexibility by impacting the dynamics of task switching.

Conflict of interest

Nothing declared.

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

Supported by NIH grants NS066587, NS070583 and R03DC013997.

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