Robust circuit rhythms in small circuits arise from variable circuit components and mechanisms
Introduction
The central pattern generating circuits found in invertebrates have been the source of numerous fundamental insights into the generation of rhythmic motor patterns, brain oscillations [1, 2, 3, 4] and some of the synaptic mechanisms that control oscillator precision [5]. Computational and experimental studies have demonstrated that some individual neurons can generate bursts of action potentials that can drive circuit oscillations (Figure 1). In other cases, circuit oscillations arise as a consequence of synaptic connections among neurons that are themselves not bursting neurons [6, 7, 8] (Figure 1).
A wealth of data has shown that neuromodulators and modulatory neurons can reconfigure oscillatory networks, changing their frequency, phase relationships, and the functional interactions among neurons [9•, 10, 11•, 12, 13•]. Notably, neurons can switch among different rhythms, and the same neuron can be part of oscillatory circuits with very different cycle periods [14, 15, 16, 17, 18].
A more recent body of work on small rhythmic circuits has shown that circuit parameters, such as ion channel densities or synaptic strengths, can be widely variable across animals in the population yet still produce rhythmic motor patterns that are normal, or ‘good enough’ [19, 20, 21, 22•, 23••, 24, 25••, 26•]. In this review, we focus on recent work that illuminates the issues raised by variability in system components for robust rhythm generation.
Section snippets
Variability in system components across animals
Many small central pattern generating circuits have been studied for more than 40 years. This means that data have been collected from the same identified neurons and synapses over extended periods of time, without the confounds that arise when experimentalists are sampling neurons from a large population of unidentified or poorly identified neurons. Consequently, it is not an accident that work on identified neurons has generated much of what we know about animal-to-animal variability of
Variability in circuit structure revealed by perturbations
If, as now seems to be the case, each crab or leech or snail, has found through development and experience, a set of membrane and synaptic conductances that are sufficient for behavior, the question then becomes how consistently can animals with these potentially quite disparate solutions to circuit performance respond appropriately to the neuromodulation and environmental perturbations that they will routinely experience? This is a telling question, as it is certainly the case that there must
Neuromodulation can reveal variability or diminish its impact
Neuromodulators can alter the output of oscillatory circuits and motor patterns in numerous ways [11•]. Most members of a population of networks with different underlying structure can respond reliably to modulators, although individuals may respond differently from the mean [7]. There are many examples of state-dependent neuromodulation that depend on history [55] or initial conditions [56, 57]. There are also examples of neuromodulators that produce what appear to be paradoxical and opposing
Degeneracy in oscillator interactions and circuit performance
Although most invertebrate central pattern generating circuits consist of small numbers of neurons, this does not mean that repeated actions that appear indistinguishable necessarily employ an invariant set of neurons. Indeed, in a recent study on the Tritonia escape swim system, optical methods showed that, while many of the neurons in the circuit show stereotyped activity from cycle-to-cycle, others are active in a much more intermittent and variable fashion [65•]. This is reminiscent of
Chains of coupled oscillators to produce movement
In many animals, rhythmic movements depend on coordinated action of muscle groups in many body segments. Classical work on leech swimming [73], leech heartbeat [74], and lamprey swimming [75] was critical in posing questions of how appropriate movement could be generated by coupling of many segmental oscillators. New work seeks to understand peristaltic wave propagation in crawling Drosophila larvae [76•], C. elegans [77] and in the crayfish swimmeret system [78•, 79•], and further addresses
Conclusions
Brain rhythms and oscillations can have many functions in addition to generating rhythmic movements. Nonetheless, the study of small circuits that generate rhythmic movements has revealed principles of circuit organization and function that generalize to the organization of large circuits and the mechanisms by which they combine into functional units. In particular, it is clear that circuit function can be surprisingly robust to variations in many parameters. This is fortunate, as it keeps us
Conflict of interest statement
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
This work was supported in part by NIH grants NS17813 and MH46742.
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