Coupling between fast and slow oscillator circuits in<i>Cancer borealis</i>is temperature compensated

Powell, Daniel J.; Haddad, Sara A.; Gorur-Shandilya, Srinivas; Marder, Eve

doi:10.1101/2020.06.26.173427

Cited by 6 publications

(10 citation statements)

References 110 publications

(175 reference statements)

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“…This concept of nested CPGs has recently been extended to explain flexible coordination of behaviors ranging from fish swimming to bird song (Berkowitz, 2019). In a recent publication, a very similar nested CPG to the one we are proposing here has been described in the crab stomatogastric ganglion where fast pyloric and slow gastric mill rhythms are coupled (Powell, Haddad, Gorur-Shandilya, & Marder, 2020). We map fly grooming behavior into this framework in Figure 6 .…”

Section: Discussionsupporting

confidence: 66%

“…In a recent publication, nested CPGs similar to the one we are proposing here have been described in the crab stomatogastric ganglion, where fast pyloric and slow gastric mill rhythms are coupled and compensate for temperature changes (Powell, Haddad, Gorur-Shandilya, & Marder, 2020). The combination of two rhythmic behaviors raises the possibility that the governing circuits interact, like meshed gears of different sizes, to simplify control of a repetitive behavior on multiple time-scales.…”

Section: Discussionmentioning

confidence: 61%

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Behavioral evidence for nested central pattern generator control ofDrosophilagrooming

Ravbar

Zhang

Simpson

2020

Preprint

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Central pattern generators (CPGs) are neurons or neural circuits that produce periodic output without requiring patterned input. More complex behaviors can be assembled from simpler subroutines, and nested CPGs have been proposed to coordinate their repetitive elements, simplifying control over different time-scales. Here, we use behavioral experiments to establish that Drosophila grooming may be controlled by nested CPGs. On the short time-scale (5-7 Hz), flies execute periodic leg sweeps and rubs. More surprisingly, transitions between bouts of head cleaning and leg rubbing are also periodic on a longer time-scale (0.3 - 0.6 Hz). We examine grooming at a range of temperatures to show that the frequencies of both oscillations increase – a hallmark of CPG control – and also that the two time-scales increase at the same rate, indicating that the nested CPGs may be linked. This relationship also holds when sensory drive is held constant using optogenetic activation, but the rhythms decouple in spontaneously grooming flies, showing that alternative control modes are possible. Nested CPGs simplify generation of complex but repetitive behaviors, and identifying them in Drosophila grooming presents an opportunity to map the neural circuits that constitute them.

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Section: Discussionsupporting

confidence: 66%

Section: Discussionmentioning

confidence: 61%

Behavioral evidence for nested central pattern generator control ofDrosophilagrooming

Ravbar

Zhang

Simpson

2020

Preprint

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“…PD spikes were identified from pdn , intracellular recordings, and lvn . We used a custom-designed spike identification and sorting software (called “crabsort”) that we have made freely available at https://github.com/sg-s/crabsort previously described in Powell et al (2021). Spikes are identified using a fully connected neural network that learns spike shapes from small labelled data sets.…”

Section: Methodsmentioning

confidence: 99%

“…This study used a large dataset collected by various experimenters, and included data originally collected for other studies (Tang et al, 2012(Tang et al, , 2010Haddad and Marder, 2018;Haley et al, 2018;Rosenbaum and Marder, 2018;Powell et al, 2021;He et al, 2020). As such, this post-hoc analysis is limited ultimately by the data: its quantity, the way it was collected, and the decisions made and tradeoffs chosen by the experimenter who collected it.…”

Section: Ahead-of-time Experimental Design Can Maximize Utility and Interpretability Of Datamentioning

confidence: 99%

Mapping circuit dynamics during function and dysfunction

Gorur-Shandilya

Cronin

et al. 2021

Preprint

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Neural circuits can generate many spike patterns, but only some are functional. The study of how circuits generate and maintain functional dynamics is hindered by a poverty of description of circuit dynamics across functional and dysfunctional states. For example, although the regular oscillation of a central pattern generator is well characterized by its frequency and the phase relationships between its neurons, these metrics are ineffective descriptors of the irregular and aperiodic dynamics that circuits can generate under perturbation or in disease states. By recording the circuit dynamics of the well-studied pyloric circuit in C. borealis, we used statistical features of spike times from neurons in the circuit to visualize the spike patterns generated by this circuit under a variety of conditions. This unsupervised approach captures both the variability of functional rhythms and the diversity of atypical dynamics in a single map. Clusters in the map identify qualitatively different spike patterns hinting at different dynamical states in the circuit. State probability and the statistics of the transitions between states varied with environmental perturbations, removal of descending neuromodulation, and the addition of exogenous neuromodulators. This analysis reveals strong mechanistically interpretable links between complex changes in the collective behavior of a neural circuit and specific experimental manipulations, and can constrain hypotheses of how circuits generate functional dynamics despite variability in circuit architecture and environmental perturbations.

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“…Saline or peptide solution was continuously superfused (10 ml/min) at 10-12°C across the preparation for the duration of each experiment. Saline temperature was maintained within this narrow range because these animals are poikilotherms and so neuronal activity is affected by temperature (Tang et al, 2010;Stadele et al, 2015;Powell et al, 2020).…”

Section: Methodsmentioning

confidence: 99%

Degenerate circuits use distinct mechanisms to respond similarly to the same perturbation

Powell

Marder

Nusbaum

2020

Preprint

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There is considerable flexibility embedded within neural circuits. For example, separate modulatory inputs can differently configure the same underlying circuit but these different configurations generate comparable, or degenerate, activity patterns. However, little is known about whether these mechanistically different circuits in turn exhibit degenerate responses to the same inputs. We examined this issue using the crab (Cancer borealis) stomatogastric nervous system, in which stimulating the modulatory projection neuron MCN1 and bath applying the neuropeptide CabPK II elicit similar gastric mill (chewing) rhythms in the stomatogastric ganglion, despite differentially configuring the same neural circuit. We showed previously that bath applying the peptide hormone CCAP or stimulating the muscle stretch-sensitive sensory neuron GPR during the MCN1-elicited gastric mill rhythm selectively prolongs the protraction or retraction phase, respectively. Here, we found that these two influences on the CabPK-rhythm elicited some unique and unexpected consequences compared to their actions on the MCN1-rhythm. For example, in contrast to its effect on the MCN1-rhythm, CCAP selectively decreased the CabPK-rhythm retraction phase and thus increased the rhythm speed, whereas the CabPK-rhythm response to stimulating GPR during the retraction phase was similar its effect on the MCN1-rhythm (i.e. prolonging retraction). Interestingly, despite the comparable GPR actions on these degenerate rhythms, the underlying synaptic mechanism was distinct. Thus, degenerate circuits do not necessarily exhibit degenerate responses to the same influence, but when they do, it can occur via different underlying mechanisms.Significance StatementCircuits generating seemingly identical behaviors are often thought to arise from identical circuit states, as that is the most parsimonious explanation. Here we take advantage of an alternate scenario wherein a well-defined circuit with known connectivity generates similar activity patterns using distinct circuit states, via known mechanisms. The same peptide hormone modulation of these distinct circuit states produced divergent activity patterns, whereas the same sensory feedback altered these circuit outputs similarly but via different synaptic pathways. The latter observation limits the insights available from comparable studies in systems lacking detailed access to the underlying circuit.

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Coupling between fast and slow oscillator circuits inCancer borealisis temperature compensated

Cited by 6 publications

References 110 publications

Behavioral evidence for nested central pattern generator control ofDrosophilagrooming

Behavioral evidence for nested central pattern generator control ofDrosophilagrooming

Mapping circuit dynamics during function and dysfunction

Degenerate circuits use distinct mechanisms to respond similarly to the same perturbation

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