Coupling between fast and slow oscillator circuits in Cancer borealis is temperature-compensated

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

doi:10.7554/elife.60454

Cited by 25 publications

(56 citation statements)

References 107 publications

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“…Thus, different modulators can elicit different dynamical mechanisms of rhythm generation. In support of this hypothesis, it has been reported that similar gastric mill rhythms, which are generated by a stimulation of disparate neuromodulatory pathways, have different temperature sensitivity ( Powell et al, 2021a ; Städele et al, 2015 ). A modest temperature increase of 3°C abolishes the MCN1-rhythm ( Städele et al, 2015 ), in contrast, the VCN-rhythm is temperature-robust over a wide range of temperatures, between 7°C and 25°C ( Powell et al, 2021a ).…”

Section: Discussionmentioning

confidence: 82%

“…In support of this hypothesis, it has been reported that similar gastric mill rhythms, which are generated by a stimulation of disparate neuromodulatory pathways, have different temperature sensitivity ( Powell et al, 2021a ; Städele et al, 2015 ). A modest temperature increase of 3°C abolishes the MCN1-rhythm ( Städele et al, 2015 ), in contrast, the VCN-rhythm is temperature-robust over a wide range of temperatures, between 7°C and 25°C ( Powell et al, 2021a ). We propose that the difference in temperature sensitivity between the two versions of the gastric mill rhythm could be explained by the differences in their dynamical mechanisms of oscillation.…”

Section: Discussionmentioning

confidence: 82%

“…Because temperature differentially affects many nonlinear processes shaping circuit output, it is nontrivial for a circuit to maintain its function over a wide range of temperatures. Despite that, many neuronal circuits, including the pyloric and half-center driven gastric mill circuits of crustaceans, are temperature compensated and function over an extended physiological temperature range ( Haddad and Marder, 2018 ; Kushinsky et al, 2019 ; Powell et al, 2021a ; Soofi et al, 2014 ; Tang et al, 2010 ; Tang et al, 2012 ). Complicating the situation, circuit susceptibility to temperature changes is strongly influenced by the modulatory environment ( Haddad and Marder, 2018 ; Soofi and Prinz, 2015 ; Städele et al, 2015 ).…”

Section: Discussionmentioning

confidence: 99%

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Reciprocally inhibitory circuits operating with distinct mechanisms are differently robust to perturbation and modulation

Morozova

Newstein

Marder

2022

eLife

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Reciprocal inhibition is a building block in many sensory and motor circuits. We studied the features that underly robustness in reciprocally inhibitory two neuron circuits. We used the dynamic clamp to create reciprocally inhibitory circuits from pharmacologically isolated neurons of the crab stomatogastric ganglion by injecting artificial graded synaptic (ISyn) and hyperpolarization-activated inward (IH) currents. There is a continuum of mechanisms in circuits that generate antiphase oscillations, with 'release' and 'escape' mechanisms at the extremes, and mixed mode oscillations in between these extremes. In release, the active neuron primarily controls the off/on transitions. In escape, the inhibited neuron controls the transitions. We characterized the robustness of escape and release circuits to alterations in circuit parameters, temperature, and neuromodulation. We found that escape circuits rely on tight correlations between synaptic and H conductances to generate bursting but are resilient to temperature increase. Release circuits are robust to variations in synaptic and H conductances but fragile to temperature increase. The modulatory current (IMI) restores oscillations in release circuits but has little effect in escape circuits. Perturbations can alter the balance of escape and release mechanisms and can create mixed mode oscillations. We conclude that the same perturbation can have dramatically different effects depending on the circuits' mechanism of operation that may not be observable from basal circuit activity.

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Section: Discussionmentioning

confidence: 82%

Section: Discussionmentioning

confidence: 82%

Section: Discussionmentioning

confidence: 99%

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Reciprocally inhibitory circuits operating with distinct mechanisms are differently robust to perturbation and modulation

Morozova

Newstein

Marder

2022

eLife

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“…The coordination of the activities of coupled neural networks at different temperatures is particularly challenging, but often required for proper behavioral functioning. Powell et al (2021) have recently demonstrated that the coordination between two oscillatory circuits in the stomatogastric nervous system (STNS, Figure 1A ) of the crab Cancer borealis is maintained across a broad range of temperatures (7–23°C). The gastric mill and pyloric central pattern generators (CPGs) are coupled, but these rhythms run at very different speeds ( Nadim et al, 1998 ; Bartos et al, 1999 ; Stein, 2017 ).…”

Section: Introductionmentioning

confidence: 99%

Neuromodulation Enables Temperature Robustness and Coupling Between Fast and Slow Oscillator Circuits

Städele

Stein

2022

Front. Cell. Neurosci.

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Acute temperature changes can disrupt neuronal activity and coordination with severe consequences for animal behavior and survival. Nonetheless, two rhythmic neuronal circuits in the crustacean stomatogastric ganglion (STG) and their coordination are maintained across a broad temperature range. However, it remains unclear how this temperature robustness is achieved. Here, we dissociate temperature effects on the rhythm generating circuits from those on upstream ganglia. We demonstrate that heat-activated factors extrinsic to the rhythm generators are essential to the slow gastric mill rhythm’s temperature robustness and contribute to the temperature response of the fast pyloric rhythm. The gastric mill rhythm crashed when its rhythm generator in the STG was heated. It was restored when upstream ganglia were heated and temperature-matched to the STG. This also increased the activity of the peptidergic modulatory projection neuron (MCN1), which innervates the gastric mill circuit. Correspondingly, MCN1’s neuropeptide transmitter stabilized the rhythm and maintained it over a broad temperature range. Extrinsic neuromodulation is thus essential for the oscillatory circuits in the STG and enables neural circuits to maintain function in temperature-compromised conditions. In contrast, integer coupling between pyloric and gastric mill rhythms was independent of whether extrinsic inputs and STG pattern generators were temperature-matched or not, demonstrating that the temperature robustness of the coupling is enabled by properties intrinsic to the rhythm generators. However, at near-crash temperature, integer coupling was maintained only in some animals while it was absent in others. This was true despite regular rhythmic activity in all animals, supporting that degenerate circuit properties result in idiosyncratic responses to environmental challenges.

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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 (copy archived at swh:1:rev:6a67e765e90caa536e6a11f67d9d4737d059af50 ; Gorur-Shandilya, 2021 ), previously described in Powell et al, 2021 . Spikes are identified using a fully connected neural network that learns spike shapes from small labeled datasets.…”

Section: Methodsmentioning

confidence: 99%

Mapping circuit dynamics during function and dysfunction

Gorur-Shandilya

Cronin

Schneider

et al. 2022

eLife

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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 Cancer 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 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 neuromodulatory inputs, 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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Coupling between fast and slow oscillator circuits in Cancer borealis is temperature-compensated

Cited by 25 publications

References 107 publications

Reciprocally inhibitory circuits operating with distinct mechanisms are differently robust to perturbation and modulation

Reciprocally inhibitory circuits operating with distinct mechanisms are differently robust to perturbation and modulation

Neuromodulation Enables Temperature Robustness and Coupling Between Fast and Slow Oscillator Circuits

Mapping circuit dynamics during function and dysfunction

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