scholarly journals Augmenting Flexibility: Mutual Inhibition Between Inhibitory Neurons Expands Functional Diversity

2020 ◽  
Author(s):  
Belle Liu ◽  
Alexander James White ◽  
Chung-Chuan Lo

AbstractOne of the most intriguing observations of recurrent neural circuits is their flexibility. Seemingly, this flexibility extends far beyond the ability to learn, but includes the ability to use learned procedures to respond to novel situations. Here, we report that this flexibility arises from the synergistic interplay between recurrent mutual excitation and recurrent mutual inhibition. Specifically, we show that mutual inhibition is critical in expanding the functionality of the circuit, far beyond what feedback inhibition alone can accomplish. By taking advantage of dynamical systems theory and bifurcation analysis, we show mutual inhibition doubles the number of cusp bifurcations in the system in small neural circuits. As a concrete example, we build a simulation model of a class of functional motifs we call Coupled Recurrent inhibitory and Recurrent excitatory Loops (CRIRELs). These CRIRELs have the advantage of being multi-functional, performing a plethora of functions, including decisions, switches, toggles, central pattern generators, depending solely on the input type. We then use bifurcation theory to show how mutual inhibition gives rise to this broad repertoire of possible functions. Finally, we demonstrate how this trend also holds for larger networks, and how mutual inhibition greatly expands the amount of information a recurrent network can hold.

2000 ◽  
Vol 84 (3) ◽  
pp. 1186-1193 ◽  
Author(s):  
Peter T. Morgan ◽  
Ray Perrins ◽  
Philip E. Lloyd ◽  
Klaudiusz R. Weiss

Intrinsic and extrinsic neuromodulation are both thought to be responsible for the flexibility of the neural circuits (central pattern generators) that control rhythmic behaviors. Because the two forms of modulation have been studied in different circuits, it has been difficult to compare them directly. We find that the central pattern generator for biting in Aplysia is modulated both extrinsically and intrinsically. Both forms of modulation increase the frequency of motor programs and shorten the duration of the protraction phase. Extrinsic modulation is mediated by the serotonergic metacerebral cell (MCC) neurons and is mimicked by application of serotonin. Intrinsic modulation is mediated by the cerebral peptide-2 (CP-2) containing CBI-2 interneurons and is mimicked by application of CP-2. Since the effects of CBI-2 and CP-2 occlude each other, the modulatory actions of CBI-2 may be mediated by CP-2 release. Although the effects of intrinsic and extrinsic modulation are similar, the neurons that mediate them are active predominantly at different times, suggesting a specialized role for each system. Metacerebral cell (MCC) activity predominates in the preparatory (appetitive) phase and thus precedes the activation of CBI-2 and biting motor programs. Once the CBI-2s are activated and the biting motor program is initiated, MCC activity declines precipitously. Hence extrinsic modulation prefacilitates biting, whereas intrinsic modulation occurs during biting. Since biting inhibits appetitive behavior, intrinsic modulation cannot be used to prefacilitate biting in the appetitive phase. Thus the sequential use of extrinsic and intrinsic modulation may provide a means for premodulation of biting without the concomitant disruption of appetitive behaviors.


2016 ◽  
Vol 371 (1685) ◽  
pp. 20150057 ◽  
Author(s):  
Paul S. Katz

Comparisons of rhythmic movements and the central pattern generators (CPGs) that control them uncover principles about the evolution of behaviour and neural circuits. Over the course of evolutionary history, gradual evolution of behaviours and their neural circuitry within any lineage of animals has been a predominant occurrence. Small changes in gene regulation can lead to divergence of circuit organization and corresponding changes in behaviour. However, some behavioural divergence has resulted from large-scale rewiring of the neural network. Divergence of CPG circuits has also occurred without a corresponding change in behaviour. When analogous rhythmic behaviours have evolved independently, it has generally been with different neural mechanisms. Repeated evolution of particular rhythmic behaviours has occurred within some lineages due to parallel evolution or latent CPGs. Particular motor pattern generating mechanisms have also evolved independently in separate lineages. The evolution of CPGs and rhythmic behaviours shows that although most behaviours and neural circuits are highly conserved, the nature of the behaviour does not dictate the neural mechanism and that the presence of homologous neural components does not determine the behaviour. This suggests that although behaviour is generated by neural circuits, natural selection can act separately on these two levels of biological organization.


2020 ◽  
Author(s):  
Primoz Ravbar ◽  
Neil Zhang ◽  
Julie H. Simpson

AbstractCentral 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.


eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Akira Fushiki ◽  
Maarten F Zwart ◽  
Hiroshi Kohsaka ◽  
Richard D Fetter ◽  
Albert Cardona ◽  
...  

Animals move by adaptively coordinating the sequential activation of muscles. The circuit mechanisms underlying coordinated locomotion are poorly understood. Here, we report on a novel circuit for the propagation of waves of muscle contraction, using the peristaltic locomotion of Drosophila larvae as a model system. We found an intersegmental chain of synaptically connected neurons, alternating excitatory and inhibitory, necessary for wave propagation and active in phase with the wave. The excitatory neurons (A27h) are premotor and necessary only for forward locomotion, and are modulated by stretch receptors and descending inputs. The inhibitory neurons (GDL) are necessary for both forward and backward locomotion, suggestive of different yet coupled central pattern generators, and its inhibition is necessary for wave propagation. The circuit structure and functional imaging indicated that the commands to contract one segment promote the relaxation of the next segment, revealing a mechanism for wave propagation in peristaltic locomotion.


2016 ◽  
Vol 116 (5) ◽  
pp. 2405-2419 ◽  
Author(s):  
Eve Armstrong ◽  
Henry D. I. Abarbanel

We propose a functional architecture of the adult songbird nucleus HVC in which the core element is a “functional syllable unit” (FSU). In this model, HVC is organized into FSUs, each of which provides the basis for the production of one syllable in vocalization. Within each FSU, the inhibitory neuron population takes one of two operational states: 1) simultaneous firing wherein all inhibitory neurons fire simultaneously, and 2) competitive firing of the inhibitory neurons. Switching between these basic modes of activity is accomplished via changes in the synaptic strengths among the inhibitory neurons. The inhibitory neurons connect to excitatory projection neurons such that during state 1 the activity of projection neurons is suppressed, while during state 2 patterns of sequential firing of projection neurons can occur. The latter state is stabilized by feedback from the projection to the inhibitory neurons. Song composition for specific species is distinguished by the manner in which different FSUs are functionally connected to each other. Ours is a computational model built with biophysically based neurons. We illustrate that many observations of HVC activity are explained by the dynamics of the proposed population of FSUs, and we identify aspects of the model that are currently testable experimentally. In addition, and standing apart from the core features of an FSU, we propose that the transition between modes may be governed by the biophysical mechanism of neuromodulation.


2018 ◽  
Author(s):  
Jeonghyuk Park ◽  
Shu Kondo ◽  
Hiromu Tanimoto ◽  
Hiroshi Kohsaka ◽  
Akinao Nose

ABSTRACTRhythmic animal behaviors are regulated in part by neural circuits called the central pattern generators (CPGs). Classifying neural population activities correlated with body movements and identifying the associated component neurons are critical steps in understanding CPGs. Previous methods that classify neural dynamics obtained by dimension reduction algorithms often require manual optimization which could be laborious and preparation-specific. Here, we present a simpler and more flexible method that is based on the pre-trained convolutional neural network model VGG-16 and unsupervised learning, and successfully classifies the fictive motor patterns in Drosophila larvae under various imaging conditions. We also used voxel-wise correlation mapping to identify neurons associated with motor patterns. By applying these methods to neurons targeted by 5-HT2A-GAL4, which we generated by the CRISPR/Cas9-system, we identified two classes of interneurons, termed Seta and Leta, which are specifically active during backward but not forward fictive locomotion. Optogenetic activation of Seta and Leta neurons increased backward locomotion. Conversely, thermogenetic inhibition of 5-HT2A-GAL4 neurons or application of a 5-HT2 antagonist decreased backward locomotion induced by noxious light stimuli. This study establishes an accelerated pipeline for activity profiling and cell identification in larval Drosophila and implicates the serotonergic system in the modulation of backward locomotion.


2010 ◽  
Vol 56 (5) ◽  
pp. 537-549 ◽  
Author(s):  
Gordon A. Wyse

Abstract Many behavioral activities of the horseshoe crab Limulus are rhythmic, and most of these are produced in large part by central pattern generators within the CNS. The chain of opisthosomal ('abdominal') ganglia controls gill movements of ventilation and gill cleaning, and the prosomal ring of fused ganglia (brain and segmental 'thoracic' ganglia) controls generation of feeding and locomotor movements of the legs. Both the opisthosomal CNS and the prosomal CNS can generate behaviorally appropriate patterns of motor output in isolation, without movements or sensory input. Preparations of the isolated opisthosomal CNS generate rhythmic output patterns of motor activity characterized as fictive ventilatory and gill cleaning rhythms. Moreover, CNS preparations also express longer-term patterns, such as intermittent ventilation or sequential bouts of ventilation and gill cleaning. Such longer-term patterns are commonly observed in intact animals. The isolated prosomal CNS does not spontaneously generate the activity patterns characteristic of walking, swimming, and feeding. However, perfusion of octopamine in the isolated prosomal CNS activates central pattern generators underlying rhythmic chewing movements, and injection of octopamine into intact Limulus promotes the chewing pattern of feeding, whether or not food is presented. Our understanding of the ability of neuromodulators such as octopamine to elicit or alter central motor programs may help to clarify the central neural circuits of pattern generation that produce and coordinate these rhythmic behaviors.


eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Primoz Ravbar ◽  
Neil Zhang ◽  
Julie H Simpson

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, organizing control over different time scales. Here, we use behavioral experiments to establish that Drosophila grooming may be controlled by nested CPGs. On a short time scale (5–7 Hz, ~ 200 ms/movement), flies clean with periodic leg sweeps and rubs. More surprisingly, transitions between bouts of head sweeping and leg rubbing are also periodic on a longer time scale (0.3–0.6 Hz, ~2 s/bout). 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 rhythms at the two time scales increase at the same rate, indicating that the nested CPGs may be linked. This relationship holds when sensory drive is held constant using optogenetic activation, but oscillations can decouple in spontaneously grooming flies, showing that alternative control modes are possible. Loss of sensory feedback does not disrupt periodicity but slow down the longer time scale alternation. Nested CPGs simplify the 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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