Nested Neuronal Dynamics Orchestrate a Behavioral Hierarchy across Timescales

Kaplan, Harris S.; Thula, Oriana Salazar; Khoss, Niklas; Zimmer, Manuel

doi:10.1016/j.neuron.2019.10.037

Cited by 121 publications

(171 citation statements)

References 85 publications

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“…A single pair of PVD sensory neurons are able to regulate proprioception as well as responses to harsh touch (Tao et al, 2019). SMD neurons are also multifunctional and play roles at multiple hierarchical levels such as fast head casting and omega turn behaviors (Kaplan et al, 2020). This growing body of evidence indicates that complex brain functions rely on not only the vast number of neurons, but also multiple functions of individual neurons.…”

Section: Discussionmentioning

confidence: 99%

AC. elegansneuron both promotes and suppresses motor behavior to fine tune motor output

Zhou

Wani

et al. 2020

Preprint

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How neural circuits drive behavior is a central question in neuroscience. Proper execution of motor behavior requires the precise coordination of many neurons. Within a motor circuit, individual neurons tend to play discrete roles by promoting or suppressing motor output. How exactly neurons function in specific roles to fine tune motor output is not well understood. In C. elegans, the interneuron RIM plays important yet complex roles in locomotion behavior. Here, we show that RIM both promotes and suppresses distinct features of locomotion behavior to fine tune motor output. This dual function is achieved via the excitation and inhibition of the same motor circuit by electrical and chemical neurotransmission, respectively. Additionally, this bi-directional regulation contributes to motor adaptation in animals placed in novel environments. Our findings reveal that individual neurons within a neural circuit may act in opposing ways to regulate circuit dynamics to fine tune behavioral output.

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Section: Discussionmentioning

confidence: 99%

AC. elegansneuron both promotes and suppresses motor behavior to fine tune motor output

Zhou

Wani

et al. 2020

Preprint

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“…They have been previously implicated in directional head bending and steering. [37][38][39][40] To better define the behavioral effects of SMD modulation, we more closely examined body bending in animals overexpressing ckr-1 under control of the odr-2 (16) promoter, and also using a second promoter, flp-22∆4, that was recently shown to drive selective expression in the SMD neurons 41 (Fig. 6A).…”

Section: Ckr-1 Functions In the Smd Head Motor Neurons To Modulate Bomentioning

confidence: 99%

A conserved neuropeptide system links head and body motor circuits to enable adaptive behavior

Ramachandran

Banerjee

Bhattacharya

et al. 2020

Preprint

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Neuromodulators promote adaptive behaviors in response to either environmental or internal physiological changes. These responses are often complex and may involve concerted activity changes across circuits that are not physically connected. It is not well understood how neuromodulatory systems act across circuits to elicit complex behavioral responses. Here we show that the C. elegans NLP-12 neuropeptide system shapes responses to food availability by selectively modulating the activity of head and body wall motor neurons. NLP-12 modulation of the head and body wall motor circuits is generated through conditional involvement of alternate GPCR targets. The CKR-1 GPCR is highly expressed in the head motor circuit, and functions to enhance head bending and increase trajectory reorientations during local food searching, primarily through stimulatory actions on SMD head motor neurons. In contrast, NLP-12 activation of CKR-1 and CKR-2 GPCRs regulates body bending under basal conditions, primarily through actions on body wall motor neurons. Thus, locomotor responses to changing environmental conditions emerge from conditional NLP-12 stimulation of head or body wall motor neuron targets.

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“…Furthermore, experiments are increasingly shining light on the hierarchical mechanisms of sequential behaviour. An example is movement sequences in multiple animal models, such as Drosophila (Seeds et al 2014;Berman et al 2016;Jovanic et al 2016), mice (Jin and Costa 2015;Geddes et al 2018;Markowitz et al 2018) and C. elegans (Kato et al 2015; Kaplan et al 2020). Simultaneous recordings of behaviour and neural activity are now possible in order to relate the two together (Vogelstein et al 2014;Berman 2018).…”

Section: Introductionmentioning

confidence: 99%

Learning compositional sequences with multiple time scales through a hierarchical network of spiking neurons

Maes

Barahona

Clopath

2020

Preprint

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Sequential behaviour is often compositional and organised across multiple time scales: a set of individual elements developing on short time scales (motifs) are combined to form longer functional sequences (syntax). Such organisation leads to a natural hierarchy that can be used advantageously for learning, since the motifs and the syntax can be acquired independently. Despite mounting experimental evidence for hierarchical structures in neuroscience, models for temporal learning based on neuronal networks have mostly focused on serial methods. Here, we introduce a network model of spiking neurons with a hierarchical organisation aimed at sequence learning on multiple time scales. Using biophysically motivated neuron dynamics and local plasticity rules, the model can learn motifs and syntax independently. Furthermore, the model can relearn sequences efficiently and store multiple sequences. Compared to serial learning, the hierarchical model displays faster learning, more flexible relearning, increased capacity, and higher robustness to perturbations. The hierarchical model redistributes the variability: it achieves high motif fidelity at the cost of higher variability in the between-motif timings.

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Nested Neuronal Dynamics Orchestrate a Behavioral Hierarchy across Timescales

Cited by 121 publications

References 85 publications

AC. elegansneuron both promotes and suppresses motor behavior to fine tune motor output

AC. elegansneuron both promotes and suppresses motor behavior to fine tune motor output

A conserved neuropeptide system links head and body motor circuits to enable adaptive behavior

Learning compositional sequences with multiple time scales through a hierarchical network of spiking neurons

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