Precise timing is ubiquitous, consistent and coordinated across a comprehensive, spike-resolved flight motor program

Conn, Rachel; Putney, Joy; Sponberg, Simon

doi:10.1101/602961

Cited by 7 publications

(13 citation statements)

References 73 publications

(18 reference statements)

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“…The previously published data set used in this analysis recorded the comprehensive, spike-resolved motor program of the hawk moth, Manduca sexta (N = 7), and its motor output in a tethered flight preparation [12,20]. EMG signals from the 10 primary muscles actuating each moth's wings were recorded with spike-level resolution using implanted silver wire electrodes (Fig 1A ,C).…”

Section: Comprehensive Spike-resolved Motor Program Data Setmentioning

confidence: 99%

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An information theoretic method to resolve millisecond-scale spike timing precision in a comprehensive motor program

Putney

Niebur

Barker

et al. 2021

Preprint

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Sensory inputs in nervous systems are often encoded at the millisecond scale in a temporally precise code. There is now a growing appreciation for the prevalence of precise timing encoding in motor systems. Animals from moths to birds control motor outputs using precise spike timing, but we largely do not know at what scale timing matters in these circuits due to the difficulty of recording a complete set of spike-resolved motor signals and relatively few methods for assessing spike timing precision. We introduce a method to estimate spike timing precision in motor circuits using continuous MI estimation at increasing levels of added uniform noise. This method can assess spike timing precision at fine scales for encoding rich motor output variation. We demonstrate the advantages of this approach compared to a previously established discrete information theoretic method of assessing spike timing precision. We use this method to analyze a data set of simultaneous turning (yaw) torque output and EMG recordings from the 10 primary muscles of Manduca sexta as tethered moths visually tracked a robotic flower moving with a 1 Hz sinusoidal trajectory. We know that all 10 muscles in this motor program encode the majority of information about yaw torque in spike timings, but we do not know whether individual muscles receive information encoded at different levels of precision. Using the continuous MI method, we demonstrate that the scale of temporal precision in all motor units in this insect flight circuit is at the sub-millisecond or millisecond-scale, with variation in precision scale present between muscle types. This method can be applied broadly to estimate spike timing precision in sensory and motor circuits in both invertebrates and vertebrates.

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Section: Comprehensive Spike-resolved Motor Program Data Setmentioning

confidence: 99%

“…The motor output M is represented as the projection of each wing stroke onto the first two principal component (PC) loadings that explain the variance of the fully dimensional τ z . Data shown and panels A-B taken and adapted from Putney et al 2019 [12,20].…”

Section: Comprehensive Spike-resolved Motor Program Data Setmentioning

confidence: 99%

An information theoretic method to resolve millisecond-scale spike timing precision in a comprehensive motor program

Putney

Niebur

Barker

et al. 2021

Preprint

Self Cite

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“…Nevertheless, the increased minimum to maximum range of IPIs observed in the histograms in result of four applied methods of synchronization turns our attention to a significance of rate coding. In a recent study on insects Putney et al (2019) [49] reveled that timing of impulses between motoneuron discharge patterns plays a higher role than a number of pulses, but it is well known that changes in IPIs are crucial for the force development also in the mammalian (cat and rat) muscles [29,30,35,50,51,52].…”

Section: Models Of Mu Synchronizationmentioning

confidence: 99%

Effect of synchronization of firings of different motor unit types on the force variability in a model of the rat medial gastrocnemius muscle

Raikova

Krasteva

Krutki³

et al. 2021

PLoS Comput Biol

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The synchronized firings of active motor units (MUs) increase the oscillations of muscle force, observed as physiological tremor. This study aimed to investigate the effects of synchronizing the firings within three types of MUs (slow—S, fast resistant to fatigue–FR, and fast fatigable–FF) on the muscle force production using a mathematical model of the rat medial gastrocnemius muscle. The model was designed based on the actual proportion and physiological properties of MUs and motoneurons innervating the muscle. The isometric muscle and MU forces were simulated by a model predicting non-synchronized firing of a pool of 57 MUs (including 8 S, 23 FR, and 26 FF) to ascertain a maximum excitatory signal when all MUs were recruited into the contraction. The mean firing frequency of each MU depended upon the twitch contraction time, whereas the recruitment order was determined according to increasing forces (the size principle). The synchronization of firings of individual MUs was simulated using four different modes and inducing the synchronization of firings within three time windows (± 2, ± 4, and ± 6 ms) for four different combinations of MUs. The synchronization was estimated using two parameters, the correlation coefficient and the cross-interval synchronization index. The four scenarios of synchronization increased the values of the root-mean-square, range, and maximum force in correlation with the increase of the time window. Greater synchronization index values resulted in higher root-mean-square, range, and maximum of force outcomes for all MU types as well as for the whole muscle output; however, the mean spectral frequency of the forces decreased, whereas the mean force remained nearly unchanged. The range of variability and the root-mean-square of forces were higher for fast MUs than for slow MUs; meanwhile, the relative values of these parameters were highest for slow MUs, indicating their important contribution to muscle tremor, especially during weak contractions.

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“…The demand for understanding the implications of convergent and divergent structure for the information coding of a spiking neural network is especially high in light of growing experimental evidence showing that spike timing can encode significantly more information about inputs [33] and outputs [34] than spike count. At the sensory input level, millisecond-level variations in spike timings encode significant proprioceptive [35], visual [36], auditory [37], olfactory [38] and tactile [39] information.…”

Section: Introductionmentioning

confidence: 99%

Temporal resolution of spike coding in feedforward networks with signal convergence and divergence

Mobille,

Sikandar,

Sponberg

et al. 2024

Preprint

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Convergent and divergent structures in the networks that make up biological brains are found universally across many species and brain regions at various scales. Neurons in these networks fire action potentials, or "spikes", whose precise timing is becoming increasingly appreciated as large sources of information about both sensory input and motor output. While previous theories on coding in convergent and divergent networks have largely neglected the role of precise spike timing, our model and analyses place this aspect at the forefront. For a suite of stimuli with different timescales, we demonstrate that structural bottlenecks (small groups of neurons) post-synaptic to network convergence have a stronger preference for spike timing codes than expansion layers created by structural divergence. Additionally, we found that a simple network model with similar convergence and divergence ratios to those found experimentally can reproduce the relative contribution of spike timing information about motor output in the hawkmoth Manduca sexta. Our simulations and analyses suggest a relationship between the level of convergent/divergent structure present in a feedforward network and the loss of stimulus information encoded by its population spike trains as their temporal resolution decreases, which could be confirmed experimentally across diverse neural systems in future studies. We further show that this relationship can be generalized across different models and measures, implying a potentially fundamental link between network structure and coding strategy using spikes.

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Precise timing is ubiquitous, consistent and coordinated across a comprehensive, spike-resolved flight motor program

Cited by 7 publications

References 73 publications

An information theoretic method to resolve millisecond-scale spike timing precision in a comprehensive motor program

An information theoretic method to resolve millisecond-scale spike timing precision in a comprehensive motor program

Effect of synchronization of firings of different motor unit types on the force variability in a model of the rat medial gastrocnemius muscle

Temporal resolution of spike coding in feedforward networks with signal convergence and divergence

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