Sparse spike trains and the limitation of rate codes underlying rapid behaviours

Fabian, Joseph M.; O'Carrol, David C.; Wiederman, Steven D.

doi:10.1098/rsbl.2023.0099

Cited by 3 publications

References 23 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

Sparse spike trains and the limitation of rate codes underlying rapid behaviours

Fabian,

O'Carrol,

Wiederman

2023

Biol. Lett.

Self Cite

View full text Add to dashboard Cite

Animals live in dynamic worlds where they use sensorimotor circuits to rapidly process information and drive behaviours. For example, dragonflies are aerial predators that react to movements of prey within tens of milliseconds. These pursuits are likely controlled by identified neurons in the dragonfly, which have well-characterized physiological responses to moving targets. Predominantly, neural activity in these circuits is interpreted in context of a rate code, where information is conveyed by changes in the number of spikes over a time period. However, such a description of neuronal activity is difficult to achieve in real-world, real-time scenarios. Here, we contrast a neuroscientists' post-hoc view of spiking activity with the information available to the animal in real-time. We describe how performance of a rate code is readily overestimated and outline a rate code's significant limitations in driving rapid behaviours.

show abstract

Sparse spike trains and the limitation of rate codes underlying rapid behaviours

Fabian,

O'Carrol,

Wiederman

2023

Biol. Lett.

Self Cite

View full text Add to dashboard Cite

show abstract

Wireless recordings from dragonfly target detecting neurons during prey interception flight

Lin,

Siwanowicz,

Leonardo

2024

Preprint

View full text Add to dashboard Cite

Target interception is a complex sensorimotor behavior which requires fine tuning of the sensory system and its strategic coordination with the motor system. Despite various theories about how interception is achieved, its neural implementation remains unknown. We have previously shown that hunting dragonflies employ a balance of reactive and predictive control to intercept prey, using sophisticated model driven predictions to account for expected prey and self-motion. Here we explore the neural substrate of this interception system by investigating a well-known class of target-selective descending neurons (TSDNs). These cells have long been speculated to underlie interception steering but have never been studied in a behaving dragonfly. We combined detailed neuroanatomy, high-precision kinematics data and state-of-the-art neural telemetry to measure TSDN activity during flight. We found that TSDNs are exquisitely tuned to prey angular size and speed at ethological distances, and that they synapse directly onto neck and wing motoneurons in an unusual manner. However, we found that TSDNs were only weakly active during flight and are thus unlikely to provide the primary steering signal. Instead, they appear to drive the foveating head movements that stabilize prey on the eye before and likely throughout the interception flight. We suggest the TSDN population implements the reactive portion of the interception steering control system, coordinating head and wing movements to compensate for unexpected prey motion.

show abstract

Localized and Long-Lasting Adaptation in Dragonfly Target-Detecting Neurons

Schwarz,

O'Carroll,

Evans

et al. 2024

eNeuro

View full text Add to dashboard Cite

Some visual neurons in the dragonfly (Hemicordulia tau) optic lobe respond to small, moving targets, likely underlying their fast pursuit of prey and conspecifics. In response to repetitive targets presented at short intervals, the spiking activity of these “small target motion detector” (STMD) neurons diminishes over time. Previous experiments limited this adaptation by including intertrial rest periods of varying durations. However, the characteristics of this effect have never been quantified. Here, using extracellular recording techniques lasting for several hours, we quantified both the spatial and temporal properties of STMD adaptation. We found that the time course of adaptation was variable across STMD units. In any one STMD, a repeated series led to more rapid adaptation, a minor accumulative effect more akin to habituation. Following an adapting stimulus, responses recovered quickly, though the rate of recovery decreased nonlinearly over time. We found that the region of adaptation is highly localized, with targets displaced by ∼2.5° eliciting a naive response. Higher frequencies of target stimulation converged to lower levels of sustained response activity. We determined that adaptation itself is a target-tuned property, not elicited by moving bars or luminance flicker. As STMD adaptation is a localized phenomenon, dependent on recent history, it is likely to play an important role in closed-loop behavior where a target is foveated in a localized region for extended periods of the pursuit duration.

show abstract

Sparse spike trains and the limitation of rate codes underlying rapid behaviours

Cited by 3 publications

References 23 publications

Sparse spike trains and the limitation of rate codes underlying rapid behaviours

Sparse spike trains and the limitation of rate codes underlying rapid behaviours

Wireless recordings from dragonfly target detecting neurons during prey interception flight

Localized and Long-Lasting Adaptation in Dragonfly Target-Detecting Neurons

Contact Info

Product

Resources

About