Rapid Adaptation to Changing Mechanical Load by Ordered Recruitment of Identified Motor Neurons

Abstract

As they interact with their environment and encounter challenges, animals adjust their behavior on a moment-to-moment basis to maintain task fitness. This dynamic process of adaptive motor control occurs in the nervous system, but an understanding of the body's biomechanics is essential to properly interpret the behavioral outcomes. To study how animals respond to changing task conditions, we used a model system in which the functional roles of identified neurons and the relevant biomechanics are well understood and can be studied in intact behaving animals: feeding in the marine mollusc Aplysia. We monitored the motor neuronal output of the feeding circuitry as intact animals fed on uniform food stimuli under unloaded and loaded conditions, and we measured the force of retraction during loaded swallows. We observed a previously undescribed pattern of force generation, which can be explained within the appropriate biomechanical context by the activity of just a few key, identified motor neurons. We show that, when encountering load, animals recruit identified retractor muscle motor neurons for longer and at higher frequency to increase retraction force duration. Our results identify a mode by which animals robustly adjust behavior to their environment which is experimentally tractable to further mechanistic investigation. Significance Statement Understanding adaptive motor control requires studying the brain and body together during behavior. Studying motor control systems at the level of individual neurons in intact animals is challenging. The Aplysia feeding system has individual neurons that can be identified from animal to animal and well-studied biomechanics. Prior work showed that animals respond adaptively to changing mechanical load, but did not measure or did not find strong neural correlates. As animals generate increasing force on food, we find that the increased activity and size-ordered recruitment of identified motor neurons allows animals to adapt their behavior. This is the first demonstration of a relationship between identified motor neurons and adaptive motor behavior in intact behaving Aplysia in response to changing mechanical load.

The brain as a dynamically active organ

“…The animal's vision is poorly developed and the smell or the superficial texture of the seaweed are unreliable predictors of its biomechanical properties, such as toughness or size. The different kinds of seaweeds it feeds on not only vary dramatically in these biomechanical properties before the animals arrive, but they can also change in response to herbivory, or once the animal has started to ingest [126][127][128][129]. Therefore, Aplysia has no other choice than trying out how to best ingest the seaweed it is encountering.…”

“…Therefore, Aplysia has no other choice than trying out how to best ingest the seaweed it is encountering. This process manifests itself not only in a high variability of behavioral parameters between each feeding attempt [20,[130][131][132][133], but also during each attempt [126,134,135].…”

Control for Multifunctionality: Bioinspired Control Based on Feeding in Aplysia californica

“…Analysis of experimental data was aided by the Python package neurotic (NEURoscience Tool for Interactive Characterization) [48], and analysis procedures were similar to those described by [47]. Briefly, spikes were detected using window discriminators.…”

“…Amplitude thresholds were determined manually. Spikes were grouped into bursts using firing frequency criteria (see [47] for details; for B7, the burst initiation and termination frequencies were 20 Hz and 10 Hz, respectively, based on observations by [154,155]). Video was used to determine the timing of inward movement of food during swallowing and outward movement of tubing during rejection.…”

Heteroclinic cycling and extinction in May-Leonard models with demographic stochasticity

“…Additionally, both parameters have similar influence on the variance of the cycle length. Recent work has shown that the feeding CPG of the marine mollusk Aplysia californica recruits additional motor neurons when the organism encounters unexpected resistance in swallowing food [17,18], and that variability of motor neuronal activity is reduced for those components of feeding behavior that matter most for task fitness [11]. Although the isolated three pool model considered here lacks important circuit components (such as sensory feedback [10]), the relative sensitivity of the cycle time variance to µ versus Ω could nevertheless suggest experimentally testable questions.…”