Preparing the Periphery for a Subsequent Behavior: Motor Neuronal Activity during Biting Generates Little Force but Prepares a Retractor Muscle to Generate Larger Forces during Swallowing inAplysia

Abstract

Some behaviors occur in obligatory sequence, such as reaching before grasping an object. Can the earlier behavior serve to prepare the musculature for the later behavior? If it does, what is the underlying neural mechanism of the preparation? To address this question, we examined two feeding behaviors in the marine mollusk Aplysia californica, one of which must precede the second: biting and swallowing. Biting is an attempt to grasp food. When that attempt is successful, the animal immediately switches to swallowing to ingest food. The main muscle responsible for pulling food into the buccal cavity during swallowing is the I3 muscle, whose motor neurons B6, B9, and B3 have been previously identified. By performing recordings from these neurons in vivo in intact, behaving animals or in vitro in a suspended buccal mass preparation, we demonstrated that the frequencies and durations of these motor neurons increased from biting to swallowing. Using the physiological patterns of activation to drive these neurons intracellularly, we further demonstrated that activating them using biting-like frequencies and durations, either alone or in combination, generated little or no force in the I3 muscle. When biting-like patterns preceded swallowing-like patterns, however, the forces during the subsequent swallowing-like patterns were significantly enhanced. Sequences of swallowing-like patterns, either with these neurons alone or in combination, further enhanced forces in the I3 muscle. These results suggest a novel mechanism for enhancing force production in a muscle, and may be relevant to understanding motor control in vertebrates.

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

“…As a first step toward locating the bursts of identified motor neurons and their firing frequencies, individual spikes were detected and grouped into spike trains using manually specified window discriminators, which captured signal peaks on a given channel occurring within a given amplitude range and time window. Individual motor neurons can be identified from extracellular nerve signals in this system because of their reliable relative amplitudes and phase of activity (Morton and Chiel, 1993b;Lu et al, 2013Lu et al, , 2015McManus et al, 2014;Cullins et al, 2015b) (see Table 1). The spike amplitude of some neurons, especially B8a/b and B4/B5, can vary when these neurons activate at high frequencies due to spike collisions seen in the extracellular nerve recordings (Morton and Chiel, 1993b;Warman and Chiel, 1995), so we designed the window discriminators to account for this variability.…”

“…Burst identification using frequency thresholds. Previous work has shown that muscles in this system act as low-pass filters, and motor neuron activity may not result in measurable force if firing rates are too slow or activity is too brief (Yu et al, 1999;Lu et al, 2015). To address this, frequency thresholds were applied to the spike trains identified in the previous step to determine the start and end of candidate bursts (see Table 1).…”

“…In some analyses, the B3 and B6/B9 motor neurons were combined due to their functional similarity (Lu et al, 2015) and are referred to collectively as B3/B6/B9. The combined unit was said to be bursting if either B3 or B6/B9 (or both) was bursting.…”

“…The much larger forces animals generate on their own when swallowing tough foods in their natural habitat have not been measured, nor have the neural correlates of adaptation to high loads. Recent studies of the biomechanics of feeding (Neustadter et al, 2002(Neustadter et al, , 2007Kehl et al, 2019), modeling (Neustadter et al, 2002;Sutton et al, 2004a), and neural control (McManus et al, 2014;Cullins et al, 2015b;Lu et al, 2015) have provided further insights into the behavioral roles of individual neurons, suggesting that it might now be possible to relate behavior to neural activity despite the high variability.…”

Tactile suppression in goal-directed movement

“…One working hypothesis to still explore is that by such attenuation the 'scene' (i.e., the body environment) is prepared/made ready/transformed into the scene for something else. For example, nature is rife with examples of processes which were once thought of as irrelevant, and which have proved to be meaningful (e.g., the aplysia biting or swallowing muscles; Lu, Mcmanus, Cullins, & Chiel, 2015).…”