Hand-jaw coordination as mice handle food is organized around intrinsic structure-function relationships

Abstract

Rodent jaws evolved structurally to support dual functionality, for either biting or chewing food. Rodent hands also function dually during food handling, for actively manipulating or statically holding food. How are these oral and manual functions coordinated? We combined electrophysiological recording of muscle activity and kilohertz kinematic tracking to analyze masseter and hand actions as mice of both sexes handled food. Masseter activity was organized into two modes synchronized to hand movement modes. In holding/chewing mode, mastication occurred as rhythmic (∼5 Hz) masseter activity while the hands held food below the mouth. In oromanual/ingestion mode, bites occurred as lower-amplitude aperiodic masseter events that were precisely timed to follow regrips (by ∼200 ms). Thus, jaw and hand movements are flexibly coordinated during food handling: uncoupled in holding/chewing mode, and tightly coordinated in oromanual/ingestion mode as regrip-bite sequences. Key features of this coordination were captured in a simple model of hierarchically orchestrated mode-switching and intra-mode action sequencing. We serendipitously detected an additional masseter-related action, tooth-sharpening, identified as bouts of higher-frequency (∼13 Hz) rhythmic masseter activity, which was accompanied by eye displacement, including rhythmic proptosis, attributable to masseter contractions. Collectively, the findings demonstrate how a natural, complex, and goal-oriented activity is organized as an assemblage of distinct modes and complex actions, adapted for the divisions of function arising from anatomical structure. These results reveal intricate, high-speed coordination of disparate effectors, and show how natural forms of dexterity can serve as a model for understanding the behavioral neurobiology of multi-body-part coordination in general.

Significance statement Survival hinges on efficiently handling and ingesting food. During food handling, mice switch between statically holding and actively manipulating food with the hands, and also between biting with the incisors or chewing with the molars. Using masseter electromyography and kilohertz frame rate video, we show that the two modes of hand movement and of jaw movement are tightly linked, with holding co-occurring with chewing and handling with biting. On faster timescales, biting is precisely timed to occur after rapid sequences of manipulative hand movements. Our findings reveal fast, intricate, hierarchical coordination of hand and jaw movements, show how morphology influences the organization of complex behavior, and establish food handling as a model for neurobiological studies of multi-body-part coordination.