Validation of a multiscale Hill-type actuator against comprehensive benchmarks of motor unit and muscle force measurements

Computational Hill-type muscle models are widely used to simulate muscle force production because of their efficiency and physiological interpretability. However, their formulation relies on limiting assumptions, including debated multiscale simplifications, a simplified excitation-activation dynamics and an inability to capture slow and fast fibres. Moreover, existing Hill-type models remain insufficiently validated across physiological scales, fibre types, and contraction modes. We addressed these limitations by developing a multiscale fibre-type specific Hill-type neuromuscular actuator with mechanistic excitation-activation dynamics and systematically validated it against comprehensive experimental benchmarks. The model built upon a previously proposed motoneuron-driven actuator incorporating calcium-kinetics-based activation dynamics. The excitation-activation formulation was further refined to strengthen its physiological basis, while the contraction dynamics was extended by including an activation- and length-dependent force-velocity relationship, elastic tendon, passive elastic element, and the fibre-type-specific effects of yielding and sag. Validation was performed against four benchmark datasets spanning motor-unit and whole-muscle scales, including slow and fast fibres under both isometric and dynamic conditions. Experimental force traces were obtained from six muscles of rats and cats using a broad range of stimulation frequencies, muscle lengths, and imposed length changes, combining previous literature datasets with experiments performed ad hoc for this study. Overall, the model reproduced forces across all benchmark conditions, with mean absolute errors typically below 15% of the maximum isometric force, although larger errors were observed in specific submaximal and dynamic trials. The inclusion of physiologically based excitation-activation dynamics, together with yielding and sag, improved model performance under submaximal activation conditions. This study presents the first systematic validation of a single multiscale Hill-type neuromuscular actuator against comprehensive experimental motor unit and muscle force data, providing a benchmark framework for the development and assessment of future models. Author summarySkeletal muscles generate force through a complex sequence of events that links neural signals to muscle contraction. Because direct measurements are difficult to obtain, researchers often rely on computer models to investigate neuromuscular function and estimate muscle forces. However, most modelling approaches rely on simplifying assumptions about how force is generated across different biological scales, how muscles are activated, and how slow and fast muscle fibres behave. Moreover, they have not been validated against comprehensive experimental data. As a result, it remains unclear how accurately these models can reproduce muscle force across different physiological conditions. In this study, we established the first comprehensive set of experimental benchmarks spanning both motor-unit and whole-muscle scales, including slow and fast muscles under isometric and dynamic conditions. We used these benchmarks to validate a newly developed multiscale muscle model that explicitly represents the physiological pathway from neural stimulation to force production. The model incorporates experimentally based descriptions of calcium dynamics, activation, tendon elasticity, and fibre-type-specific contractile properties. We then compared simulated and experimental force responses across a wide range of stimulation frequencies, muscle lengths, and length-change conditions.