(A) Framework of isometric musculotendon simulations. We simulated an in-series muscle-tendon with ends fixed to its initial length. The extrafusal muscle length was shared with the intrafusal muscle fibers, which were activated independently from the extrafusal muscle. (B) Decoupling of intra- and extrafusal force during short isometric contractions. Different combinations of extrafusal (purple bars) and intrafusal (green bars) activation were simulated. Top row contains intra- (green) and extrafusal (purple) stress during these conditions. Middle row is the simulated Ia afferent firing rate, generated by using our mechanistic model simulated driving potential combined with a leaky integrate-and-fire neural model. Extrafusal activation shortens the extrafusal muscle, and in the absence of sufficient intrafusal activation, silences the Ia afferent firing. Intrafusal activation by itself causes the Ia afferent to fire more. When both intra- and extrafusal muscle are activated concomitantly, the relative weighting of activity determines whether the Ia afferent will increase or decrease its firing rate. (C-E) Schematic representation of the multi-scale mechanics responsible for Ia afferent behavior in these simulations. When the effects of extrafusal shortening overpower the effect of fusimotor activity on the spindle, the Ia afferent firing rate decreases, or stops altogether (left, green). When fusimotor activity overpowers the effect of extrafusal shortening on the spindle, the Ia afferent firing rate increases (center, pink). In theory, this suggests there are combinations of fusimotor activity and shortening that will result in no net change to the Ia afferent firing, despite the dynamics of the muscle (right, blue). (F) A spectrum of musculotendon isometric conditions arising from the interplay of extrafusal shortening and intrafusal activation. We activated the musculotendon model with ramp activations and simulated the intrafusal muscle force with and without concomitant gamma activation. When increasing alpha motor neuron drive (purple traces; directionally indicated in all plots by an arrow), extrafusal muscle shortened more (top plot). (G) The passive spindle always decreased its force because of the shortening imposed by the surrounding extrafusal muscle (top plot). When the intrafusal muscle was activated with concomitant drive, similar to the largest amplitude ramp of extrafusal muscle, we observed the spectrum of responses predicted in C-E: the intrafusal force either decreased (green), stayed relatively constant (purple), or increased (pink). (H) Experimental examples of one muscle spindle decreasing its firing rate (top traces) and another increasing its firing rate (bottom traces) during an isometric task in human. Figure 8H is reproduced from Edin and Vallbo, 1990 with permission from The American Physiological Society. It is not covered by the CC-BY 4.0 license and further reproduction of these panels would need permission from the copyright holder.