Humans accurately judge their direction of heading when translating in a rigid environment, unless independently moving objects (IMOs) cross the observer's focus of expansion (FoE). Studies show that an IMO on a laterally moving path that maintains a fixed distance with respect to the observer (non-approaching; C. S. Royden & E. C. Hildreth, 1996) biases human heading estimates differently from an IMO on a lateral path that gets closer to the observer (approaching; W. H. Warren & J. A. Saunders, 1995). C. S. Royden (2002) argued that differential motion operators in primate brain area MT explained both data sets, concluding that differential motion was critical to human heading estimation. However, neurophysiological studies show that motion pooling cells, but not differential motion cells, in MT project to heading-sensitive cells in MST (V. K. Berezovskii & R. T. Born, 2000). It is difficult to reconcile differential motion heading models with these neurophysiological data. We generate motion sequences that mimic those viewed by human subjects. Model MT pools over V1; units in model MST perform distance-weighted template matching and compete in a recurrent heading representation layer. Our model produces heading biases of the same direction and magnitude as humans through a peak shift in model MSTd without using differential motion operators, maintaining consistency with known primate neurophysiology.