A key clinical outcome for non-atherosclerotic peripheral vascular disease (PVD) in patients is a progressive decay in skeletal muscle performance and its ability to resist fatigue with elevated metabolic demand. This study builds on previous work to evaluate in situ arteriolar hemodynamics in cremaster muscle of obese Zucker rats (OZR) model of the metabolic syndrome, manifesting a non-atherosclerotic PVD, to integrate existing knowledge into a greater understanding of impaired skeletal muscle perfusion and performance. In OZR cremaster muscle, perfusion distribution at microvascular bifurcations (γ) was consistently more heterogeneous than in controls. However, while consistent, the underlying mechanistic contributors were spatially divergent as altered adrenergic constriction was the major contributor to altered γ at proximal microvascular bifurcations, with a steady decay with distance, while endothelial dysfunction was a stronger contributor in distal bifurcations with no discernible role proximally. Using measured values of γ, simulations predict that successive alterations to γ in OZR caused more heterogeneous perfusion distribution in distal arterioles than in controls; an effect that could only be rectified by combined adrenoreceptor blockade and improvements to endothelial dysfunction. To minimize this negative outcome in spatial perfusion heterogeneity, a likely compensatory mechanism against an increased γ should be an increased temporal switching at arteriolar bifurcations to minimize downstream perfusion deficits. Using the identical in situ cremaster muscle preparation, we determined that temporal activity (the cumulative sum of absolute differences between successive values of γ, taken every 20 seconds) was lower in OZR than in control animals, and this difference was present in both proximal (1A-2A) and distal (3A-4A) arteriolar bifurcations. While adrenoreceptor blockade (phentolamine) improved temporal activity in 1A-2A arteriolar bifurcations in OZR, this was without impact in the distal microcirculation, where only interventions against oxidant stress (TEMPOL) and thromboxane A2 activity (SQ-29548) were effective. Analysis of the attractor for γ indicated that it was not only elevated in OZR as compared to LZR, but also exhibited severe reductions in range. Taken together, these results suggesting that the ability of the microcirculation to respond to any imposed physiological or pathological challenge becomes highly restricted with metabolic syndrome, and may represent the major contributors to the manifestation of poor muscle performance at this age in OZR.