Cortico-basal ganglia-thalamic (CBT) β oscillations (15–30 Hz) are elevated in Parkinson's disease and correlated with movement disability. To date, no experimental paradigm outside of loss of dopamine has been able to specifically elevate β oscillations in the CBT loop. Here, we show that activation of striatal cholinergic receptors selectively increased β oscillations in mouse striatum and motor cortex. In individuals showing simultaneous β increases in both striatum and M1, β partial directed coherence (PDC) increased from striatum to M1 (but not in the reverse direction). In individuals that did not show simultaneous β increases, β PDC increased from M1 to striatum (but not in the reverse direction), and M1 was characterized by persistent β-high frequency oscillation phase–amplitude coupling. Finally, the direction of β PDC distinguished between β sub-bands. This suggests that (1) striatal cholinergic tone exerts state-dependent and frequency-selective control over CBT β power and coordination; (2) ongoing rhythmic dynamics can determine whether elevated β oscillations are expressed in striatum and M1; and (3) altered striatal cholinergic tone differentially modulates distinct β sub-bands.