The parafascicular (PF) thalamic nucleus participates in functions such as arousal, consciousness, learning, and behavioral flexibility, which are linked to its projections to the striatum and receives strong cholinergic input from the pedunculopontine nucleus. Using electrophysiological recordings, we identified two neuronal populations based on their afterhyperpolarization potential (AHP) characteristics: Brief AHP neurons and Prolonged AHP neurons. Only Prolonged AHP neurons were modulated by cholinergic receptor activation, which reduced AHP amplitude and duration, and increased their firing frequency. These effects were associated with SK-type calcium-activated potassium channels and specifically activated by M1 type muscarinic receptors. Together, these findings indicate clear differential cholinergic modulation in the PF thalamic nucleus, which may be related to its functional roles.