One contention within the field of neuroimaging concerns the character of the depicted activity - does it represent neuronal action potential generation, i.e., spiking, or post-synaptic excitation? This question is related to the metabolic costs of different aspects of neurosignaling. The cerebellar cortex is well-suited for addressing this problem, as synaptic input to and spiking of the principle cell, the Purkinje cell (PC), are spatially segregated. Also, PCs are pacemakers, able to generate spikes endogenously. We examined the contributions to cerebellar cortical oxygen consumption (CMRO₂) of post-synaptic excitation and PC spiking during evoked and on-going neuronal activity in the rat. By inhibiting excitatory synaptic input using ionotropic glutamate receptor blockers, we found that the increase in CMRO₂ evoked by parallel fiber (PF) stimulation depended entirely upon post-synaptic excitation. In contrast, PC spiking was largely responsible for the increase in CMRO₂ when on-going neuronal activity was increased by GABA_A receptor blockade. In this case, CMRO₂ increased equally during PC spiking with excitatory synaptic activity as during PC pacemaker spiking without excitatory synaptic input. Subsequent inhibition of action potential propagation and neurotransmission by blocking voltage-gated Na⁺-channels eliminated the increases in CMRO₂ due to PF stimulation and increased PC spiking, but left a large fraction of CMRO₂, i.e., basal CMRO₂, intact. In conclusion, while basal CMRO₂ in anesthetized animals did not seem to be related to neurosignaling, increases in CMRO₂ could be induced by all aspects of neurosignaling. Our findings imply that CMRO₂ responses cannot a priori be assigned to specific neuronal activities.