Parkinson’s disease (PD), characterized by the absence of dopamine in the striatum, is due to the death of the substantia nigra pars compacta dopamine (SNcDA) neurons in the midbrain. This cell loss is attributed to a dysregulation cascade originating from excess cytosolic dopamine. This presents a paradox. Why is the cytosolic dopamine, while available and in excess, not being released into the striatum and instead causing cell death? Here, we apply our recent theory wherein neurons self-initiate action potentials to maintain metabolic homeostasis. We propose that in PD, such metabolically regulated spikes are diminished and can account for the symptoms of PD and the subsequent cell loss. Neurons, presumably in anticipation of synaptic inputs, keep their ATP levels at a maximum such that they are ATP-surplus/ADP-scarce during synaptic quiescence. When ADP levels are low, ATP production nearly stalls in their mitochondria, leading to the formation of toxic Reactive Oxygen Species(ROS). Under such circumstances, metabolically regulated spikes restore ATP production and preempt ROS toxicity. In a metabolism-coupled computational model of SNcDA that senses ROS and initiates spikes, we identified three categories of failures that would decrease metabolic spikes and thus deplete the dopamine tone. Furthermore, lowered extracellular dopamine causes denovo dopamine synthesis and a disruptive aldehyde as a byproduct, clearing which ultimately leads to cell death. Metabolically regulated spikes, though relevant for cellular health, maybe an integrated neuronal mechanism that operates in synergy with synaptic integration and forms a basic principle of network dynamics and behavior, as exemplified in PD.