Metabolic indices of neuronal activity are thought to predict changes in the frequency of action potentials. There are stimuli that do not shift action potential frequency but change the temporal organization of neuronal firing following modifications of excitatory inputs by inhibitory synaptic activation. To our knowledge it is unknown whether this kind of stimulus associates with adjustments of metabolic markers of neuronal activity. Here, we used the hypothalamic-neurohypophysial system of lactating rats to address whether shifts in the temporal organization of neuronal firing relate with modifications of metabolic markers of neuronal activity. Cytochrome oxidase activity, (3)H-2-deoxyglucose uptake, and the area occupied by blood vessels increased in the paraventricular nucleus and neurohypophysis of lactating rats, as compared with their virgin counterparts. Taken together, these results suggest that metabolic demands denote shifts in the temporal organization of action potentials related with the adjustment of excitatory synaptic activation, and support that changes in metabolic markers do not necessarily reflect shifts in the frequency of action potentials.