The arcuate nucleus of the hypothalamus (ARH) controls rat feeding behavior, in part, through peptidergic neurons projecting to the hypothalamic paraventricular nucleus (PVH). Hindbrain catecholaminergic (CA) neurons innervate both the PVH and ARH, and ablation of CA afferents to PVH neuroendocrine neurons prevents them from mounting cellular responses to systemic metabolic challenges such as insulin or 2-deoxy-D-glucose (2-DG). Here, we asked whether ablating CA afferents also limits their ARH responses to the same challenges or alters ARH connectivity with the PVH. We examined ARH neurons for three features: (1) CA afferents, visualized by dopamine-β-hydroxylase-immunoreactivity (DBH-ir); (2) activation by systemic metabolic challenge, as measured by increased numbers of neurons immunoreactive for phosphorylated ERK1/2 (pERK1/2-ir); and (3) density of PVH-targeted axons immunoreactive for the feeding control peptides Agouti-related Peptide (AgRP) and alpha-melanocyte stimulating hormone (αMSH). Loss of PVH DBH-ir resulted in concomitant ARH reductions of DBH-ir and pERK1/2-ir neurons in the medial ARH, where AgRP neurons are enriched. In contrast, pERK1/2-ir following systemic metabolic challenge was absent in αMSH-ir ARH neurons. Yet surprisingly, axonal αMSH-ir in the PVH was markedly increased in CA-ablated animals. These results indicate: (1) intrinsic ARH activity is insufficient to recruit pERK1/2-ir ARH neurons during systemic metabolic challenges; rather, hindbrain-originating CA neurons are required; and (2) rats may compensate for a loss of CA innervation to the ARH and PVH by increased expression of αMSH. These findings highlight the existence of a hierarchical dependency for ARH responses to neural and humoral signals that influence feeding behavior and metabolism.