The dual-oscillator model, originally proposed as a mechanism for how vertebrates adapt to seasonal changes, has been invoked to explain circadian entrainment in Drosophila melanogaster. Distinct subsets of neurons have been designated as "morning" and "evening" oscillators that function as regulators of rhythmic activity/rest behavior. Some studies have led to a model in which a subset of 8 "morning" cells (4 bilaterally located small ventral lateral neurons) and another subset of approximately 130 "evening" cells exert different levels of dominance within the circadian circuit in different seasons. However, many studies propose a more integrative neuronal network, with the whole network orchestrating activity/rest rhythms in different seasons, as opposed to hierarchical dominance among neurons. Within the circadian network, our understanding of the role of the large ventral lateral neurons (l-LN(v)) has thus far been limited to conveying light information to the clocks and as light-activated neurons mediating arousal. In support of the framework of a more distributed model, we report an important circadian clock-related role for the l-LN(v) in electrical activity-dependent phasing of the evening peak across a range of photoperiods. Further, we propose a model in which l-LN(v) enable adaptation to seasonal changes by regulating the phase of the evening peak. Additionally, we demonstrate a hitherto unknown role for the small ventral lateral neurons (s-LN(v)) in the arousal circuit, thus showing that neuronal function is flexible such that certain neurons can play more than one role in distinct circuits.