A two-oscillator SCN model with period adaptation and systemic feedback captures photoperiod and T-cycle aftereffects in vivo and in explants

Abstract

Light history leaves persistent changes in circadian period, but where this history is stored remains unresolved. Suprachiasmatic nucleus (SCN) network models have often approached photoperiodic encoding through phase organization or coupling strength. We computationally tested slow adaptation of subregion-specific intrinsic periods as an alternative memory mechanism. The model asymmetrically couples dorsal (D) and ventral (V) SCN oscillators and adds a systemic oscillator (X) representing putative circadian feedback present in vivo but lost ex vivo. With a single parameter set, period adaptation captured the direction and approximate magnitude of behavioral aftereffects across photoperiod and T-cycle conditions. Adapting coupling strength instead of period failed to reproduce the V-leading-D phase order reported after T22. Removing systemic feedback preserved the photoperiod-dependent period ordering but inverted the T22 and T26 aftereffects, an inversion that matched SCN explant observations. The model also yielded distinct D-V phase organization for each of 18:6 LD, T23, and T25. These results suggest that subregion-specific period plasticity provides a parsimonious substrate for encoding light history, while the dependence on systemic feedback indicates that behavioral period may not be a readout of the SCN alone. Graphical Abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=160 SRC="FIGDIR/small/743784v1_ufig1.gif" ALT="Figure 1"> View larger version (33K): org.highwire.dtl.DTLVardef@d48266org.highwire.dtl.DTLVardef@1bd15bdorg.highwire.dtl.DTLVardef@de3d9forg.highwire.dtl.DTLVardef@9fbc39_HPS_FORMAT_FIGEXP M_FIG C_FIG A model with dorsal period adaptation and phenomenological systemic feedback accounts for behavioral and explanted SCN aftereffects. (A) During T22 entrainment, dorsal (D), ventral (V), and systemic (X) oscillators remain phase-locked. After release into constant darkness, systemic coupling maintains a unified in vivo rhythm, whereas removing X feedback in the explant simulation allows the D-V network to express a distinct ex vivo period aftereffect. (B) The SCN model is modeled as an asymmetrically coupled attractive-repulsive oscillator network with stronger photic input to V. Light history is encoded via plasticity of the intrinsic period in D, while X represents putative systemic circadian feedback available in vivo and lacking direct photic input. (C) The model reproduces concordant period changes in behavior and SCN explants across photoperiods, but opposing period changes following T-cycle entrainment.