Dim nighttime illumination alters photoperiodic responses of hamsters through the intergeniculate leaflet and other photic pathways

Abstract

In mammals, light entrains the central pacemaker within the suprachiasmatic nucleus (SCN) through both a direct neuronal projection from the retina and an indirect projection from the intergeniculate leaflet (IGL) of the thalamus. Although light comparable in intensity to moonlight is minimally effective at resetting the phase of the circadian clock, dimly lit and completely dark nights are nevertheless perceived differentially by the circadian system, even when nighttime illumination is below putative thresholds for phase resetting. Under a variety of experimental paradigms, dim nighttime illumination exerts effects that may be characterized as enhancing the plasticity of circadian entrainment. For example, relative to completely dark nights, dimly lit nights accelerate development of photoperiodic responses of Siberian hamsters transferred from summer to winter day lengths. Here we assess the neural pathways underlying this response by testing whether IGL lesions eliminate the effects of dim nighttime illumination under short day lengths. Consistent with previous work, dimly lit nights facilitated the expansion of activity duration under short day lengths. Ablation of the IGL, moreover, did not influence photoperiodic responses in animals held under completely dark nights. However, among animals that were provided dimly lit nights, IGL lesions prevented the short-day typical expansion of activity duration as well as the seasonally appropriate gonadal regression and reduction in body weight. Thus, the present data indicate that the IGL plays a central role in mediating the facilitative effects of dim nighttime illumination under short day lengths, but in the absence of the IGL, dim light at night influences photoperiodic responses through residual photic pathways.

Figure 1

Line drawing illustrating the lesion of a representative hamster with a complete ablation of the IGL (area of lesion indicated by dotted line). d = dorsal lateral geniculate nuclei, v = ventral lateral geniculate nuclei.

Figure 2

Representative double-plotted actograms depicting general locomotor activity rhythms of animals transferred from long day (LD 14:10) to short day photoperiods (LD 10:14), with the inset illustrating the results of histological analyses of NPY-ir within the SCN of each animal. Internal shading within center of each actogram indicates the timing of the scotophase (either dimly lit or completely dark). Activity counts were recorded with passive infrared motion detectors (actograms scaled 0 to 5 counts/ 6 min bin).

Figure 3

Short day induced changes in behavioral and physiological measures. A) Weekly measures of activity duration (top) and activity counts (bottom). Week 0 is the last five days under LD 14:10 and Weeks1-8 are under LD 10:14. B) Measures of estimated testes volume (top) and body weight loss (bottom) collected during the eighth week of short day photoperiod.

Figure 4

Variability in the pattern of entrainment displayed by IGL-lesioned animals provided LD 10:14 with dim nighttime illumination. Unlike other groups, the majority of DIM-IGLx animals displayed a short active phase entrained unambiguously to either lights-off (A, 7/19 animals) or lights-on (B, 9/19 animals). Only three DIM-IGLx animals displayed an expansion of activity duration under LD 10:14 (C).