Two components of nocturnal locomotor suppression by light

Abstract

In nocturnal rodents, millisecond light ("flash") stimuli can induce both a large circadian rhythm phase shift and an associated state change from highly active to quiescence followed by behavioral sleep. Suppression of locomotion ("negative masking") is an easily measured correlate of the state change. The present mouse studies used both flashes and longer light stimuli ("pulses") to distinguish initiation from maintenance effects of light on locomotor suppression and to determine whether the locomotor suppression exhibits temporal integration as is thought to be characteristic of phase shift responses to pulse, but not flash, stimuli. In experiment 1, locomotor suppression increased with irradiance (0.01-100 microW/cm( 2)), in accordance with previous reports. It also increased with stimulus duration (3-3000 sec), but interpretation of this result is complicated by the ability of light to both initiate and maintain locomotor suppression. In experiment 2, an irradiance response curve was determined using a stimulus series of 10 flashes, 2 msec each, with total flash energy varying from 0.0025 to 110.0 J/m(2). This included a test for temporal integration in which the effects of two equal energy series of flashes that differed in the number of flashes per series (10 vs 100), were compared. The 10 flash series more effectively elicited locomotor suppression than the 100 flash series, a result consistent with prior observations involving flash-induced phase shifts. In experiment 3, exposure of mice to an 11-h light stimulus yielded irradiance-dependent locomotor suppression that was maintained for the entire stimulus duration by a 100-microW/cm(2) stimulus. Light has the ability to initiate a time-limited (30-40 min) interval of locomotor suppression (initiation effect) that can be extended by additional light (maintenance effect). Temporal integration resembling that seen in phase-shifting responses to light does not exist for either phase shift or locomotor suppression responses to flashes or for locomotor suppression responses to light pulses. The authors present an alternative interpretation of data thought to demonstrate temporal integration in the regulation of phase shift responses to light pulses.

Figure 1

Running patterns of mice following light exposure for 3, 30, 300 or 3000 sec at (A) 100 μW/cm²; (B) 10 μW/cm²; (C) 1 μW/cm²; and (D) 0.1 μW/cm². Plot (A) also includes results for an no-light control condition (solid line without symbol; N=24). The data obtained with 0.01 μW/cm² light are not shown, but were similar to those exposed to 0.1 μW/cm². The median wheel revolutions during each 5 min interval is shown as a percentage of baseline wheel revolutions. Time 0 = onset of the light stimulus. The legend in (D) applies to panels (A–D).

Figure 2

Locomotor suppression, calculated as zero minutes over a 70 min interval beginning with stimulus onset varies with both irradiance and duration. Results for all combinations of stimulus irradiance and duration are shown except those involving irradiances of 0.1 or 0.01 μW/cm² which failed to induce locomotor suppression regardless of duration. Numbers indicate stimulus durations in seconds.

Figure 3

Zero minutes from Fig. 2 plotted relative to stimulus energy (J/m²). The solid line represents the best fit described by a 4 parameter logistic equation based on the Marquardt-Levenberg algorithm (SigmaPlot v. 9.02).

Figure 4

Effect of stimulus duration on locomotor suppression as measured by the zero counts during a 40 min interval beginning at the termination of the light stimulus. The figure shows that post-stimulus locomotor suppression is greater with higher irradiances, but long stimuli tend to induce less post-stimulus suppression than shorter stimuli.

Figure 5

Locomotor suppression in response to 100 flashes is not the same as the response to 10 flashes despite the two flash series having equal energy indicating that normal photon integration is absent. Treatment labels indicate the number of flashes and total energy received. Each group differs significantly from the other groups.

Figure 6

Locomotor activity remains suppressed in irradiance-dependent fashion by light administered across the night. (A,B) Patterns of locomotor activity in response to difference irradiances which lasted 11 hr beginning at ZT13. (C) Wheel revolutions in response to the various irradiances. Groups bearing common letter identifiers do not differ.