Increased visual sensitivity following periods of dim illumination

Abstract

Purpose: We measured changes in the sensitivity of the human rod pathway by testing visual reaction times before and after light adaptation. We targeted a specific range of conditioning light intensities to see if a physiological adaptation recently discovered in mouse rods is observable at the perceptual level in humans. We also measured the noise spectrum of single mouse rods due to the importance of the signal-to-noise ratio in rod to rod bipolar cell signal transfer.

Methods: Using the well-defined relationship between stimulus intensity and reaction time (Piéron's law), we measured the reaction times of eight human subjects (ages 24-66) to scotopic test flashes of a single intensity before and after the presentation of a 3-minute background. We also made recordings from single mouse rods and processed the cellular noise spectrum before and after similar conditioning exposures.

Results: Subject reaction times to a fixed-strength stimulus were fastest 5 seconds after conditioning background exposure (79% ± 1% of the preconditioning mean, in darkness) and were significantly faster for the first 12 seconds after background exposure (P < 0.01). During the period of increased rod sensitivity, the continuous noise spectrum of individual mouse rods was not significantly increased.

Conclusions: A decrease in human reaction times to a dim flash after conditioning background exposure may originate in rod photoreceptors through a transient increase in the sensitivity of the phototransduction cascade. There is no accompanying increase in rod cellular noise, allowing for reliable transmission of larger rod signals after conditioning exposures and the observed increase in perceptual sensitivity.

Keywords: hypersensitivity; phototransduction; rod vision; rods; scotopic sensitivity.

Figure 1

The setup and procedure for psychophysical reaction time measurements. (A) The tachistoscope, with beam splitter, presents two channels of visual stimulation. There was a red LED fixation point and a green stimulus LED 20.4° to the temporal side of the visual field. The conditioning background was illuminated by the slide projector, driven on a 3-minute timer. (B) The subject's view, with fixation and stimulus locations overlaid by the conditioning background. The subject did not initiate any trials while the background was on. The background encompassed both the fixation point and the stimulus. (C) Representation of a single reaction time trial. A trial was initiated by a button press, and after a variable preperiod ranging from 300 to 1300 ms, a 5-ms stimulus flash was delivered. The subject released the button when they detected the flash. The time between the midpoint of the stimulus flash and the button release was logged as the reaction time for that trial. 200 to 800 ms after button release, a 1-KHz tone sounded to indicate that the subject could initiate another trial. This tone was delivered with variable timing to prevent subject rhythm. If the subject did not react to the flash delivery, the trial timed out at 1000 ms, and the tone sounded to instruct the subject release the button and begin another trial.

Figure 2

Relationship between reaction time and stimulus intensity. (A) Reaction times plotted against the stimulus intensity for an individual subject over three different days. Reaction time–stimulus curves were tested each day to ensure the test stimulus elicited RTs that were in the right range, as indicated by the black rectangle. The red curve is a power fit to the data of the form f(x) = a(x^b) + c, with constants: a = 0.073, b = −1.06, and c = 349, R² = 0.762. (B) Plotting the average RTs of all nine subjects across all testing days. The red curve is a power fit to the data of the form f(x) = a(x^b) + c, with constants: a = 29.8, b = −0.31, and c = 288, R² = 0.938. Error bars represent ±1 SD. For comparison with luminous intensity, a second axis showing the number of photoisomerizations per rod per flash is given (see Methods section).

Figure 3

Reaction times depend on conditioning background light intensities. (A) An individual subject collected RTs before the onset of a conditioning background (negative time) and immediately after the conditioning background was extinguished (time zero, relative to background offset). At a background intensity of 0.129 cd/m², there was a masking of the stimulus that persisted for ~20 seconds, as the subject did not appear to perceive the test stimulus flashes. (B) When the conditioning background intensity was 10-fold dimmer (0.013 cd/m²), the subject exhibited an initial increase in RT that quickly returned to prebackground levels.

Figure 4

Individual RTs from the subject shown in Figure 2A in both control (A) and test (B) conditions. (A) Individual RT trials are plotted prior to the control period of sustained darkness (negative time) and immediately after the control period (time zero, relative to the end of 3-minute control period). Three different sessions of RTs (1 block/day) were normalized to the mean of the pre-darkness RT trials for each block. (B) Data plotted as in (A) with three different sessions of RTs (three blocks/day), normalized to the mean of the prebackground RT grouping for each block. In the test condition, the subject experienced 3 minutes of a conditioning background (1.29 × 10⁻³ cd/m²) before resuming RT trials. Note that the RTs immediately postbackground are consistently faster than those prebackground.

Figure 5

Average RTs for eight subjects in both control and test conditions. (A) The average RTs from multiple subjects are plotted relative to the onset of the control period (negative time) and immediately after the 3-minute period of sustained darkness (time zero, relative to the end of 3-minute control period). There is no obvious trend when comparing pre- and postdarkness RTs. n = 19 trials in the control conditions. (B) Data are plotted as in (A) before and after a 3-minute conditioning period. An immediate decrease in reaction time is observed that persists for ~15 seconds. The black line fit is a single exponential that with a decay time constant of 7.5 ± 1.3 seconds. n = 54 trials in the test condition. Error bars represent SEM.

Figure 6

Spectral analysis of individual mouse rod photoreceptor noise reveals no significant increase in continuous noise over the range of rod bipolar sampling. (A) An example of physiological data collected from a single mouse rod photoreceptor before (black trace) and immediately after (red trace) exposure to a 3-minute conditioning light exposure. The same 2-ms test flash was delivered at time zero before and after the conditioning exposure, demonstrating the increased magnitude of the light response due to adaptive potentiation. Boxed area indicates data used in FFT noise analysis. (B) Fast Fourier transform spectral analysis of mouse rod recordings (n = 15 cells). The rod to rod bipolar cell synapse has been proposed to act as a bandpass filter of rod membrane voltage changes over the 2- to 5-Hz range (shaded area). The noise collected in darkness (black points) and noise collected immediately after conditioning exposures (red points, AP noise) were not significantly different in 10/13 data points in the rod bipolar sampling range. The blue data represents the instrument noise of the system, in which a rod is exposed to an intense saturating light that closes all the rod membrane channels.