Adaptive changes in visual cortex following prolonged contrast reduction

Abstract

How does prolonged reduction in retinal-image contrast affect visual-contrast coding? Recent evidence indicates that some forms of long-term visual deprivation result in compensatory perceptual and neural changes in the adult visual pathway. It has not been established whether changes due to contrast adaptation are best characterized as "contrast gain" or "response gain." We present a theoretical rationale for predicting that adaptation to long-term contrast reduction should result in response gain. To test this hypothesis, normally sighted subjects adapted for four hours by viewing their environment through contrast-reducing goggles. During the adaptation period, the subjects went about their usual daily activities. Subjects' contrast-discrimination thresholds and fMRI BOLD responses in cortical areas V1 and V2 were obtained before and after adaptation. Following adaptation, we observed a significant decrease in contrast-discrimination thresholds, and significant increase in BOLD responses in V1 and V2. The observed interocular transfer of the adaptation effect suggests that the adaptation has a cortical origin. These results reveal a new kind of adaptability of the adult visual cortex, an adjustment in the gain of the contrast-response in the presence of a reduced range of stimulus contrasts, which is consistent with a response-gain mechanism. The adaptation appears to be compensatory, such that the precision of contrast coding is improved for low retinal-image contrasts.

Figure 1

Two potential mechanisms describing effects of prolonged contrast adaptation on Threshold vs. Contrast (TvC) functions and Contrast Response Functions (CRF): (A) TvCs; (B) CRF Contrast gain; (C) Response gain. Dotted lines indicate before adaptation, dashed line for contrast-gain and solid line for response-gain.

Figure 2

Schematic diagram of experimental design.

Figure 3

A schematic diagram of one trial in the contrast-discrimination task.

Figure 4

A schematic diagram of the block design for the fMRI contrast response task. The top panel (a) depicts the block design for one scan. The bottom panel (b) depicts the sequence of two test trials.

Figure 5

Simultaneous fits to group averaged TvCs and fMRI CRFs in V1 and V2 respectively. Both TvC and CRF data are from the pre-test condition of the main experiment. (A) TvC. Discrimination thresholds (%) are plotted as a function of filtered pedestal contrast in log-log coordinates. Each data point represents the geometric mean of threshold estimates across subjects (n = 3); (B) fMRI CRF in V1; (C) fMRI CRF in V2, averaged across subjects (n = 3). The fMRI BOLD signal changes (%) are plotted as a function of filtered stimulus contrast in linear-log coordinates. The error bars represent 1 SEM. Note: The filtered contrast denotes the stimulus contrast taking into account attenuation by the contrast-reducing goggles. It is obtained by dividing the stimulus contrast on screen by a factor of 3.

Figure 6

Difference values (bar height) between pre- and post-tests as a function of stimulus contrast (first column for the main experiment and second column for the control experiment): TvCs (first row), CRFs in V1 (second row), and CRFs in V2 (third row). The horizontal dashed lines represent no pre-post difference (value of 0). The error bars represent 1 SEM.

Figure 7

TvCs and fMRI BOLD CRFs (Top panels: main experiment, Bottom panels: control experiment): (A) TvC functions, averaged across subjects (n = 3). Discrimination thresholds (%) are plotted as a function of filtered pedestal contrast in log-log coordinates. Each panel contains two TvC functions, one from the pre-test (open squares), and one from the post-test (closed circles); (B) fMRI BOLD CRFs in V1 and (C) V2, averaged across subjects (n = 3). The fMRI BOLD signal changes (%) are plotted as a function of filtered stimulus contrast in linear-log coordinates. The open squares represent the CRF from the pre-test and the closed circles for the CRF from the post-test. The error bars represent 1 SEM. Smooth curves are the predictions of the best fitting model (i.e., response gain).

Figure 8

Contrast discrimination functions showing that the adaptation effect exhibits interocular transfer. Each panel shows data from one subject and contains two TvC functions measured in the eye that is occluded by a translucent occluder during the four-hour adaptation period: one from the pre-test (dotted line with open squares) and the other from the post-test (solid line with closed circles). Each data point represents the geometric mean of four threshold estimates, each derived from a forced-choice staircase. Each error bar represents 1 SEM.