Modulation of visual cortical excitability by working memory: effect of luminance contrast of mental imagery

Abstract

Although much is known about the impact of stimulus properties such as luminance contrast, spatial frequency, and orientation on visually evoked neural activity, much less is known about how they modulate neural activity when they are properties of a mental image held in working memory (WM). Here we addressed this question by investigating how a parametric manipulation of an imagined stimulus attribute affects neuronal excitability in the early visual cortex. We manipulated luminance contrast, a stimulus property known to strongly affect the magnitude of neuronal responses in early visual areas. Luminance contrast modulated neuronal excitability, as assessed by the frequency of phosphenes induced by transcranial magnetic stimulation (TMS) with the exact nature of this modulation depending on TMS intensity. These results point to a strong overlap in the neuronal processes underlying visual perception and mental imagery: not only does WM maintenance selectively engage neurons which are tuned to the maintained attribute (as has previously been shown), but the extent to which those neurons are activated depends on the image contrast (as is the case with visually evoked responses). From a methodological viewpoint, these results suggest that assessment of visual cortical excitability using TMS is affected by the TMS intensity used to probe the neuronal population.

Keywords: excitability; noise; phosphenes; stochastic resonance; visuo-spatial working memory.

Figure 1

Timelines of a TMS trial (above) and of a catch trial (below) in Experiment 1 in the visual imagery condition. The trials in the “Passive viewing” condition had the same structure as the TMS trials. In the “Passive viewing” condition, there were no catch trials and subjects were not asked to maintain a mental image of the grating.

Figure 2

The mean (n = 8) proportion of “Phosphene present” judgments as a function of stimulus contrast (0. 1, 0.5, or 0.9) and task condition (Imagery vs. Passive viewing), collapsed over the three response types which indicate that a phosphene was perceived (i.e., “weak,” “almost clear” and “absolutely clear” on the response scale). TMS was applied at phosphene threshold, which refers to the intensity at which phosphenes are perceived at 50% of trials (i.e., proportion of “phosphene present” trials is 0.5). Overall subjects perceived more phosphenes in the Visual imagery condition compared to the Passive viewing condition. However, grating contrast had no impact. Error bars represent ±1 SEM.

Figure 3

Mean (n = 8) vividness rating for perceived phosphenes in the “Visual imagery condition” (A) and in the “Passive viewing” condition (B) of Experiment 1. Error bars represent ±1 SEM.

Figure 4

Mean (n = 8) proportion of “Phosphene present” judgments in Experiment 2. The measure is collapsed over the three response types which indicate that a phosphene was perceived, i.e., “weak,” “almost clear” and “absolutely clear” on the response scale rating. Error bars represent ±1 SEM. Mental imagery contrast interacted with TMS intensity. When TMS was applied at 90% of PT, significantly more phosphenes were perceived in the high and middle contrast conditions relative to the low contrast condition, indicating that an increase in luminance contrast enhances visual cortical excitability. When TMS was applied at 100% of PT, a significant difference was found between the low and middle contrast conditions, but not between the low and high contrast conditions.

Figure 5

Mean (n = 8) vividness ratings of perceived phosphenes in Experiment 2 for (A) 100% PT condition; and (B) 90% PT condition. Error bars represent ±1 SEM.

Figure 6

Mean (n = 7) proportion of “Phosphene present” judgments in Experiment 3. As in Experiment 2, there was no difference in phosphene frequency between the low and high contrast stimuli when TMS was applied at 100% of phosphene threshold. When TMS was applied at 90% of PT, significantly more phosphenes were perceived during high contrast mental imagery than in the low contrast imagery condition, indicating that an increase in contrast enhanced visual cortical excitability. Error bars represent ±1 SEM.

Figure 7

The mean (n = 11) proportion of “Phosphene present” judgments in Experiment 4. There was no significant difference in the proportion of perceived phosphenes between the “auditory memory” and “passive listening” conditions. This shows that non-visual cognitive load did not modulate the excitability of the visual cortex. Error bars represent ±1 SEM.