Learning and Timing of Voluntary Blink Responses Match Eyeblink Conditioning

Abstract

Can humans produce well-timed blink responses to a neutral stimulus voluntarily, without receiving any blink-eliciting, unconditional, stimulus? And if they can, to what degree does classical eyeblink conditioning depend on volition? Here we show that voluntary blink responses learned in two paradigms that did not involve any unconditional blink-eliciting stimuli, display timing that is as good, or better than, the timing of blink responses learned in a standard eyeblink conditioning paradigm. The exceptional timing accuracy likely stems from the fact that, in contrast to previous studies, we challenged our participants to blink in a timed manner, and not merely to blink so as to avoid the corneal air puff. These results reveal a remarkable level of voluntary control over a simple movement, and they challenge the view that learning during eyeblink conditioning is necessarily automatic and involuntary.

Figure 1

Experimental protocol. First, participants were trained to produce accurately timed blinks voluntarily (light and dark blue) in response to a tone, using visual feedback or a click sound. The target time was first 300 ms and then 500 ms, or vice versa. After each voluntary training session (40 trials), the participants were instructed to continue to blink to the tone with the same delay, but without the feedback. Next, participants were trained in a standard eyeblink conditioning protocol (light and dark red) with the same two intervals. Training consisted of 50 trials with 20 percent probes, followed by 10 tone only trials. In the last ten trials participants were instructed to blink as rapidly as possible.

Figure 2

Learning curves. (a–d) Percentage of blink responses in successive blocks of five trials, that would be categorized as conditioned responses (CRs) according to standard criteria (a blink starting later than 150 ms after tone onset and before the target time or time of the air puff). The break in the lines indicate where Click or Visual feedback was ceased (a and c), or when the air puff was no longer delivered (b and d).

Figure 3

Timing of blink responses. (a,b) Learning of voluntary response timing. Average (mean ± SEM) difference between the target time and the peak of the blink response for the delayed visual feedback paradigm and the click paradigm. (c) Response timing (mean ± SEM) on randomly interspersed probe trials during training and on the 10 CS alone trials after training in the standard eyeblink. (d–g) Comparison of blink responses on CS alone trials after training in a voluntary paradigm (dark and light blue) and a standard eyeblink conditioning paradigm (red and pink).

Figure 4

Timing comparisons. (a) Top: Two blink responses produced after training in the click paradigm with two different delays, 300 ms (light-blue) and 500 ms (dark-blue). Green and red markers denote the identified onset and peak respectively. Bottom: Boxplots illustrating the timing of the peak in the different paradigms. (b) The timing error variability on CS alone trials for the different training paradigms and target times.