Behavioural, pupillometric and imaging evidence of experience-dependent changes in visual perception

This thesis presents four experiments involving adult human participants, where we combined a range of techniques (psychophysics, pupillometry and neuroimaging) to explore the many ways in which sensory processing adapts to the context, as set by behavioural goals (attention) or experience (sensory deprivation). Chapter 1 (General Introduction) presents our main methodological tools: binocular rivalry, the classical paradigm to investigate ocular dominance and binocular vision; pupillometry, a non-invasive technique to index the strength of visual representations; monocular deprivation, a standard paradigm to boost or suppress visual cortical representations; and functional MRI (magnetic resonance imaging), which allowed us to study the functional connectivity of the visual brain at rest. In chapter 2, we analyzed the reliability of a set of indices that may be extracted from binocular rivalry and have been traditionally associated with a variety of perceptual and cognitive functions. On the one hand, our findings advise caution when interpreting the association between stable psychological characteristics (e.g., personality traits) and the rate of switching or the probability of fused percepts, given the state-dependent variability of these parameters. On the other hand, they provide strong support for the use of binocular rivalry to track ocular dominance, given the excellent stability and reliability of this parameter. Chapter 3 proceeded to using this binocular rivalry-based index of ocular dominance for investigating the effects of endogenous cueing. We combined this with a pupillometry measurement, to objectively index the dominance of the two stimuli during rivalry. We found that attention biases binocular rivalry dynamics, boosting the dominance of the cued stimulus; however, it does not enhance the associated pupil response. These results are consistent with two interpretations. One possibility is that attention biases rivalry dynamics without affecting the perceptual representation of the stimuli, but merely shifting the decision criterion that participants use for reporting their percepts. Another possibility is that attention does affect the perceptual representation of the cued stimulus, but only when there is competition between the two stimuli (e.g., during mixed percept, when we do see a transient pupil-size modulation); once one of the two stimuli has gained exclusive perceptual dominance, there is no more room for attention to enhance or suppress visual representations. Preliminary evidence against this second possibility was acquired in Chapter 4, which used the same 3 combined paradigm to investigate the perceptual consequences of short-term sensory deprivation. Two hours of monocular deprivation reliably boosted the dominance of the stimuli in the deprived eye, replicating previous studies and altering rivalry dynamics in a way that was qualitatively similar to the effects of endogenously cueing attention. However, contrary to what was found with attention cueing, here we observed that the perceptual boost was accompanied by a measurable change in the associated pupil responses. Thus, sensory deprivation had an effect on the dynamics of binocular rivalry that, unlike the effect of attention cueing, was faithfully reflected by the pupil-size modulations. This supports the concept that short-term sensory deprivation reliably, although transiently, affects the strength of visual representations, boosting visually evoked responses to stimuli in the deprived eye in a way that is reflected in perception as well as in basic visually evoked responses like pupil-size modulations. Chapter 5 showed that the effects of sensory deprivation extend beyond perceptual dynamics and visually evoked responses, influencing the functional connectivity of the visual brain at rest. In a series of fMRI tests, we found that 2h of monocular deprivation were sufficient to reduce the functional connectivity of the visual cortex with the ventral pulvinar, while leaving the connectivity with the lateral geniculate nucleus unaltered. We propose that this reflects a reconfiguration of the flow of information within the visual system, which could change the way bottom-up sensory evidence (sensory input) is combined with top-down predictions (what we expect to see, which may be carried through cortico-pulvino-cortical connections). As discussed in Chapter 6 (general discussion), this provides initial evidence for the pathway through which contextual factors could affect sensory evidence – without interfering with the first swipe of signals from the periphery through the sensory cortex but modulating the recurrent exchange of information across brain areas, which combines sensory data with a priori information.