Short-Term Monocular Deprivation Enhances Physiological Pupillary Oscillations

Abstract

Short-term monocular deprivation alters visual perception in adult humans, increasing the dominance of the deprived eye, for example, as measured with binocular rivalry. This form of plasticity may depend upon the inhibition/excitation balance in the visual cortex. Recent work suggests that cortical excitability is reliably tracked by dilations and constrictions of the pupils of the eyes. Here, we ask whether monocular deprivation produces a systematic change of pupil behavior, as measured at rest, that is independent of the change of visual perception. During periods of minimal sensory stimulation (in the dark) and task requirements (minimizing body and gaze movements), slow pupil oscillations, “hippus,” spontaneously appear. We find that hippus amplitude increases after monocular deprivation, with larger hippus changes in participants showing larger ocular dominance changes (measured by binocular rivalry). This tight correlation suggests that a single latent variable explains both the change of ocular dominance and hippus. We speculate that the neurotransmitter norepinephrine may be implicated in this phenomenon, given its important role in both plasticity and pupil control. On the practical side, our results indicate that measuring the pupil hippus (a simple and short procedure) provides a sensitive index of the change of ocular dominance induced by short-term monocular deprivation, hence a proxy for plasticity.

Short-term plasticity of the human adult visual cortex measured with 7T BOLD

“…In line with previous studies (26,27,29,30,43), short-term monocular contrast deprivation induced a 30% increase of phase duration for the deprived eye (POST to PRE-deprivation ratio: 1.30 ± 0.31) and a 15% decrease of phase duration for the non-deprived eye (ratio: 0.86 ± 0.31), producing a significant time × eye interaction (Fig. 3A, repeated measure ANOVA on the mean phase durations for each participant, interaction: F(1,17) = 21.40085, p = 0.00024).…”

“…For example, selective deprivation of one cardinal orientation over few hours leads to paradoxically enhanced sensitivity to the deprived orientation (25). Similarly, short-term monocular deprivation leads to a transient boost of the deprived eye responses (26)(27)(28)(29)(30)(31)(32).…”

Neuroplasticity in adult human visual cortex

“…The improvement in visual acuity of about 2 lines lasted for up to one year, indicating long-term neuroplastic changes . Binda & Lunghi (2017) more recently tackled another biomarker of neuroplasticity in adult humans by demonstrating that monocular deprivation affects spontaneous low frequency oscillations of the pupil diameter at rest, a phenomenon called hippus (Diamond, 2001). The authors measured pupillary oscillations before and after monocular occlusion, following the same paradigm as Lunghi et al (2011), and found that hippus amplitude increased after visual deprivation and that participants with more pronounced pupillary fluctuations also showed stronger ocular dominance changes in binocular rivalry dynamics.…”

“…Finally, in light of the recent results by Binda & Lunghi (2017) showing both increased pupillary hippus at rest and enhanced eye-dominance of the deprived eye during binocular rivalry after monocular deprivation, the role of the neurotransmitter norepinephrine (NE) in mediating homeostatic plasticity should be further investigated in adult humans. This neurotransmitter may indeed constitute the common source of visual cortical excitability underlying these phenomena, given its known role in regulating both pupil diameter modulation (Joshi et al, 2016) and visual cortical plasticity (Kasamatsu et al, 1979(Kasamatsu et al, , 1981.…”

“…However, several recent lines of evidence have put this assumption into question: in animal models, ocular dominance plasticity can be reactivated after the closure of the critical period by manipulating the visual cortex excitability, either pharmacologically or through environmental enrichment and physical activity (Baroncelli et al, 2010(Baroncelli et al, , 2012Berardi et al, 2015;Harauzov et al, 2010;He et al, 2006;Hensch and Fagiolini, 2005;Hensch et al, 1998;Maya Vetencourt et al, 2008;Pizzorusso et al, 2002;Sale et al, 2007Sale et al, , 2014Spolidoro et al, 2009). In adult humans, evidence of preserved visual plasticity has been demonstrated by behavioral and neural changes associated with perceptual learning (Beyeler et al, 2017;Dosher and Lu, 2017;Fiorentini and Berardi, 1980;Watanabe and Sasaki, 2015), short term visual deprivation (Binda et al, 2018;Binda and Lunghi, 2017;Lunghi et al, 2011Lunghi et al, , 2013Lunghi et al, , 2015aLunghi et al, ,b, 2018Lunghi and Sale, 2015;Zhou et al, 2013Zhou et al, , 2014, progressive blinding pathologies and visual restoration therapies (Aguirre et al, 2016;Baseler et al, 2011a;Burton, 2003;Castaldi et al, 2016;Cunningham et al, 2015a,b;Dormal et al, 2015;Heimler et al, 2014).…”