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Studying the neuronal mechanisms underlying bistable perception: the role of adaptation, persistence, and inhibition on perceptual decision

Teresa Sousa1, 2, 3, Alexandre Sayal2, 3, 4, João V. Duarte2, 3, 4, Gabriel N. Costa2, 3, 4, Ricardo Martins2, 3, 4 and Miguel Castelo-Branco2, 3, 4*
  • 1 Coimbra Institute for Biomedical Imaging and Translational Research (CIBIT), University of Coimbra, Portugal
  • 2 Institute of Nuclear Sciences Applied to Health, University of Coimbra, Portugal
  • 3 CNC.IBILI Consortium, University of Coimbra, Portugal
  • 4 Coimbra Institute for Biomedical Imaging and Translational Research (CIBIT), Portugal

Studying the human brain response to shifts in perception provides an insight on the neuronal processes which underlie perceptual decision. Visual ambiguous stimuli are a powerful tool to investigate such processes, since perception varies over time despite the physically unchanging properties of stimuli (1). A classic example of an ambiguous visual stimulus is when two moving gratings are superimposed to form a plaid (2). The perception of a moving plaid switches back and forth between two interpretations: it can be perceived as a single surface with coherent motion or as two surfaces sliding one over the other (incoherent motion). It has been highly discussed whether this phenomenon arises from competition between opposing percepts (3), which might be influenced by mechanisms such as neuronal adaptation, inhibition, and memory (4). Current perceptual stability models consider bistable perception as a result of the interaction between these mechanisms, but the relative contribution of each one is still under debate (5,6). Here, we explore how each of these contributes to perceptual decision during bistable visual perception of moving plaids, taking into account the possible interaction between them. We hypothesized that the crucial role of adaptation in perceptual bistability (7–9) arises from its influence on other mechanisms, such as perceptual persistence (a special form of short term visual memory) and inhibition. Based on a set of three functional Magnetic Resonance Imaging (fMRI) experiments, we first tested for distinct levels of adaptation during visual motion perceptual bistability. Then, we investigated how such adaptation competes with persistence to influence perceptual experience. Finally, we tested whether cross-inhibitory effects occur between bistable percepts of a moving plaid, elicited by adaptation. We found that adaptation can contribute to regulating percept duration during visual bistability, with distinct weights, depending on the type of percept (10). Our results provide further evidence for continuous competition between adaptation and persistence, with a relevant role for perceptual experience. Finally, we demonstrated, both at the behavioral and neuronal level, that inhibition plays a key role in the disambiguation of moving plaids. Taken together, our findings add to the understanding of how the visual system achieves perceptual decisions based on interactions between low and high-level neuronal mechanisms.

Acknowledgements

This research work was funded by the Portuguese Foundation for Science and Technology (FCT) (grants: COMPETE UID/NEU/04539/2013, COMPETE POCI-01-0145-FEDER-007440), BIGDATIMAGE project (CENTRO-01-0145-FEDER-000016) and BIAL project 207/16.

References

1. Parker, A. J. & Krug, K. Neuronal mechanisms for the perception of ambiguous stimuli. Curr. Opin. Neurobiol. 13, 433–439 (2003). 2. Adelson, E. H. & Movshon, J. A. Phenomenal coherence of moving visual patterns. Nature 300, 523– 525 (1982). 3. Leopold, D. A. & Logothetis, N. K. Multistable phenomena: Changing views in perception. Trends Cogn. Sci. 3, 254–264 (1999). 4. Wang, M., Arteaga, D. & He, B. J. Brain mechanisms for simple perception and bistable perception. Proc. Natl. Acad. Sci. (2013). 5. Sterzer, P., Kleinschmidt, A. & Rees, G. The neural bases of multistable perception. Trends Cogn. Sci. (2009). 6. Brascamp, J., Sterzer, P., Blake, R. & Knapen, T. Multistable Perception and the Role of Frontoparietal Cortex in Perceptual Inference. Annu. Rev. Psychol. 69, (2018). 7. Kohn, A. & Movshon, J. A. Adaptation changes the direction tuning of macaque MT neurons. Nat. Neurosci. 7, 764–772 (2004). 8. Long, G. M. & Toppino, T. C. Enduring Interest in Perceptual Ambiguity: Alternating Views of Reversible Figures. Psychol. Bull. 130, 748–768 (2004). 9. Patterson, C. A., Wissig, S. C. & Kohn, A. Adaptation Disrupts Motion Integration in the Primate Dorsal Stream. Neuron 81, 674–686 (2014). 10. Sousa, T. et al. Evidence for distinct levels of neural adaptation to both coherent and incoherently moving visual surfaces in visual area hMT+. Neuroimage 179, 540–547 (2018).

Keywords: Ambiguous visual motion, perceptual bistability, perceptual decision, visual motion integration, fMRI, Ambiguous visual motion, perceptual bistability, perceptual decision, Visual motion integration, fMRI

Conference: XVI Meeting of the Portuguese Society for Neuroscience (SPN2019), Lisboa, Portugal, 30 May - 1 Jun, 2019.

Presentation Type: Pitch communication + Poster presentation

Topic: Sensory Processing

Citation: Sousa T, Sayal A, Duarte JV, Costa GN, Martins R and Castelo-Branco M (2019). Studying the neuronal mechanisms underlying bistable perception: the role of adaptation, persistence, and inhibition on perceptual decision. Front. Cell. Neurosci. Conference Abstract: XVI Meeting of the Portuguese Society for Neuroscience (SPN2019). doi: 10.3389/conf.fncel.2019.01.00045

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Received: 16 Apr 2019; Published Online: 27 Sep 2019.

* Correspondence: MD, PhD. Miguel Castelo-Branco, Coimbra Institute for Biomedical Imaging and Translational Research (CIBIT), Coimbra, Coimbra, Portugal, mcbranco@fmed.uc.pt