The Interhemispheric Switch model of Perceptual Rivalry: More than a decade on.

Our model of the switch has accumulated support in the 14 years since it was proposed¹². Its relevance to psychiatry has been realised in Japan, for example, where the link between a slow switch and bipolar disorder has been replicated, with some new features such as differentiation of the Bipolar subtypes¹, and a new serotonin 1A antagonist has been synthesised with the predicted slowing effect on the switch². The changes that have taken place in the rivalry field in those 14 years include:

. more links between the rivalry switch and emotion;³

. pupillary dilation predicts the timing of an ensuing switch⁴

. accumulating studies of the neuropharmacology of the switch;⁵

. increasing evidence that all perceptual rivalries, including binocular rivalry whose enthusiasts have often maintained its separateness, have a shared underlying switch mechanism despite the differences in cortical areas involved.⁶

On the other hand, despite these advances, a study that I just read refuses to engage the hypothesis⁷, even though it is admirably positioned to do so using TMS, a technique that we used to test the interhemispheric hypothesis successfully in the past¹². The study comes from the lab.of Randolph Blake, who is one of the acknowledged authorities on binocular rivalry. It is therefore disappointing to find this timid avoidance of our hypothesis, as well as misreferences suggesting that they had never actually read the studies on the pharmacology of the switch and its likely common basis to all perceptual rivalries

In the study mentioned⁷, Pearson, Tadin and Blake tried very hard to avoid any features of their experimental design that might reveal the interhemispheric feature that is the key to our model of rivalry! For example, they placed the TMS coil on the midline, specifically “to avoid hemispheric effects”. In addition, they devalued the temporal specificity of TMS by randomising the timing of the delivery of the TMS pulse with respect to the rivalry switch of the volunteer. They justified their effort to eliminate any hemispheric effect on the basis of a famous split brain patient whose reports were inferred to rule out the interhemispheric model of rivalry (by O’Shea and Corballis ⁸). I have already discussed in detail the many problems associated with the interpretation of subjective reports by split brain subjects (as opposed to forced choices). There is also a very common, misguided tendency to latch onto the corpus callosum in the context of our interhemispheric model of rivalry, despite the fact that the clumsy suggested callosal mechanism can easily be ruled out in favour of a sub-cortical one⁹. The Mackays, working with Sperry on game-playing by split-brain observers, put the lie to the notion that the split-brain patients cannot integrate information from both hemispheres into subjective awareness¹⁰. Philosophical-type inferences about the structures involved in conscious awareness, like those made by O’Shea and Corballis¹¹, have to be tempered by evidence from positive interventions, such as unihemispheric TMS and vestibular caloric stimulation, which have specifically tested the interhemispheric switch hypothesis and failed to reject it. The various specific tests of the hypothesis, irrespective of the flawed underlying assumptions of the split-brain study, are to be contrasted with the study by Pearson, Tadin and Blake⁷, who went out of their way to avoid any procedures that might test the hypothesis (e.g. they did not check to see if they could replicate our finding that TMS interference in rivalry is hemisphere- and phase-specific. In other words, the TMS pulse has to be delivered to a specific hemisphere during a specific phase of rivalry). The precise timing that is possible with TMS makes this an attractive possible test. By using midline TMS and randomising timing in relation to the phase of rivalry, the study by Pearson, Tadin and Blake discards these attractive features of the experimental situation, in a stated aim to remain agnostic about the interhemispheric switch model of rivalry! I suppose that one might accept this as a back-handed compliment about a hypothesis that is found to be too intimidating to test.

So there is more than one way to fail replication of the interhemispheric switch hypothesis of rivalry. On the one hand you can make a serious attempt at replication, with careful design and faultless logic, like O’Shea and Corballis, but fail because of a dubious underlying assumption about the split brain state. Alternatively, you can go to some lengths to avoid any experimental conditions that would enable a successful replication, like Pearson, Tadin and Blake, and so fail out of timidity rather than a genuine attempt to test the hypothesis.

Despite efforts by Pearson, Tadin and Blake to ignore the interhemispheric model, their data actually support it. At least, they fail to find any support for their own model where rivalry timing is derived from intrinsic processes from within visual cortical processing networks. This model contrasts with the interhemispheric model, where the timing signal comes from external sources (to whit, the executive network of catecholaminergic and serotoninergic oscillator systems in the midbrain). They found that the TMS effect upon rivalry timing was fixed in an individual as a function of that individual’s genetic propensity to a given switch rate (e.g. longer delay in slow switchers), but was unaffected by visually-stimulated changes in rivalry rate. This indicates a timing mechanism that is independent of those visual cortical processes that determine the quality of the percept, as opposed to the timing of its alternations.

Reference and Notes:

1. Nagamine M, Yoshino A, Miyazaki M, Takahashi Y, Nomura S (2009) Difference in

binocular rivalry rate between patients with bipolar I and bipolar II disorders. Bipolar

Disord 11:539–546.

2. Nagamine M, Yoshino A, Miyazaki M, Takahashi Y, Nomura S (2008) Effects of

selective 5-HT1A agonist tandospirone on the rate and rhythmicity of binocular rivalry.

Psychopharmacology (Berl) 198:279–286

3. Sheppard B. M. and Pettigrew J. D. (2006) Plaid Motion Rivalry: correlates with binocular rivalry and positive mood state. Perception 35(2):157-69

4. Einhäuser, W., Stout, J., Koch, C. & Carter, O. (2008) Pupil dilation reflects perceptual selection and predicts subsequent stability in perceptual rivalry. Proc Natl Acad Sci 105(5): 1704-1709

5. Carter, O., Pettigrew, J., Hasler, F. & Wallis, G., Liu, G. B., Hell, D., & Vollenweider, F. X. (2005) Modulating the rate and rhythmicity of perceptual rivalry alternations with the mixed 5-HT2A and 5-HT1A agonist psilocybin. Neuropsychopharmacology 30: 1154-1162

6. Carter, O., Konkle, T., Wang, Q., Hayward, V. & Moore, C. (2008) Tactile rivalry demonstrated with ambiguous apparent motion quartet. Current Biology 18(4):1050-54

7. Pearson J, Tadin D, Blake R (2007) The effects of transcranial magnetic stimulation on

visual rivalry. J Vis 10.1167/7.7.2.

8. O’Shea R. P., Corballis P. M. (2001). Binocular rivalry between complex stimuli in split-brain observers. Brain and Mind, 2, 151–160.

9. Pettigrew JD (2001) Searching for the switch: Neural bases for perceptual rivalry

alternations. Brain Mind 2:85–118

10. Mackay, D.M. and Mackay, V., 1982: Explicit dialogue between left and right half systems of split brains, Nature 295, 690.

11. I note from his website that Mike Corballis now credits a role for subcortical structures in interhemispheric integration by split br

ain subjects.

12. Miller, SM, Liu, G-B, Ngo T, Carson R, Riek S and Pettigrew JD (2000) Interhemipheric switching mediates perceptual rivalry. Current Biology 10: 383-392

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