Friday 31 January 2014

Research Briefing: Does TMS-induced ‘blindsight’ rely on ancient reptilian pathways?

Source Article: Allen C.P.G., Sumner P., & Chambers C.D. (2014). Timing and neuroanatomy of conscious vision as revealed by TMS-induced blindsight. Journal of Cognitive Neuroscience, in press.  [pdf] [study data]  


One of the things I find most fascinating about cognitive neuroscience is the way it is shaping our understanding of unconscious sensory processing: brain activity and behaviour caused by imperceptible stimuli. Lurking below the surface of awareness is an army of highly organised activity that influences our thoughts and actions.

Unconscious systems are, by definition, invisible to our own introspection but that doesn’t make them invisible to science. One simple way to unmask them is to gradually weaken an image on a computer screen until a person reports seeing nothing. Then, when the stimulus is imperceptible, you ask the person to guess what type of stimulus it is, for instance, whether it is “<” or “>”. What you find is that people are remarkably good at telling the difference. They’ll insist they see nothing yet correctly discriminate invisible stimuli much higher than predicted by chance – often at 70-80% correct. It’s really quite head-scratching.

Back in the 1970s, a psychologist named Larry Weiskrantz found that this contrast between conscious and unconscious processing was thrown into sharp relief following damage to a part of the brain called the primary visual cortex (V1). Weiskrantz (and later others) found that patients with damage to V1 would report being blind to one part of their visual field, yet, when push came to shove, they could discriminate stimuli above chance or even navigate successfully around invisible objects in a room. He coined this intriguing phenomenon “blindsight”.

Since then, blindsight has drawn the attention of psychologists, neurologists and philosophers. One of the major debates in the literature has centred on the neurophysiology of the phenomenon: how, exactly, is this unconscious vision achieved? Blindsight proved that information was somehow influencing behaviour without being processed by V1.

Two schools of thought took shape. One argued that, during blindsight, unconscious information reached higher brain systems by activating spared islands of cortex near the damaged V1. An opposing school argued that the information was taking a different road altogether: an ancient reptilian route known as the retinotectal pathway, which bypasses visual cortex to reach frontal and parietal regions.

In our latest study, published in the Journal of Cognitive Neuroscience, we sought to pit these accounts against each other by generating blindsight in healthy people with transcranial magnetic stimulation (TMS). The study was originally conceived by Chris Allen, then a PhD student in my lab and now a post-doctoral researcher. We hadn’t used TMS like this before but we knew from the work of Tony Ro’s lab that it could be done with a particularly powerful type of TMS coil.

Knocking out conscious awareness with TMS was one thing – and apparently doable – but how could we tell which brain pathways were responsible for whatever visual ability was left over? Fortunately I’d recently moved to Cardiff University where Petroc Sumner is based. Some years earlier, Petroc had developed a clever technique to isolate the role of different visual pathways by manipulating colour. When presented under specific conditions, these coloured stimuli activated a type of cell on the retina that has no colour-opponent projections to the superior colliculus. These stimuli, known as “s-cone stimuli”, were invisible to the retinotectal pathway (1). We teamed up with Petroc, and Chris set about learning how to generate these stimuli.

Now that we had a technique for dissociating conscious and unconscious vision (TMS), and a type of stimulus that bypassed the retinotectal pathway, we could bring them together to contrast the competing theories of blindsight. Our logic was this: if the retinotectal pathway is a source of unconscious vision then blindsight should not be possible for s-cone stimuli because, for these stimuli, the retinotectal pathway isn’t available. On the other hand, if blindsight arises via cortical routes at (or near) V1 then blocking the retinotectal route should be inconsequential: we should find the same level of blindsight for s-cone stimuli as for normal stimuli (2).

There were other aspects to the study too (including an examination of the timecourse of TMS interference), but our main result is summarised in the figure below. When we delivered TMS to visual cortex about a tenth of a second after the onset of a normal stimulus, we found textbook blindsight: TMS reduced awareness of the stimuli while leaving unaffected the ability to discriminate them on ‘unaware’ trials. 

Crucially, we found the same thing for s-cone stimuli: blindsight occurred even for these specially coloured stimuli that bypass the retinotectal route. Since blindsight occurred for stimuli that weren’t processed by the retinotectal pathway, our results allow us to reject the retinotectal hypothesis in favour of the cortical hypothesis. This suggests that blindsight in our study arose from unperturbed cortical systems rather than the reptilian route.

Our key results. The upper plot shows conscious detection performance when TMS was applied to visual cortex at 90-130 milliseconds after a stimulus appeared. Compared to "sham" (the control TMS condition), active TMS reduced conscious detection for both the normal stimuli and S-cone stimuli that bypass the retinotectal pathway. The lower plot shows the corresponding results for discrimination of unaware stimuli; that is, how accurately people could distinguish "<" from ">" when also reporting that they didn't see anything. For for both normal stimuli and S-cone, this unconscious ability was unaffected by the TMS. And because this TMS-induced blindsight was found for stimuli that bypass the retinotectal route, we can conclude that the retinotectal pathway isn't crucial for blindsight found here.

While the results are quite clear there are nevertheless several caveats to this work. There is evidence from other sources that the retinotectal pathway can be important and our results don’t explain all of the discrepancies in the literature. What we do show is that blindsight can arise in the absence of afferent retinotectal processing, which disconfirms a strong version of the retinotectal hypothesis.

Also, we don’t know whether the results will translate to blindsight in patients following permanent injury. TMS is a far cry from a brain lesion – unlike brain damage, it is transient, safe and reversible, which of course makes it highly attractive for this kind of research but also distances it from work in clinical patients. Furthermore, even though we can rule out a role of the retinotectal pathway in producing blindsight as shown here, we don’t know which cortical pathways did produce the effect. 

Finally, our paper reports a single experiment that has yet to be replicated – so appropriate caution is warranted as always.

Still, I’m rather proud of this study. I take little of the intellectual credit, which belongs chiefly to Chris Allen. Chris brought together the ideas and tackled the technical challenges with a degree of thoroughness and dedication that he’s become well known for in Cardiff. This paper – his first as primary author – is a nice way to kick off a career in cognitive neuroscience.

1. By “afferent” I mean the initial “feedforward” flow of information from the retina. It’s entirely possible (and likely) that s-cone stimuli activate retinotectal structures such as the superior colliculus after being processed by the visual cortex and then feeding down into the midbrain. What’s important here is that s-cone stimuli are invisible to the retinotectal pathway in that initial forward sweep. 

2. Stats nerds will note that we are attempting to prove a version of the null hypothesis. To enable us to show strong evidence for the null hypothesis, we used Bayesian statistical techniques developed by Zoltan Dienes that assess the relative likelihood of H0 and H1.


  1. Curious to know how your work (above) squares with that of Lloyd, D. A., Abrahamyan, A., & Harris, J. A. (2013). Brain-stimulation induced blindsight: unconscious vision or response bias?. PloS one, 8(12), e82828.

  2. Interesting question. I'd like to make a few points in response:
    - The above study did apply signal detection theory (SDT) as suggested by Lloyd et al and still finds differences.
    - Lloyd et al draw almost all there conclusions on the basis of null/non-significant t-test or ANOVAs (sometime with p values at 0.07!) which do not allow for such conclusions (should have used Bayesian stats). Also they do present some evidence for unconscious processing and a dissociation between the effects of TMS.
    - I think Lloyd et al.'s application of SDT is highly questionable: imbalances in stimulus present /absent conditions calls into question the assumption of normality - A problem which exacerbates the issue of the non-linearity of z-transforms when dealing with low numbers of false alarms (which are presumably lower under the YN condition, although information not presented). Also the claim of Lloyd et al is that many of the differences observed can be accounted for by criteria/bias, yet even though the data is available to them, they do not analyse such differences (e.g. in the form of c, or beta or Br type measures).
    -The interpretation offered by Lloyd et al seems to me to be based on a misunderstanding, or at least a selective reading, of the literature (e.g. review see Seth Dienes Cleeremans Overgaard Pessoa, TICS, 2008 or more foundational texts in consciousness research like Dennett 1991 or Varela Thompson Rosch 1991), in that it does not seem to respect the difference (and epistemic referent) of subjective and objective measures. A fluctuation in criteria can be taken to reflect a change in subjective state (awareness) which may be independent of residual capacity. An example of the confusion can be found in the last sentence of Lloyd et al where the suggestion is made that a measure of awareness should be independent of subjective experience!
    Thanks for the question.
    Chris Allen.

  3. Interesting study. I'm curious about figure D: am I correct in interpreting this as meaning that people has as much blindsight in the sham condition as they had in the experimental condition? In both conditions it seems that their correct identification, when the stimulus was 'unseen' is similar.

    1. Hi - thanks for commenting. It's true that their unseen discrimination performance didn't differ between sham vs active TMS, for either s-cone stimuli or for luminance stimuli (the two lower graphs). But I wouldn't say that participants therefore had as much blindsight in the sham condition as the active condition. Blindsight, as defined here, is the consequence of interfering with the visual cortex and is only measurable in a TMS experiment through the contrast of active vs. sham. In other words, there can be no blindsight at all in the sham condition because sham TMS doesn't interfere with visual cortex.