The Story Behind the Atlantic Salmon

HBM-SalmonThe Atlantic Salmon fMRI poster has garnered a fair amount of attention since its presentation at the Human Brain Mapping conference last June in San Francisco. So far the reaction from other researchers has been almost unanimously positive. A sizable number of people stopped by the poster while it was displayed and Rainer Goebel (of BrainVoyager fame) was kind enough to give the fish a shout-out during the closing ceremonies (see photo).

All in all I am quite pleased that the Salmon seems to be generating a fresh discussion of multiple comparisons correction in neuroimaging.But, how did it all begin? I mean, really, why would anybody want to scan a fish? This was one of the top five questions I was asked during the HBM poster session. It it a story that deserves to be told, and a weblog post is perhaps the ideal medium to tell it. So, for all readers who are curious, I have written up the story of the Salmon.

The story begins during my first year in graduate school at Dartmouth College. I was working with Abigail Baird on fMRI studies investigating the maturation of decision-making and we were developing a large number of new MRI protocols to use with adolescents and adults. Not wanting to waste valuable magnet time imaging and reimaging a MRI phantom, we instead challenged ourselves to scan the most curious objects we could find at the local grocery store.

For our first attempt we scanned a pumpkin. One result of this endeavor can be seen here. This is a pretty standard fruit to scan, as just about every imaging center around the country obtains a T1-weighted image of them in late October. Still, it was exciting to us. During the next pilot testing session Abby brought in a Cornish game hen to be scanned. This really upped the ante, as we had now put a dead bird into the head coil. When pondering our next step the comment was made: “we should scan a whole fish”.

I picked up the salmon from our local supermarket early on an early Saturday morning in spring of 2005. The clerk behind the counter was a little shocked to be selling a full-length Atlantic salmon at 6:30 AM, especially when I told her what was about it happen to it. About an hour later we were in the imaging center with the fish wrapped in plastic and securely placed within the head coil. We proceeded to test our entire protocol with the salmon in the magnet. In total, we did an anatomical localizer scan, four functional runs, a T1-weighted anatomical scan, and a diffusion tensor imaging (DTI) scan.

After transferring the data off of the scanner we first took a look at the high resolution anatomical image. It was simply incredible. Slice the fish along the sagittal plane and you could see the fish split right down the middle. Slice the fish coronally and you could see what looked like salmon steaks on the viewer. By far it was our crowning achievement in terms of ridiculous objects to scan. Then, our curiosity satisfied, I socked the salmon data away for the next three years.

In early 2008 I was working with my co-adviser George Wolford on a presentation he was giving regarding the multiple comparisons problem in fMRI. We were discussing false positives in MRI phantom data and I brought up the idea of processing the salmon fMRI data to look for some ‘active’ voxels. I ran the fish data through my SPM processing pipelines and couldn’t believe what I saw. Sure, there were some false positives. Just about any volume with 65,000 voxels is going to have some false positives with uncorrected statistics. Rather, it was where the false positives occurred that really floored me. A cluster of three significant voxels were arranged together right along the midline of the salmon’s brain. If they would have been anywhere else the salmon would have been just a curious anecdote, but now we had a story.

Bennett-Salmon-Figure1

George presented the salmon data at our local fMRI methods group, but nothing much happened for a while after that. George was convinced that we could/should publish the data and that it was an excellent example of the multiple comparisons problem. I was less convinced, remarking about how silly that would be and how terrible it would be for a young postdoc to become known as ‘the fish guy’. For the next year we went back and forth about the issue, until one day in January, 2009. George was out in Los Angeles and came up to UCSB to visit. Over lunch he said that it was time to ‘get the fish out’. I relented, and agreed to start writing the paper.

About a week later the HBM conference poster deadline came around and we decided to submit the salmon as an abstract. We genuinely wanted it to be a part of the conference, but we really doubted that it would be approved. How right we were. Through some sources close to the matter I have learned that the salmon poster was indeed rejected by every reviewer who saw the abstract. Just about everyone thought it was a joke – some rogue student who was playing a prank on the OHBM. It was only when the rejected abstract went before the OHBM Program Committee that it was given approval to stay as part of the conference. I hear that even that vote was contentious.

While the abstract reviewers were busy rejecting the salmon poster my co-authors and I were diligently writing a full-on salmon manuscript. The overall outline of the paper had been in our heads for some time and the writing went rather quickly. By April we had a polished manuscript ready for review and we sent it off to a major neuroimaging journal. Within a week we heard back that it was being rejected on an editorial basis. We heard that there were several major discussions within the journal staff regarding whether to even review the piece. In the end they decided to pass the responsibility, and the trouble, on to another journal.

That brings us to today. The ‘Post-Mortem Atlantic Salmon’ was a strong success at the OHBM conference. It is also under review at a second major neuroimaging journal. The more I think about the affair the more I believe that the fish has the chance to impact the field of neuroimaging in a very positive way. Predefined significance thresholds with a specified cluster extent are a weak control to the problem of false positives in imaging data. Statisticians and methods researchers have argued about the need for multiple comparisons correction for some time. In just one figure the salmon data illustrates exactly why we need stronger controls for the false positive problem in fMRI. I hope it finds a good home in an open-minded journal.

You can find a copy of the ‘Post-Mortem Atlantic Salmon’ poster at this link:

http://prefrontal.org/blog/2009/06/human-brain-mapping-2009-presentations/

41 Responses to “The Story Behind the Atlantic Salmon”

  1. Will - September 18th, 2009

    Brilliant. I appreciate both your highlighting the issue of false positives, and the rather hilarious means by which you did so. Thanks :)

  2. What a dead salmon reminds us about fMRI analysis « Stanford Center for Law & the Biosciences Blog - September 18th, 2009

    [...] author Craig Bennett explains further on his blog: In early 2008 I was working with my co-adviser George Wolford on a presentation he was giving [...]

  3. Neil - September 18th, 2009

    I have to say, I can understand why reviewers have rejected it; you really should add data obtained in dead tuna, sea bass, and squid to make these findings generalizable. One simply can’t say, based on your salmon data, that the fundamental properties of statistical comparison will apply in all species of dead sea creature.

  4. Wow, fish really is brain food! § Unqualified Offerings - September 18th, 2009

    [...] researcher at my alma mater detected brain activity in a dead salmon.  Insert undergrad joke [...]

  5. Mokawi - September 18th, 2009

    I think you should take this data and publish an esoteric book about how the animal soul remains after death and eviceration.

  6. David - September 18th, 2009

    Perhaps you aren’t aware that the term “Atlantic” when used to specify a type of salmon actually means that the salmon is a farmed fish.

    Farmed fish, also known as “Frankenfish” are fed an undisclosed diet of hormones, antibiotics, ground up sheep spines, mad cow tripe and radioactive manure of unknown, possibly intergalactic origin.

    That fish, due to its diet, may in fact be capable of reading human emotion when exposed to photographs of emoting humans even though the fish is or appears to be dead.

    It would be best practice to replicate the scans using a dead Alaska salmon as control.

  7. Just for Fun: MRI a Pumpkin - kaylaiacovino2.0 - September 18th, 2009

    [...] This MRI of a pumpkin was taken by Craig Bennett and Abigail Baird from the University of California Santa Barbara, along with a suite of other unusual objects. [...]

  8. Andrew - September 19th, 2009

    Fabulous. I’m really happy that this got out and about and I wanted to congratulate you on a point well made. Good luck with the reviews at the second journal!

  9. Scanning Dead Salmon in fMRI Machine Highlights Risk of Red Herrings « A Bit of Stardust - September 19th, 2009

    [...] the salmon scanning would simply live on in Dartmouth lore as a “crowning achievement in terms of ridiculous objects to scan.” But the fish had a surprise in store. When they got around to analyzing the voxel (think: 3-D [...]

  10. Simon Spero - September 20th, 2009

    The poster misses an important problem. An overly conservative attempt to generate corrected results when measuring emotional responses in chocolates failed to yield any significant results whatsoever.

    The resulting in-fighting destroyed a once productive research team. This has lead to a marked bias against Bonbon-Furore corrections.

  11. Scanning Dead Salmon in fMRI Machine Highlights Risk of Red Herrings « allbloom - September 20th, 2009

    [...] the salmon scanning would simply live on in Dartmouth lore as a “crowning achievement in terms of ridiculous objects to scan.” But the fish had a surprise in store. When they got around to analyzing the voxel (think: 3-D [...]

  12. Ian Osmond - September 20th, 2009

    I’d like to congratulate you on your clearly inevitable IgNobel.

  13. DaveK - September 21st, 2009

    Ahhh… this is what science is all about!

  14. Marko Crivaro - September 21st, 2009

    You call salmon ridicilous? Try a tree trunk. (I knew a guy who wanted to see if you could track the water diffusion in a tree with MRI, turned out you couldn’t). I have also inserted a good 10 kilo (20 pound or so) ham inside the scanner for.. reasons that are NDA. But still good job, for causing all this rucus. Now we all just need to hope all the not-so mathematical people working with MRI learn about this.

  15. Josh Chang - September 21st, 2009

    I was wondering first of all where I can get a preprint of the paper. I’m curious as to if the authors did any sort of analysis of significance levels. “Statistical significance” is a very arbitrary cutoff and I am wondering if the authors performed any sensitivity analysis of significance levels.

    Thanks

    Josh – I have added you to the list of folks to send the paper as soon as it is in press. We did not do any analysis of significance levels since our primary argument was related to the multiple comparisons problem. ~ Craig [Prefrontal]

  16. Josh Chang - September 21st, 2009

    Personally, I see this less as a weakness in multiple comparison p-value adjustment strategies, and more as a general weakness in Fisher’s formulation of frequentist statistics.

  17. SCE - September 22nd, 2009

    Clearly the next round of tests should be on members of congress!

  18. Ohio Cyclist - September 22nd, 2009

    And I suppose it was silly when Luigi Galvani applied an
    electric current to a dead frogs leg, and it twitched.
    Do we think that everything totally ceases when an
    organism is no longer alive? Galvani proved otherwise.

    Similarly though the fish is dead, this is another proof
    that all activity has NOT ceased. Considering that fish
    are cold-blooded, there may be an even higher chance of
    functioning even longer after death, than might be expected
    of warm-blooded organisms.

    Ohio – Whether or not this is the case, the version of fMRI that we used for the salmon scans would not be sensitive to residual electrical currents in the brain. It is only sensitive to differences in magnetic susceptibility due to changes in the ratio of oxygenated and deoxygenated blood, hence the term blood oxygen level dependent (BOLD) imaging. There was no blood flow in our salmon, meaning that the signal could not rise and fall in synchrony with our experimental design. ~Craig [Prefrontal]

  19. Careful What You Fish For… « Scepticon - September 22nd, 2009

    [...] a must in order to draw valid conclusions. Read Bennett’s description of event’s at his Blog and see the poster based on the data Here. « [...]

  20. K - September 24th, 2009

    While I do agree on the importance of correcting for multiple comparisons – in a random effects study, wouldn’t a big amount of the false positives even out across the subjects, thus somewhat lessening the impact that any single-salmon study could have on the field? Would be great to see a group result – otherwise the big neuroimaging journals would be justified to not publish that paper, and refer you to Neurocase instead… :)

  21. Astoundingly Sympathetic Dead Fish | a Conservation Blog - September 25th, 2009

    [...] Bennett and colleagues at UCSB have found something truly extraordinary: a dead fish that can read our minds. Bennett conducted an fMRI on the length of a dead salmon, [...]

  22. Nick - September 25th, 2009

    Reminds me of the push-back over the paper by Vul et al. that you can find at (http://www.edvul.com/voodoocorr.php) — there will always be resistance to these kinds of corrections, and I think they always come in the peer review process because it’s fairly anonymous, and someone who uses questionable methods can defend them without being forced to make an argument in their defense.

    Which would be hard, because so much of behavioral neuroscience is a recapitulation of just-so-stories from sociobiology, correlated by questionable methods and data.

    Long story short: way to go. You’re not the ‘fish guys’, you’re the ‘good guys’.

    Nick
    publicoption.blogspot.com

  23. Justin Marley - September 27th, 2009

    Hi (?) Craig,
    Didn’t realise it was your poster until just now. Nice one. Very cheeky. Just reviewed it in a bit more detail over here.

    http://theamazingworldofpsychiatry.wordpress.com/2009/09/27/news-round-up-september-2009-4th-edition/

    Is there any chance the highlighted areas could be the substantia nigra – as it’s relevant to a recent PNAS paper

    http://www.pubmedcentral.nih.gov/picrender.fcgi?artid=2732704&blobtype=pdf

    Regards
    Justin

    Justin -I enjoyed your article, and made a more lengthy comment there. Briefly, I will just say that I do not know if the dorsal spinal region is close to the salmon substantia nigra. Unfortunately my years of human neuroanatomy do not transfer that well to the brain of a fish! ~ Craig [Prefrontal]

  24. Personality Pedagogy Newsletter Volume 4, Number 1, Sept, 2009 « Personality Pedagogy Blog - September 28th, 2009

    [...] parts of the brain of a dead salmon responds to human emotion. See also the Story Behind the Salmon here and the pdf of the study [...]

  25. jim - September 28th, 2009

    I saw something similar to this in the mid-1990′s. I think that it also showed that imaging found brain activity or spinal activity in a dead fish. I’m not 100% sure, nor am I sure where it was (I’m a molecular biologist, not an imager), but it was probably somewhere on the web – a site that someone alerted me to.

  26. marcoilbiondo - October 2nd, 2009

    interesting, but could it be just a new exemple of cryptobiose (like tardigrada), so the salmon should be just a little alive (only the brain awaked, like a computer switch off but ready to start) !!

    Freezing is knowing to conserve life, and salmons are not killed before freeze, are they ?

    To live with him in the the future, just reed before the Umberto Eco novel : “how to travel with a salmon”, a funny story.

    Sorry for my bad english

  27. P. Jennings - October 8th, 2009

    Salmon navigate, right? How do they do that? Sense of smell when that works – close to land. Or by magnetism, when out at sea.

    There are magnetic particles in the lateral line:

    >Magnetization measurements with a superconducting quantum >inference device magnetometer of various tissues of the >Atlantic salmon (Salmo salar L.) have shown the presence >of magnetic material associated with the lateral line. The >data suggest that the material is magnetite and of a size >suitable for magnetoreception. Magnetic particles were >isolated from the lateral line and nerve …
    – Magnetic Particles in the Lateral Line of the Atlantic Salmon (Salmo salar L.) A. Moore, et al.

    Have to wonder if there are also such particles in their brains? Enough to cause a change (even in a dead salmon) if exposed to fMRI?

    There may very well be some magnetic particles in their brain. Also, I cannot discount that there may be some interaction of these particles with the scanner’s magnetic field. However, I do not believe that this effect would explain the repetitive rise and fall in the signal needed for the voxels to be considered significant. It is likely that voxels with such particles would have a relatively stable signal or a signal that slowly drifts over time – trends that are removed during image processing of the data. ~ Craig [Prefrontal]

  28. fMRI of dead salmon: how not to do science « Science Notes - October 22nd, 2009

    [...] read “The story behind the Atlantic salmon.” Posted in humor, science. Tags: scientific method. Leave a Comment [...]

  29. Lingoland » Arkiv » Post-mortem mentalization processes in the Atlantic Salmon - January 14th, 2010

    [...] be careful when drawing conclusions from fMRI scans. The salmon scans (poster) and the story behind it. Skrevet af Anders K. Madsen | Ingen kommentarer Emneord: fMRI, kognition, MRI, [...]

  30. Law and Biosciences Blog | What a dead salmon reminds us about fMRI analysis - February 7th, 2010

    [...] author Craig Bennett explains further on his blog: In early 2008 I was working with my co-adviser George Wolford on a presentation he was giving [...]

  31. laci - March 18th, 2010

    love salmon very much. we raised salmon in are class

  32. Dead Salmon “haunts” fMRI data « brainfrontiers - April 10th, 2010

    [...] search for behavior-related activation can begin. Case in point is this wonderful story found here about an Atlantic Salmon that despite being dead appeared to show brain activity in it’s [...]

  33. The new Twinkie defence: abuse and misuse of fMRI's and science, and using the label psychopath as an excuse - blog by Gurdur - Blogs on the Heathen Hub - July 6th, 2010

    [...] of the brain. There are many complex difficulties in interpreting fMRI scan data, as for example when researchers ran fMRI scans on a dead salmon fish, and discovered false positives. In 1985, Brian Dugan, who was already in prison for the murder of a 27-year-old woman and the [...]

  34. Something fishy with MRI scans « - January 7th, 2011

    [...] fishy with MRI scans By dwighttowers This article (via the brainiac Cosma Shalizi), is hilarious, from a postdoc who will probably now be known as [...]

  35. Crystal - May 6th, 2011

    Well, because it hasn’t been asked yet (and I’m quite surprised it hasn’t);

    You neglected to tell us. Was the fish delicious? :)

  36. Diane Erwin - July 15th, 2011

    Ah, you’ve found the Salmon of Knowledge

  37. ‘was not alive at the time of testing’ | lautopolis - February 16th, 2012

    [...] the story behind how this came about: http://prefrontal.org/blog/2009/09/the-story-behind-the-atlantic-salmon/ Share this:TwitterFacebookLike this:LikeBe the first to like this post. This entry was posted in [...]

  38. The problem with multiple comparisons « psuc5d - February 18th, 2012

    [...] The voxel appears to be active (to a significantly high level) but where in reality, it is not. Bennett wanted to demonstrate these false positives by looking for active voxels on something that would [...]

  39. Start - September 5th, 2012

    [...] it is a well-known scientific truth that research results which are accompanied by a fancy, colorful fMRI scan, are perceived as more believable and more persuasive than simple bar graphs or text results (McCabe & Castel, 2007; Weisberg, Keil, Goodstein, Rawson, & Gray, 2008). Readers even agree more with fictitious and unsubstantiated claims, as long as you provide a colorful brain image, and it works even when the subject is a dead salmon. [...]

  40. The IgNobel Prize winners 2012: speech jamming, dead salmon brain activity, green hair and more – misc.ience - September 20th, 2012

    [...] Miller and Wolford for using sophisticated brain scanning technology (fMRI scanners) to detect brain activity in dead salmon as a lesson in the multiple comparisons [...]

  41. Seeing is Believing. Which is Dangerous. | Meta Rabbit - October 4th, 2013

    [...] On twitter, Jim Procter (@foreveremain), points out a great example: the story of the salmon fMRI: we can see it, but we shouldn’t believe it. Share this:EmailTwitterFacebookGoogleLike [...]

Leave a Reply