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Monday, 4 July 2011

Gamma Waves: The Brain's Clock, Or Neural Noise?

Gamma waves are very hot at the moment.


Gamma band activity is a term for electrical oscillations recorded from the brain that have a frequency of over 25 Hz. In most brains, a peak frequency of about 40 Hz is seen. This makes gamma waves the fastest brain waves.

If you believe some recent claims, gamma waves are the answer to all the mysteries of life and the universe. They're said to underlie the symptoms of schizophrenia and autism, and they've been invoked to answer deep questions such as the binding problem and maybe conciousness itself. You can even buy a Nintendo game that promises to boost them.

A new paper from Burns et al casts doubt on all of these grand claims. Gamma-based theories of brain function all assume that gamma waves act a bit like a clock, with a consistent rhythm of about 40 Hz. Activity of about 40 Hz is indeed observed in brain recordings but is that just because the brain is randomly generating all kinds of signals, and only the 40 Hz ones "get through"?

To put it another way, imagine that you got a letter in the mail at 9 am every morning. That could be because someone is sending you one letter each day like clockwork. But it could also be that loads of people are sending you letters at random times, and your mailman only has room in his sack to deliver one each morning.

Here's the key data, recorded using electrodes implanted into the brains of two male macaque monkeys:


This shows that the monkey data closely resemble what you'd expect if gamma activity were filtered noise, and are not what you'd see if it were a more meaningful "clock". The "triangle" on the graph shows the number of bursts of a given frequency and duration.
The data also show that the phase of the gamma activity isn't consistent, which it would be if it were clocklike. In fact, the phases change entirely randomly.

So if gamma is just "filtered noise", what's the "filter"? Why 40 Hz, not 80 or 4000? Probably because this is just the maximum frequency at which neurons can fire. It takes a certain finite amount of time for cells to communicate with each other: a silicon chip can get a clock speed of many billions of hertz, but a cell just physically can't.

There's a catch, though. These monkeys were asleep, anaesthetized with the powerful opiate sufentanil. This is a good choice of drug: unlike most other sedatives and anaesthetics, you wouldn't expect an opiate to directly affect gamma oscillations. But still. If you believe that coherent gamma waves are the key to high-level concious experience, as many do, you might not expect to see much of that in the primary visual cortex in asleep animals.

However, this is clearly a very important issue, and it's not the first gamma-skeptic paper. In 2008, Yuval-Greenberg et al reported that many attempts to measure gamma activity using EEG were contaminated by electrical activity from scalp muscles. Rather than coming from the brain, the "gamma" activity reflected nothing more than tiny eye movements. The implications are still being debated.

This paper attacks the gamma hypothesis from a completely different angle, saying that even the "real" gamma in the brain, may be nothing more interesting than filtered noise.

ResearchBlogging.orgBurns SP, Xing D, & Shapley RM (2011). Is gamma-band activity in the local field potential of v1 cortex a "clock" or filtered noise? The Journal of neuroscience : the official journal of the Society for Neuroscience, 31 (26), 9658-64 PMID: 21715631

12 comments:

Anonymous said...

Boy, neuroscience has certainly given us hard answers in psychiatry!!!! And novel ground-breaking treatments are all around us! Gotta love gamma! But what treatments can I show my mama?

Richard said...

- Haven't read the paper fully yet (thanks for pointing it out, this is definitely an area of interest for me!), but regarding these comments:

'Gamma band activity is a term for electrical oscillations recorded from the brain that have a frequency of over 25 Hz. In most brains, a peak frequency of about 40 Hz is seen. This makes gamma waves the fastest brain waves.'

- Very Fast Oscillations >70 Hz also exist (sometimes up to 250Hz), often nested with gamma oscillations. These appear to rely on axon-axon gap junction coupling between excitatory cells.

'So if gamma is just "filtered noise", what's the "filter"? Why 40 Hz, not 80 or 4000? Probably because this is just the maximum frequency at which neurons can fire. It takes a certain finite amount of time for cells to communicate with each other: a silicon chip can get a clock speed of many billions of hertz, but a cell just physically can't.'

Most gamma oscillations are not generated by cells firing rhythmically on each cycle of the oscillation, but by much sparser firing. When you look at the spike trains of individual neurons it's hard to pick out any kind of gamma activity as they seem almost Poissonian, but the network frequency of a large collection of cells gives rise to the full gamma oscillation. Many of the interneurons (thought to be a key gamma sculptor) and chattering pyramidal cells can fire faster than this, too.

Sorry to nitpick, interesting article, I'll be back once I've read the paper ;)

Neuroskeptic said...

Richard, thanks for the comment, I love nitpicking.

Re: fast oscillations, I've seen anything up to 100 Hz referred to as "high gamma" in some sources. But I've never heard of the gap-junction based stuff - that makes sense, though.

Richard said...

I tend to see 20-30Hz referred to as beta, 30-70/80Hz as gamma (fast oscillations) and anything above 70-80Hz as Very Fast Oscillations (VFO). But the terminology does seem a little flexible depending on whom you're reading. I'm not really familiar with EEG studies, mainly in vitro stuff (and I'm not an experimentalist myself...).

As for gamma, there are various different ways it can be generated, each with different underlying mechanisms and properties other than the overall frequency.

If anyone wants a good but technical background on some oscillatory mechanisms in the neocortex you can get the lecture notes from a 2009 Society for Neuroscience course on them here: http://www.sfn.org/index.aspx?pagename=ShortCourse2_2009 (see the "Modeling Rhythms: Detailed Cellular Mechanisms of In Vitro Oscillations with Emphasis on Very Fast Oscillations" if you're interested in axo-axonal gap junctions).

Haven't read the paper yet though still, will get round to it within the week I'm sure!

Neuroskeptic said...

Thanks, that's very handy. I'm starting to dabble in gamma EEG myself. Although at the moment, we are busy trying to get rid of the noise. We have lots of activity at 250 Hz... it is harmonics of the 50 Hz power line signal.

Neuroskeptic said...

Thinking about it more, the theory that gamma is just filtered noise would account for a lot of things.

It would explain why gamma is produced whenever a part of the brain is activated: activation means more neural firing means more "noise".

It would also explain why gamma is strongly correlated with the fMRI BOLD response: the more neural activity, the more noise, and the more metabolism: http://www.sciencemag.org/content/309/5736/948.short

If this is true, gamma might still be very interesting, as an EEG measure of general "neural activation".

orcasha said...

Pope's 2009 article (http://www.ncbi.nlm.nih.gov/pubmed/19229605) is also an interesting read regarding muscle noise and gamma oscillations. Small sample, but interesting results.

Richard said...

I have a couple of general comments about the assumptions of the paper, but I'll just state the following disclaimers first: I'm relatively new to neural oscillations, and I'm not totally up to speed with the finer points of time-frequency analysis. Anyway...

As I understand it, I'm not sure that the assumptions of the paper regarding the proposed 'clockiness' of gamma are quite right. They state that:

"Previously, gamma oscillations were thought to provide a regular temporal reference signal for the brain; we call this idea the “clock” theory of gamma activity. A clock signal would be autocoherent, meaning that it would have a stable temporal frequency and a consistent phase... Fries et al. (2007) proposed that gamma activity supplies a 'temporal reference frame' in which the 'precise spike timing' of individual spikes encodes information relative to the consistent phase of gamma activity".

The key word in that last sentence is "consistent" - I don't think the proposed coding mechanism in Fries et al. (link: http://www.sciencedirect.com/science/article/pii/S0166223607001245 ) requires consistent phase (autocoherence in the signal). Their proposed coding mechanism suggests that the "rank ordering" of spikes is decided based on when the spike is fired relative to the instantaneous phase of the gamma oscillation, with spikes occurring early in the oscillation phase being the most information rich. This does not require autocoherence in the oscillation as far as I can tell, because however long each cycle of the oscillation lasts, the spikes occurring at a certain point relative to the instantaneous phase of the oscillation will always be the most informative, as it's the relative timing that matters rather than the absolute timing. An oscillation could slow down or speed up and this would still be the case.

More important in Fries et al.'s description is oscillation coherence between different brain areas. Provided the gamma oscillation is coherent between two different areas, even if the oscillations aren't autocoherent, the two areas will be running with the same temporal reference frame for spiking. Oscillation coherence between different areas has been demonstrated in various studies mentioned in the Fries et al. review. This paper doesn't look at coherence in space, only signal autocoherence. I might well have misunderstood something, but I think this paper's clock formulation of the gamma rhythm isn't quite what has been suggested previously.

Could you make any predictions about spike timings from assuming gamma is just filtered noise? Or about coherence across brain areas? Also, what's the filter?

Albert Finnegan said...

I have to second Richard's comment above. While I have sometimes carelessly used the "clock analogy" to talk about gamma-theta modulation, the analogy should not be taken too far.

Thinking of gamma waves as filtered noise is, of course, better than selling crack on the street. ;-)

sorry

David Dobbs said...

Hm. I'm quite enchanted by Buzsaki's work, and gamma sync in general. Have to find time to read this paper carefully. Meantime, would love to hear from Buzsaki or similar ...

You skeptics!

Richard said...

Just been looking at some data from our experimental collaborators and it provides some evidence against the hypothesis that gamma is filtered noise. They are looking at Utah array (10x10 microelectrode array, spacing -.4mm between electrodes) placed recording from brain slices exhibiting persistent gamma oscillations. Looking at measures of functional connectivity between recording sites, they find that functional connectivity during persistent gamma oscillations is different from "filtered noise" functional networks. There's some other cool stuff in there too, but it's unpublished so can't say too much about it. However, this is an in vitro model and the generating mechanisms may be a bit different from in vivo.

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