Silent Neurons: The Dark Matter of the Brain?

By Neuroskeptic | February 6, 2019 3:38 pm

Now here’s a paper with an interesting title: The dark matter of the brain

Author Saak V. Ovsepian argues that “the great majority of nerve cells in the intact brain do not fire action potentials, i.e., are permanently silent.” This is a remarkable claim, and it raises the question of what these silent neurons are doing. However, I didn’t find myself convinced of the existence of this ‘dark matter’.

Ovsepian points out that numerous studies have found that only a minority of the neurons in a given brain region are observed to fire (spike), even in response to stimuli that activate that area:

In the primary auditory cortex of rat, for example, less than 10% of neurons discharge action potentials in response of acoustic stimuli, with the remaining majority keeping non-responsive (Hromadka et al. 2008). Imaging studies of other cortical areas showed similar results, with bulk of nerve cells in the olfactory bulb (Poo and Isaacson 2009), gustatory cortex (Chen et al. 2011), primary visual fields (Ohki et al. 2005; Greenberg et al. 2008) as well as in the somatosensory cortex (Kerr et al. 2007) keeping silent.

So the ‘dark matter’ of the brain are neurons which don’t fire in response to any stimulus tested.

Silent neurons are related to the concept of ‘sparse firing’, which is believed by some to be a general principle of brain organization. Sparse coding means that a given stimulus only activates a small number of neurons. By contrast, non-sparse coding would mean that every stimulus activated many neurons, but to different degrees. Both of these schemes could encode information.

The existence of silent neurons implies sparse coding – but not vice versa. Under sparse coding, most neurons will be silent in response to any single stimulus. Here’s an illustration (inspired by Fig 1 here) of sparse firing in a group of 12 neurons, where each stimulus activates 2 or 3 neurons and has no effect on the others:

SPARSEIn this example, five of the neurons are ‘silent’ – they don’t respond to any of the stimuli used in the experiment. It seems obvious, however, that this is not an absolute definition of ‘silent’. If we did a more extensive experiment using more diverse stimuli, we might find at least one stimulus that does activate each neuron – and there would be no more silent cells.

SPARSE2As Barth and Poulet put it, “the fraction of responsive cells may be underestimated because the experimental stimulus applied may not be appropriate to drive the neurons tested.” In order to know whether there are truly silent neurons that don’t respond to any stimulus, we would need to test all possible stimuli – which is a tall order.

Ovsepian does acknowledge this point, saying that:

Another possible explanation for the presence of great numbers of inactive neurons is their narrow tuning to respond only to specific inputs [i.e. sparse coding]… but whether these considerations can explain the perpetual silence of the vast majority of neurons throughout the brain remains to be shown.

Yet I’d say that the burden of proof is on someone who claims the existence of absolutely silent cells. The experiments cited by Ovsepian have used very narrow sets of stimuli, in absolute terms. No-one has yet recorded brain activity from rats while exposing them to every possible sound that a rat could hear(!).

Finally, Ovsepian goes on to discuss the evolutionary significance of silent neurons. He suggests that these inert cells might represent ancient neural circuits that have since become obsolete. These fossilized brain circuits are subject to neural inhibition which keeps them suppressed:

The brain’s dark matter epitomizes the tangible and highly composite byproduct of the natural evolution, trapped in inactive and invisible state by inhibition. Rooted deep in the phylogenic past, vast collections of fossilized neurons and networks once had been the integral part of functional circuits and played their adaptive role in life affairs.

I didn’t find Ovsepian’s evolutionary argument that persuasive, because I’m skeptical of the whole ‘dark matter’ concept. Still, the idea that remnants of our ancestors’ brains still exist in our own skulls is a rather fascinating one. It suggests Jurassic Park-like scenarios in which someone succeeds in reactivating these lost neural functions – and there is evidence that this can happen in very specific cases such as reflexes. In general, though, I don’t think we can say that the majority of our neurons are fossilized.

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  • Iandol

    Gosh, how on earth can these authors seriously suggest a “fossilised network” hypothesis instead of just marvelling at how sparse most stimulus representations are in the cortex? Yes, sparse coding as a general mechanism is still far from proven, but to imagine an alternative where the genome somehow encodes vast silent networks precisely is absurd (and ignorant of how brains develop). Those neurons will still need to be physiologically maintained, providing a huge burden for something that has no adaptive value. I much prefer Marcus Raichles analogy for brain dark matter: http://www.sciencemag.org/cgi/content/full/314/5803/1249 — intrinsic activity dominates evoked activity, yet we don’t yet really understand why (with a best guess invoking predictive coding of some sort IMO).

  • TwoMajesties

    Sounds like the makings of an intriguing sci-fi film in the near future.

  • Juan Valle Lisboa

    So we only use 10 % of the brain after all! Scarlett was right all this time …hahahaha

  • OWilson

    Most were charletans, but throughout history, many people have come forward claiming to be everybody from Napoleon, Joan of Arc, Romonanov Heirs, to even the son of god!

    Even today we have politicians claiming to channel Eleanor Roosevelt, and memories of running and ducking sniper fire in war zones. Vivid memories of none existant church burnings in Arkansas, not to mention distinct memories of being gang raped by a Supreme Court Justice, being members of Indigenous Tribes, or being War Heroes in far off lands like VietNam, they’ve never seen!

    These people’s repressed memories, can be triggered by money or ambition, as well as inherited archaic brain cells.

    Treat these claims with some discretion. But do not dismiss them out of hand.

    It would be a shame if you missed out on the Great Rapture, and got left here on a scorched Earth while true believers got carried up to Eternal Joy by the Grand mothership! :)

  • http://www.gwern.net/ gwern

    What fossilized genes code for these useless neurons specifically, and how do they survive neurodarwinism, one wonders?

    In any case, one could do a simple experiment with ANNs to demonstrate the problem here – take an ANN trained on some dataset, say, ImageNet, and run it on a small fraction like 1% of the validation data. How many ‘neurons’ contribute non-zero activations? I suspect it will be <<100%…

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  • Occasional-Cortex

    Generally speaking, the body does not continue to expend valuable resources on tissue that is not being used. Brain tissue, unlike say nipples on males, requires a disproportinate amount of glucose compared to other organs.

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  • Ricardo Vieira

    Is there any testable prediction coming out of this, such as looking at species that branched earlier in evolution and checking if they have less ‘dark neurons’?

  • Sevak

    I respect and value all critical remarks about the dark brain. The early thoughts about redundancy in the brain were disconcerting to me as well. After years of research and discussion with colleague neuroscientists, and careful analysis of the literature, I slowly came to the conclusion that large-scale presence of dormant neurons in the brain is not only likely but is real, and is deeply embedded in our biology and history. Understandably, the brief article above falls short in presenting the entire story discussed in the original paper published in Brain Structure and Functions. To appreciate the drama of the dark brain, I suggest reading the full version (doi: 10.1007/s00429-019-01835-7). I immensely enjoyed writing it, and hope that it makes an instructive read. From the author of the ‘Dark Matter of the Brain’.

  • Sevak

    I respect and value all critical remarks about the dark brain. Early thoughts about redundancy in the brain were disconcerting to me as well. After years of research and discussion with colleague neuroscientists, and careful analysis of the literature, I slowly came to the conclusion that large-scale presence of dormant neurons in the brain is not only likely but is real, and is deeply embedded in our biology and history. Understandably, the brief article above falls short in presenting the entire story discussed in the original paper published in Brain Structure and Functions. To appreciate the drama of the dark brain, I suggest reading its full version (doi: 10.1007/s00429-019-01835-7). I immensely enjoyed writing it, and hope that it makes an instructive read. From the author of ‘The Dark Matter of the Brain’.

  • Saak V. Ovsepian

    I respect and value all critical remarks about the dark brain. Early thoughts about redundancy in the brain were disconcerting to me as well. After years of research and discussion with colleague neuroscientists, and careful analysis of the literature, I slowly came to the conclusion that large-scale presence of dormant neurons in the brain is not only likely but is real, and is deeply embedded in our biology and history. Understandably, the brief article above falls short in presenting the entire story discussed in the original paper published in Brain Structure and Functions. To appreciate the drama of the dark brain, I suggest reading its full version (doi: 10.1007/s00429-019-01835-7). I immensely enjoyed writing it, and hope that it makes an instructive read. From the author of ‘The Dark Matter of the Brain’.

    • http://blogs.discovermagazine.com/neuroskeptic/ Neuroskeptic

      I enjoyed reading the paper also!

  • BrianW

    There are some interesting ideas in this paper. But to me, the argument that there are neurons with no function seems to rest on some questionable assumptions such as:

    1. The only function of (for example) auditory cortical neurons is to respond to auditory stimuli. But most obviously, they may be coincidence detectors, even involving non-auditory coincidence detection. No experiment design could activate very many of the possible coincidence detectors, so we would expect many functional neurons to appear silent.

    2. The only function of the brain is to respond to stimuli. But a sleeping brain receives little sensory input and is nonetheless quite active. I think it’s likely that a large fraction of neurons even in sensory areas are involved in other functions, like switching between brain states (e.g. sleep/wake), or focusing attention, or maintaining working memories, or activating/consolidating long-term memories. A laboratory setting is going to engage only a small fraction of these systems, so we would expect many functional neurons to appear silent.

    3. Neurons that aren’t firing action potentials aren’t doing anything. But for example astrocytes don’t fire action potentials and they still function and affect other cells. A non-firing neuron may still be functioning in some way.

    • Saak V. Ovsepian

      The main argument is simple: if all neurons are functional, then surely brains should not operate normally when 90% of tissue is missing. But sometime they do – ) There are numerous other arguments as well, also supporting redundancy of neurons, which are discussed in the paper…

      • BrianW

        I completely agree with the redundancy idea, as brains can clearly still function after being damaged. But redundant doesn’t mean silent or non-functional. To use a computer analogy, I can take one of the RAM cards out of my computer and the computer will function just fine. That doesn’t mean it wasn’t doing anything before I took it out.

        • Saak V. Ovsepian

          1. Silent neurons are not abstract conjecture, but experimetnal observation. Unless we present evidence that all neurons generate action potentials at some point in time, the posibility of permanently silent cells remains.

          2. Animals are not cartesian beast-machines and brains are not computers, but product of natural evolution. One can install as many RAMs in the computer as there is room for it. In living systems, there is no room for excess and everything functional that does not fit to adaptive purpose is eliminated.

          3. There are however examples of relict organs and traits, which have no (apparent) function, and are beyond the reach of selective pressure. And as a result, cannot be eliminated…

  • Saak V. Ovsepian
  • Marcus Kazushi Mon

    Perhaps the neurons remain silent, because its not needed on earth to activate. I think we envolved from a postbiological species. How zero gravity affects stimuli of the neurons?

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Neuroskeptic is a British neuroscientist who takes a skeptical look at his own field, and beyond. His blog offers a look at the latest developments in neuroscience, psychiatry and psychology through a critical lens.

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