Signal and noise: Spike correlations in the olfactory system

by John Hewitt report
Signal and noise: Spike correlations in the olfactory system
Spikes in the Olfactory Bulb. Credit: Monell.org

(Medical Xpress)—The olfactory system is a particular favorite among the many who study neural coding. One reason for this is that presentation of a single odorant to an otherwise featureless smellscape, at least in theory, provides an ideal and dimensionless event for the olfactory front end to code. There is ample evidence that within the olfactory bulb, odors are represented by spatial patterns of activity. There is also evidence that odors are captured by individual cells through spike timing, pattern, and their phase relative to the respiratory cycle. As expected, there is also much suggestion to the contrary for each of these cases. A new study done by researchers from Carnegie Mellon reports that the identity of an odor directly influences the amount of correlation, or linked firing, in the spikes of the output cells of the bulb. In their recent paper published in PNAS, they show that this correlation originates primarily from the act of sniffing itself, with significant contributions also arising from the local circuit connections (within a few cell diameters) in the bulb, while the odor itself contributes only a small portion of the correlation.

The output of the bulb, the Mitral and Tufted cells (MT cells) studied here, send their axons to various higher centers in the brain, but ultimately, the olfactory cortex. M/T cells appear to fire with fair degree of regularity, even in the absence of odorants, in contrast to the cortical cells which have generally have lower spontaneous rates. What really turns on the M/T cells though, is breathing. Different MT populations have been shown to favor different phases of the respiratory cycle, but individual preferences can still change on dime. Decades ago, researchers performed various manipulations including cutting nerve tracts, blocking the nostrils, tracheotomy, and presenting odorants directly to the epithelium, to try to uncover the origins of the respiratory control. They found the peripheral airflow effects were a primary driver, but that there was also some influence from above so to speak, presumably through an efference copy of the output of the respiratory center. There was also found to be an intrinsic effect, where the bulb in effect "rings" at various pre-tuned fundamentals or overtones according to its size and connectivity.

Other studies have focused on more fine-grained origins of MT cell correlations, like for example, intrinsic channel dynamics within cells or the localization of gap junctional proteins on the apical dendrites of conspiring cells. One study showed that the electrical pore forming protein, connexion 36, was critical to maintaining correlations in MT activity. To try to get a better handle on these different kinds of correlations, I asked author Nathan Urban about the coupling between firing rate and inspiration seen in his studies. He mentioned that this was not explicitly probed but that it is likely that the influence is from periodic activation of sensory neurons during breathing. Before trying to get too particular here about attributing precise mechanism to sometimes imprecise or even weak correlations, we might step back for a moment ask in ignorant bliss, is it possible to say anything at all with certainty about codes and odorants just by looking at spike trains in olfaction?

The is not so much a hard-wired telephone network where channels can be instantaneously specified and connected by number codes, and then used to transmit further codes. There is significant overgrowth and back-pruning in olfactory networks during development, and some ongoing cell replacement, but once etched, many of its larger features remain stable. The front-end receptor cells of the network express only one kind of sensor, but this sensor may respond to several different kinds of odorants. Not only that, but each odorant can potentially activate several kinds of receptors. The complication here is that we really don't know all that much about what features of they are sensing, and how they sense it. That makes understanding what is to be coded a challenge.

What happens in the development of the olfactory system, is that a kind of labelled-line network spontaneously emerges that is composed of around one or two thousand discrete synaptic glomeruli. As these glomeruli self-organize, they accept projections only from receptor cells possessing the same odor sensor. It is the glomeruli then, might be said to be the real detectors of the system, essentially transforming "odorant space" into "detector space." While there is generally no clear indication that any significant odor sorting occurs in the nasal passages or epithelium, or that any topography like that found in the retina is evident for , these possibilities should not be written off entirely.

The critical feature of the circuit remodeling in the developing bulb, is that like the other senses, it is built on the back of the spiking activity of neurons. Once the circuits stabilize, the neurons obviously don't just shut down, but rather they keep on pumping out synchronized spikes to their entire axonal tree and beyond. The key here for neural codes, is that even as many of the protein isoforms expressed in critical periods of development are taken out of service, spikes can not be considered completely independent of their direct effect on circuit structure and tone. Nor can a quiescent stimulus space be considered neutral to a detector cell.

The timescale on which the authors found significant correlations was in the range of 10-100ms. They note that when noise in the system is correlated, can be reduced because the noise does not average out. They mention the intriguing possibility that noise correlation levels are matched to population sizes, and suggest that the number of MT cells associated to a particular glomerulus (~25 in vertebrates) represents an optimal level where beyond that, information transmission would begin to saturate.

There is one major caveat in considering the olfactory system as a communication and signal conditioning network—the so-called noise on the channels, that which is measurable even in the absence of a signal, is in reality anything but. The buzz of nerves in development transitions through breathing amniotic fluid, to air without a hitch, all the while updating the brain about the condition and state not only of its peripheral sensors, but of central more generalized activating systems. Any code we define for the bulb should be considerate of the fact that while perceiving the alarming smell of smoke or methane may feel exceptional to us at the cognitive level, for the nose, it may just be a handful of atoms toggling receptor states whose larger condition and health needs to be reported in roll call among countless others. In this light any message can not stand out like the clear dots and dashes of Morse code above noise, but must surf in the ocean where every wave is considered potentially meaningful.

More information: Origins of correlated spiking in the mammalian olfactory bulb, PNAS, Published online before print September 30, 2013, DOI: 10.1073/pnas.1303830110

Abstract
Mitral/tufted (M/T) cells of the main olfactory bulb transmit odorant information to higher brain structures. The relative timing of action potentials across M/T cells has been proposed to encode this information and to be critical for the activation of downstream neurons. Using ensemble recordings from the mouse olfactory bulb in vivo, we measured how correlations between cells are shaped by stimulus (odor) identity, common respiratory drive, and other cells' activity. The shared respiration cycle is the largest source of correlated firing, but even after accounting for all observable factors a residual positive noise correlation was observed. Noise correlation was maximal on a ∼100-ms timescale and was seen only in cells separated by <200 µm. This correlation is explained primarily by common activity in groups of nearby cells. Thus, M/T-cell correlation principally reflects respiratory modulation and sparse, local network connectivity, with odor identity accounting for a minor component.

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JVK
1 / 5 (4) Oct 22, 2013
This comparison is meaningful: "...any message can not stand out like the clear dots and dashes of Morse code above noise, but must surf in the ocean where every wave is considered potentially meaningful."

In mammals, breathing transmits chemical to electrical pulses (not waves) of information that allows olfactory/pheromonal input to epigenetically effect the hypothalamic secretion of gonadotropin releasing hormone (GnRH). Pulses of GnRH integrate sensory input associated with food odors and social odors called pheromones during what we were just told is self-organized network that spontaneously emerges during prenatal and postnatal development of other sensory abilities.

That means the innate ability of the olfactory system organizes itself and emerges during development as the key integrator of all other sensory input (visual, tactile, auditory) that results in nutrient-dependent pheromone-controlled adaptive changes in the brain and behavior of invertebrates and vertebrates.
johnhew
1 / 5 (3) Oct 22, 2013
I am not as in tune to all the pheromone stuff, but your points about olfaction as a key integrator for development of other perceptions, and of the ultimate output of the brain being hpothalamic dollops of potent peptide elixer are nice. I would image olfaction as the link which gives knowledge at the level of the single cell up through multicellularity to both touch and vibration through any medium an organism finds itself within.
JVK
1 / 5 (4) Oct 22, 2013
Thanks. You forgot vision. Olfaction spontaneously highlights visual saliency map http://rspb.royal...abstract

Olfactory/pheromonal input is the only direct link from the sensory environment to the gene-cell-tissue-organ-organ system in invertebrates and vertebrates that enables the nutrient-dependent physiology of reproduction and thus survival of the species.
beleg
1 / 5 (2) Oct 24, 2013
"In this light any message can not stand out like the clear dots and dashes of Morse code above noise, but must surf in the ocean where every wave is considered potentially meaningful.-JH"

78% water. The brain.
Just add carbon.
Three molecular elements for all lipids.
JVK
1 / 5 (2) Oct 24, 2013
Experience-dependent plasticity is obviously the key to "....the innate ability of the olfactory system [which] organizes itself and emerges during development as the key integrator of all other sensory input (visual, tactile, auditory) that results in nutrient-dependent pheromone-controlled adaptive changes in the brain and behavior of invertebrates and vertebrates.

What is beleg trying to tell us about? Perception involves more that molecules. "Fine Tuning of Craniofacial Morphology by Distant-Acting Enhancers," by C. Attanasio; A.S et al. Science, 2013. http://medicalxpr...que.html
beleg
1 / 5 (2) Oct 25, 2013
"Perception involves more that molecules."- JVK

Imagine geometry giving rise and underlying all of physics perceivable:
https://www.simon...he-mind/

Excerpt:
"It's absolutely relevant to know as much as we can about the topology of the underlying structure to understand the function," said Gustavo Deco, a neuroscientist at Universitat Pompeu Fabra in Barcelona, Spain."

https://www.simon...physics/
Excerpt:
"In a sense, we would see that change arises from the structure of the object," he said. "But it's not from the object changing. The object is basically timeless."

You are a slave host to your microbiomes. You catered to their need of nutrients and olfactory needs. Microbiomes organize your olfactory system as well as your senses.
Your microbiomes control your adaptive changes in the brain and your behavior.
Epigenetic factor number one are your microbiomes
JVK
1 / 5 (2) Oct 25, 2013
Beleg wrote: "Epigenetic factor number one are your microbiomes"

Is there a model for that? "The microbiota-gut-brain axis: neurobehavioral correlates, health and sociality" http://www.fronti...13.00070

In my model, epigenetic effects of nutrient uptake result in pheromone-controlled reproduction in the bacteria that make up the microbiomes of different species. I'm not sure how anyone can move forward starting from microbiomes as epigenetic factor number one. But beleg doesn't need to elaborate on that, because it is nonsense.
beleg
1 / 5 (2) Oct 26, 2013
Elaboration:
Sterile humans are nonexistence.
The model? The human species.
Start from there and trace the evolution of higher ordered species backwards.
JVK starts with nonsense - single cells following their nose to reproduce - and moves forward.
johnhew
1 / 5 (2) Oct 26, 2013
beleg, we could some feedback on http://medicalxpr...way.html
JVK
1 / 5 (2) Oct 26, 2013
Here's an example from the recent literature that "beleg" appears to be labeling "nonsense." Signaling Crosstalk: Integrating Nutrient Availability and Sex http://stke.scien...291/pe28

We began with sex differences in yeast when we detailed the common molecular mechanisms of epigenetics in 1996. See http://www.hawaii...ion.html

The nutrient-dependent pheromone-controlled physiology of reproduction is conserved across all species from microbes to man, which is why I modeled it in http://www.socioa...53/27989

What's nonsense is to be forced to deal with anonymous fools who provide no evidence whatsoever to support their ridiculous claims but challenge my expertise, which includes a publication history and examples of model organisms from microbes to man. The human species is not a model, it exemplifies my model.
JVK
1 / 5 (2) Oct 26, 2013
beleg, we could some feedback on http://medicalxpr...way.html


If beleg knew anything about neurogenic niche construction, we would already have learned that it is nutrient-dependent and pheromone-controlled, which is obvious in my model.
beleg
1 / 5 (2) Oct 27, 2013
No resource replenishes itself indefinitely. You confuse your 'expertise' as being challenged instead of being ignored. A strange way to regard any attention you have received.
JVK
1 / 5 (2) Oct 27, 2013
beleg: My award-winning published works include: The Mind's Eyes: Human pheromones, neuroscience, and male sexual preferences http://www2.hu-be...kohl.htm and Human pheromones: integrating neuroendocrinology and ethology http://www.nel.ed...view.htm

Both added citations to research that supported our 1996 Hormones and Behavior review: From Fertilization to Adult Sexual Behavior http://www.hawaii...ion.html

Neuroanatomist Simon LeVay wrote: (p. 210) This model is attractive in that it solves the "binding problem" of sexual attraction... http://www.amazon...99737673 If all these characteristics come to be attractive because they were experienced in association with a male- or female-specific pheromone..."

Your ignorance does not suggest my works have been ignored.