Unitary response of mouse olfactory receptor neurons

Citation: Yair Ben-Chaim, Melody M. Cheng, King-Wai Yau (2011/01/11) Unitary response of mouse olfactory receptor neurons. PNAS (RSS)
DOI (original publisher): 10.1073/pnas.1017983108
Semantic Scholar (metadata): 10.1073/pnas.1017983108
Sci-Hub (fulltext): 10.1073/pnas.1017983108
Internet Archive Scholar (search for fulltext): Unitary response of mouse olfactory receptor neurons
Download: http://www.pnas.org/content/108/2/822
Tagged: Neuroscience (RSS) olfaction (RSS), mouse (RSS)

Summary

This paper studies the response of mouse olfactory receptor neurons [ORNs] to a variety of odorants, and notes that the response is relatively uniform in amplitude and kinetics, unchanging across different neurons and different odors (hence 'elementary' or 'unitary' - responding to the entire experience of a novel smell as a single smelling-event). The experiment involved followed earlier work by Yau and others on frog ORNs, showing that the same results hold for mice and so possibly for other mammals.

The olfactory response similar for different clusters of odorants it had little amplification, triggering transduction through only just single molecular complex. Successful response required only O(10) successful binding events. Both traits are similar to the results found for frog ORNs in the earlier work.

Goals and Methods

The primary goal was to check the similarity between responses of mouse and frog ORNs to address the question of whether the properties of olfactory response in mammals might have similar traits. Existing methodology was repeated with mouse cells: short bursts of odorants, varying either the concentration in bursts of fixed length or the length of bursts of fixed concentration.

The method used carried out a quantal analysis on results, assuming there was a minimum unitary response, and a Poisson distribution of individual responses. The suction-pipette method was used to measure membrane currents. As there are 1000 species of OR cells, a mixture of five odorants was used instead of two.

Temperature effects were also studied - the most detailed experiment was run at room temperature, as the cells did not last as long at higher temperatures, but macroscopic analysis of cell behavior at 35 C was evaluated for differences.

The threshold number of binding events to trigger an action potential to the brain was measured, to provide a bound on the sensitivity threshold for olfaction.

Finally, additional experiments were carried out to test the dependence of the concentration of G proteins on output signal strength. Cells from adult mice that expressed half of the normal level of G protein involved in odorant activation were compared with those from mice with normal expression.

Results and Analysis

The overall process of olfaction in mouse ORNs seems to match that observed in frog ORNs. The unitary response was the same across odorants and cells, even though the odorants varied in efficacy and each cell had different conditions and receptors.

The unitary response of neurons from mice with less of the needed G protein was also the same. This adds evidence to the theory that there is little or no amplification cascade involving those proteins, which would otherwise have a nonlinear response varying with their density.

The total number of receptor bindings needed to signal the brain was estimated at 20-25 unitary events, increasing slightly at lower (room) temperature. This is comparable to the 35 events predicted as a threshold upper bound for frog ORNs.

Some parts of this analysis differed significantly from the frog ORN study. A completely Ca2+-free solution was used, which avoids negative feedback and adaptation, but also enhances receptor current via an inward Cl- current.

Further study is needed on the olfactory threshold at consciousness. It is hypothesized that it may require only one or a few ORNs are needed to trigger perception.

References

• Elementary Response of Olfactory Receptor Neurons to Odorants . V Bhandawat, J Reisert, K-W Yau, Science (2005)
• Signaling by olfactory receptor neurons near threshold. V Bhandaat, J Reisert, K-W Yau, PNAS (2010)
• The electrochemical basis of odor transduction in vertebrate olfactory cilia. SJ Kleene, Chem Senses (2008)

Theoretical and Practical Relevance

This paper replicates the results of Bhandawat, Reisert, and Yau (which used frog ORNs) with mouse ORNs. It confirms the low amplification of smells at the single-neuron level, and provides a first upper bound on the number of odorant-binding events needed to trigger a signal in an ORN.