Odor-Specific, Olfactory Marker Protein-Mediated Sparsening of Primary Olfactory Input to the Brain after Odor Exposure

Abstract

Long-term plasticity in sensory systems is usually conceptualized as changing the interpretation of the brain of sensory information, not an alteration of how the sensor itself responds to external stimuli. However, here we demonstrate that, in the adult mouse olfactory system, a 1-week-long exposure to an artificially odorized environment narrows the range of odorants that can induce neurotransmitter release from olfactory sensory neurons (OSNs) and reduces the total transmitter release from responsive neurons. In animals heterozygous for the olfactory marker protein (OMP), this adaptive plasticity was strongest in the populations of OSNs that originally responded to the exposure odorant (an ester) and also observed in the responses to a similar odorant (another ester) but had no effect on the responses to odorants dissimilar to the exposure odorant (a ketone and an aldehyde). In contrast, in OMP knock-out mice, odorant exposure reduced the number and amplitude of OSN responses evoked by all four types of odorants equally. The effect of this plasticity is to preferentially sparsen the primary neural representations of common olfactory stimuli, which has the computational benefit of increasing the number of distinct sensory patterns that could be represented in the circuit and might thus underlie the improvements in olfactory discrimination often observed after odorant exposure (Mandairon et al., 2006a). The absence of odorant specificity in this adaptive plasticity in OMP knock-out mice suggests a potential role for this protein in adaptively reshaping OSN responses to function in different environments.

Poor human olfaction is a 19th-century myth

“…Critically, new evidence shows that 60% of human olfactory receptor “pseudogenes” are actually transcribed into mRNA in the human olfactory epithelium (22) and work in model organisms suggests that some olfactory receptor pseudogenes may actually result in functional receptors (23). Should these non-coding RNAs or unexpectedly-coding RNAs turn out to be a powerful regulatory network unique to primates (say, for matching olfactory receptor gene expression to the environment; 24, 25), would we then conclude that it is the basis for superior olfactory function in primates? If not, then we must be wary of confirmation bias whenever we find data “consistent with” a weak olfactory sense in humans.…”

Axonal ribosomes and mRNAs associate with fragile X granules in adult rodent and human brains

“…Therefore, we propose that FXGs regulate local translation in the mature axonal arbour, likely in the context of adult plasticity. In support of such a role, mammalian brain axons contain transcripts encoding the plasticity-related proteins b-catenin, a regulator of synaptic vesicle distribution (48,49) and OMP, which modulates odorinduced signal transduction (50)(51)(52)(53).…”

Associative learning and sensory neuroplasticity: how does it happen and what is it good for?

“…Reductions in firing rate or in the number of neurons responding to a stimulus (Gdalyahu et al 2012;Kass et al 2013b) may thus reflect an optimization of stimulus representations according to metabolic constraints, while changes in spike timing or synchrony (Bao et al 2004;Weinberger et al 2013;Kay 2015) or increases in neural response to one stimulus balanced by decreased response to other stimuli (Froemke et al 2013) present potentially metabolically neutral mechanisms for encoding stimulus importance. In this light the large increases in stimulus-evoked synaptic activity (Kass et al 2013d) and action potential firing rates (Bakin and Weinberger 1990;Polley et al 2004) after conditioning constitute an investment of significant resources that presumably serves an important purpose.…”