Peripheral Adaptation Codes for High Odor Concentration in Glomeruli

Abstract

Adaptation is a general property of sensory receptor neurons and has been extensively studied in isolated cell preparation of olfactory receptor neurons. In contrast, little is known about the conditions under which peripheral adaptation occurs in the CNS during odorant stimulation. Here, we used two-photon laser-scanning microscopy and targeted extracellular recording in freely breathing anesthetized rats to investigate the correlate of peripheral adaptation at the first synapse of the olfactory pathway in olfactory bulb glomeruli. We find that during sustained stimulation at high concentration, odorants can evoke local field potential (LFP) postsynaptic responses that rapidly adapt with time, some within two inhalations. Simultaneous measurements of LFP and calcium influx at olfactory receptor neuron terminals reveal that postsynaptic adaptation is associated with a decrease in odorant-evoked calcium response, suggesting that it results from a decrease in glutamate release. This glomerular adaptation was concentration-dependent and did not change the glomerular input-output curve. In addition, in situ application of antagonists of either ionotropic glutamate receptors or metabotropic GABA B receptors did not affect this adaptation, thus discarding the involvement of local presynaptic inhibition. Glomerular adaptation, therefore, reflects the response decline of olfactory receptor neurons to sustained odorant. We postulate that peripheral fast adaptation is a means by which glomerular output codes for high concentration of odor.

What Does Local Functional Hyperemia Tell about Local Neuronal Activation?

“…This phenomenon did not involve postsynaptic processing but resulted from a decrease of presynaptic Ca 2ϩ signals in ORN terminals and thus a decrease of the amount of glutamate released by these terminals. Because presynaptic GABA B receptors (Aroniadou-Anderjaska et al, 2000;Murphy and Isaacson, 2003;Vucinic et al, 2006;Pírez and Wachowiak, 2008), dopamine receptors (Hsia et al, 1999), or purinergic receptors (our unpublished observations) were not involved in the phenomenon (Lecoq et al, 2009), we could conclude that presynaptic Ca 2ϩ signal adaptation indirectly reflected peripheral adaptation. Figure 1, C and D, illustrates that, during such peripheral adaptation, the overall presynaptic Ca 2ϩ signal from ORNs and the vascular response uncoupled; during strong odor stimulation (Fig.…”

“…Animals continuously breathed filtered air enriched with oxygen (20 -30%). Olfactory nerve terminals were labeled with Ca 2ϩ green 1 dextran, 10 kDa (Invitrogen), 2-8 d before experiments, as described previously (Lecoq et al, 2009). To label vessels, a bolus of 70 kDa Texas Red dextran was injected intravenously through a catheter placed in the femoral vein.…”

“…We have recently shown that peripheral adaptation can also be detected centrally in glomeruli, with LFP responses decreasing upon strong odorant stimulation (Lecoq et al, 2009). This phenomenon did not involve postsynaptic processing but resulted from a decrease of presynaptic Ca 2ϩ signals in ORN terminals and thus a decrease of the amount of glutamate released by these terminals.…”

“…LFP negativities thus reflect the summation of EPSP in glomeruli. More recently, we have labeled ORN terminals with the calcium sensor, calcium green 1 (Lecoq et al, 2009), and shown that LFP rapid negativities are tightly correlated to presynaptic calcium (Ca 2ϩ ) signals detected in ORN terminals converging into the same glomerulus. This correlation is surprisingly strong and independent of odor stimulation intensity, suggesting that presynaptic Ca 2ϩ signals could be considered as solid markers of the amount of glutamate released onto the glomerular dendrites that generate LFP negativities.…”

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

“…However, previous studies have shown that simply changing a mouse's home cage can cause robust neuroanatomical changes (Oliva et al, 2010) to olfactory bulb glomeruli that are affected by exposure to naturally produced rodent cage odors (Oliva et al, 2008). Other laboratories have also reported notable changes in olfactory discrimination by simply enriching the olfactory environment with scent-containing mesh spheres (Mandairon et al, 2006a,b), suggesting that the sensory experience of a laboratory rodent may be so impoverished that modest environmental changes are sufficient to cause substantial alterations in neural function (Krech et al, 1962;Baroncelli et al, 2010). OMP-null mice did not show this enhancement in the SE group and in fact showed a decrease in odorant-responsive glomeruli and the size of their OSN synaptic inputs.…”