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. 2016 Dec 7;36(49):12321-12327.
doi: 10.1523/JNEUROSCI.1991-16.2016.

Postnatal Odor Exposure Increases the Strength of Interglomerular Lateral Inhibition Onto Olfactory Bulb Tufted Cells

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Free PMC article

Postnatal Odor Exposure Increases the Strength of Interglomerular Lateral Inhibition Onto Olfactory Bulb Tufted Cells

Matthew Geramita et al. J Neurosci. .
Free PMC article

Abstract

Lateral inhibition between pairs of olfactory bulb (OB) mitral cells (MCs) and tufted cells (TCs) is linked to a variety of computations including gain control, decorrelation, and gamma-frequency synchronization. Differential effects of lateral inhibition onto MCs and TCs via distinct lateral inhibitory circuits are one of several recently described circuit-level differences between MCs and TCs that allow each to encode separate olfactory features in parallel. Here, using acute OB slices from mice, we tested whether lateral inhibition is affected by prior odor exposure and if these effects differ between MCs and TCs. We found that early postnatal odor exposure to the M72 glomerulus ligand acetophenone increased the strength of interglomerular lateral inhibition onto TCs, but not MCs, when the M72 glomerulus was stimulated. These increases were specific to exposure to M72 ligands because exposure to hexanal did not increase the strength of M72-mediated lateral inhibition. Therefore, early life experiences may be an important factor shaping TC odor responses.

Significance statement: Responses of olfactory (OB) bulb mitral cells (MCs) and tufted cells (TCs) are known to depend on prior odor exposure, yet the specific circuit mechanisms underlying these experience-dependent changes are unknown. Here, we show that odor exposure alters one particular circuit element, interglomerular lateral inhibition, which is known to be critical for a variety of OB computations. Early postnatal odor exposure to acetophenone, a ligand of M72 olfactory sensory neurons, increases the strength of M72-mediated lateral inhibition onto TCs, but not MCs, that project to nearby glomeruli. These findings add to a growing list of differences between MCs and TCs suggesting that that these two cell types play distinct roles in odor coding.

Keywords: electrophysiology; lateral inhibition; olfaction; olfactory bulb; plasticity.

Figures

Figure 1.
Figure 1.
Postnatal exposure to the M72 ligand Ace increases the strength of M72-mediated lateral inhibition onto TCs, but not MCs. a, b, Schematic and example of recording from a MC that projects to a glomerulus near the M72 glomerulus in M72-ChR2-YFP mice. GL, Glomerular layer. Photostimulation of the M72 glomerulus (10 ms light pulse) evokes inhibitory currents. c, Litters were exposed to MO, Ace, or Hex beginning at P0 by daily application of the odor to the nipples of the dam. Experiments measuring M72-mediated lateral inhibition are performed between P17 and P20. d, Examples of M72-mediated lateral inhibition onto MCs (top) or TCs (bottom) from MO-exposed mice (left; black), Ace-exposed mice (middle; red), or Hex-exposed mice (right; blue). Inhibitory responses were grouped into early phase (<250 ms) and late phase (>250 ms) responses. eh, Both the peak amplitude (e) and charge transferred (g) of early and late phases of inhibition are increased in TCs, but not MCs, from Ace-exposed animals (“x” indicates cells lacking an apical dendrite). The MC/TC ratio of the peak amplitude (f) or charge transferred (h) between cells recorded sequentially in the same slice was significantly reduced in Ace-exposed animals. Data were taken from 24 MCs (MO: 10 cells, 8 animals, 2 litters; Ace: 9 cells, 9 animals, 3 litters; Hex: 9 cells, 8 animals, 2 litters) and 30 TCs (MO: 9 cells, 8 animals, 2 litters; Ace: 14 cells, 10 animals, 3 litters; Hex: 8 cells, 5 animals, 2 litters). *p < 0.05, **p < 0.01, ***p < 0.001. Data are presented as mean ± SEM.
Figure 2.
Figure 2.
Extent of the increase in M72-mediated lateral inhibition onto TCs after Ace exposure scales with the total amount of M72 activation. a, Amplitude of the early phase of M72-mediated lateral inhibition onto TCs from Ace-exposed animals is significantly correlated with the age of the animal when the recording was performed (r = 0.64, p = 0.014). bd, This correlation is not due to developmental increases in the strength of lateral inhibition. b, There is no correlation between animal age and the strength of lateral inhibition onto MCs from Ace-exposed animals (r = 0.22, p = 0.57). c, d, There is no correlation between animal age and the strength of lateral inhibition onto TCs from MO-exposed (c; r = 0.17, p = 0.66) or Hex-exposed (d; r = 0.29, 0.49) animals. Significance was assessed using Pearson's correlation.
Figure 3.
Figure 3.
Postnatal odor exposure does not affect the frequency or amplitude of sIPSCs in M/TCs innervating glomeruli near the M72 glomerulus. a, Representative traces (2 s) of sIPSCs and the average sIPSC in MCs (top) and TCs (bottom) from MO-exposed (black), Ace-exposed (red), or Hex-exposed (blue) mice. Average sIPSCs are calculated from 14,848 events in MO-exposed MCs (9 cells, 8 animals, 2 litters); 13,793 events in Ace-exposed MCs (9 cells, 9 animals, 3 litters); 14,564 events in Hex-exposed (9 cells, 8 animals, 2 litters) MCs. Average sIPSCs are calculated from 11,392 events in MO-exposed TCs (9 cells, 8 animals, 2 litters); 16,458 events in Ace-exposed TCs (14 cells, 10 animals, 3 litters); 9646 events in Hex-exposed TCs (8 cells, 5 animals, 2 litters). b, c, sIPSC frequency (b) and amplitude (c) do not differ between MCs and TCs from MO-exposed, Ace-exposed, and Hex-exposed mice. “x” indicates cells lacking an apical dendrite.

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