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. 2016 Nov 16;36(46):11646-11653.
doi: 10.1523/JNEUROSCI.0654-16.2016.

Early Odorant Exposure Increases the Number of Mitral and Tufted Cells Associated With a Single Glomerulus

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Free PMC article

Early Odorant Exposure Increases the Number of Mitral and Tufted Cells Associated With a Single Glomerulus

Annie Liu et al. J Neurosci. .
Free PMC article

Abstract

The highly specific organization of the olfactory bulb (OB) is well known, but the impact of early odorant experience on its circuit structure is unclear. Olfactory sensory neurons (OSNs) project axons from the olfactory epithelium to the OB, where they form spherical neuropil structures called glomeruli. These glomeruli and the postsynaptic targets of OSNs, including mitral and tufted cells (M/TCs) and juxtaglomerular cells, form glomerular modules, which represent the basic odor-coding units of the OB. Here, we labeled M/TCs within a single glomerular module of the mouse OB and show that odorant exposure that starts prenatally and continues through postnatal day 25 has a major impact on the structure of the glomerular module. We confirm that exposure increases the volume of the activated glomeruli and show that exposure increases M/TC number by >40% in a glomerulus-specific fashion. Given the role of M/TCs in OB output and in lateral inhibition, increasing the number of M/TCs connected to a single glomerulus may also increase the influence of that glomerulus on the OB network and on OB output. Our results show that early odorant exposure has a profound effect on OB connectivity and thus may affect odorant processing significantly.

Significance statement: Experience shapes neural circuits in a variety of ways, most commonly by changing the strength of activated connections. Relatively little is known about how experience changes circuitry in the olfactory system. Here, we show that for a genetically identified glomerulus in the mouse olfactory bulb, early odorant exposure increases the number of associated mitral and tufted cells by 40% and 100%, respectively. Understanding the structural changes induced by early odorant experience can provide insight into how bulbar organization gives rise to efficient processing. We find that odorant experience increases the number of projection neurons associated with a single glomerulus significantly, a dramatic and long-lasting structural change that may have important functional implications.

Keywords: glomerulus; mitral cells; olfaction; plasticity.

Figures

Figure 1.
Figure 1.
Prenatal and early postnatal methyl salicylate exposure increases M72 glomerulus volume and changes food preference. A, Prenatal and early postnatal odorant exposure using food odorized with methyl salicylate (mint, 1% by volume) increases the size of the lateral and medial M72 glomeruli, but food odorized with hexanal (hexanal, 1% by volume) has no effect. *p < 0.01. B, Maximum projection images of example glomeruli of control and odor-exposed (mint and hexanal) animals at P25–P35. Scale bar, 50 μm. C, Prenatal and early postnatal odorant exposure using food odorized with methyl salicylate (mint, 1% by volume) or hexanal (1% by volume) increases the ratio of time spent sniffing scented food to total time spent sniffing food. Key: Control | M, Control mice in preference test between methyl-salicylate-scented and control food; Mint | M, methyl-salicylate-exposed animals in preference test between methyl-salicylate-scented and control food; Control | H, control mice in preference test between hexanal-scented and control food; Hexanal | H, hexanal-exposed animals in preference test between hexanal-scented and control food. *p < 0.05. D, Schematic of three glomeruli with basic postsynaptic targets comprising three glomerular modules. Example M72 glomerulus is labeled, along with periglomerular cells (PG), TCs (T), and mitral cells (M). E, Example maximum projection image of electroporation-labeled M72 glomerulus (control) showing GFP-expressing OSN axons coalescing into a single glomerulus and Alexa Fluor 594 hydrazide-filled JGCs and M/TCs. Scale bar, 50 μm.
Figure 2.
Figure 2.
Prenatal and early postnatal methyl salicylate exposure increases the number of M72 M/TCs. A, Number of M/TCs connected to the lateral M72 glomerulus increases after methyl salicylate exposure. Black-filled and open circles indicate electroporation of control animals with Alexa Fluor 594 hydrazide; gray-filled and open circles indicate electroporation of control animals with Alexa Fluor 594 dextran; and red-filled and open circles indicate electroporation of methyl-salicylate-exposed animals with Alexa Fluor 594 dextran. Data are shown as means ± SD. *p < 0.0001. B, C, Spatial distribution of MCs and TCs corresponding to control (black circles, 11 animals, 74 total MCs, 32 total TCs) and odor-exposed (mint) animals (red circles, 8 animals, 80 total MCs, 51 total TCs). Green circle indicates M72 glomerulus location. Histograms of cell position are next to the corresponding axes. Black-outlined bars indicate control; red solid bars indicate mint. B, Sagittal view. C, Horizontal view. Comparison of median spatial locations was nonsignificant.
Figure 3.
Figure 3.
In vivo electroporation labels the postsynaptic targets of a single glomerulus reliably. A, Sequential dual-color electroporation of control M72 glomerulus using a theta glass electrode and no change in electrode tip position between sequential single-color electroporations of Alexa Fluor 594 dextran and Alexa Fluor 488 dextran. A1, Maximum projection image of one physical section containing the M72 glomerulus and dual-labeled JGCs and M/TCs. A2, Optical section from physical section from A1. White arrowhead indicates dual-labeled TC soma. B, C, Optical sections from separate sequential dual-color electroporations of two control M72 glomeruli using a theta glass electrode and ∼20 μm movement of electrode tip position between single-color electroporations of Alexa Fluor 594 dextran and Alexa Fluor 488 dextran. White arrowheads indicate dual-labeled MC somata. D, Optical section from dual-color electroporation of control M72 glomerulus using two separate electrodes backfilled with either Alexa Fluor 594 dextran or Alexa Fluor 488 dextran. White arrowhead indicates dual-labeled MC. Scale bar, 50 μm.

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