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, 28 (49), 13106-11

Learning-dependent Structural Plasticity in the Adult Olfactory Pathway

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Learning-dependent Structural Plasticity in the Adult Olfactory Pathway

Seth V Jones et al. J Neurosci.

Abstract

Olfactory learning in humans leads to enhanced perceptual discrimination of odor cues. Examining mouse models of both aversive and appetitive conditioning, we demonstrate a mechanism which may underlie this adult learning phenomenon. Topographically unique spatial wiring of the olfactory system allowed us to demonstrate that emotional learning of odor cues alters the primary sensory representation within the nose and brain of adult mice. Transgenic mice labeled at the M71 odorant receptor (specifically activated by the odorant acetophenone) were behaviorally trained with olfactory-dependent fear conditioning or conditioned place preference using acetophenone. Odor-trained mice had larger M71-specific glomeruli and an increase in M71-specific sensory neurons within the nose compared with mice that were untrained, trained to a non-M71 activating odorant, or had nonassociative pairings of acetophenone. These data indicate that the primary sensory neuron population and its projections may remain plastic in adults, providing a structural mechanism for learning-enhanced olfactory sensitivity and discrimination.

Figures

Figure 1.
Figure 1.
Increased M71 axon density and glomerular size with fear conditioning. A, SR-Lab Response software controls a solenoid switch (red arrows) which allows compressed air to flow through the odorant jar and into the startle chamber. When closed, clean air flows with no difference in airflow. Backflow is prevented by a series of one-way valves (yellow arrows). The odor is removed via an exhaust hose (green arrow) by outflow fan. Shock is generated by a programmable animal shocker and is delivered through the bars in the cage floor. During behavioral testing, startle is elicited by a 105 dB white noise burst. Activity and startle amplitude are measured by a piezoelectronic device beneath the floor of the cage. B, Cross-section of an olfactory bulb from a homecage mouse (top left, LacZ; top right, DAPI stain) or from an acetophenone + shock paired mouse (bottom left, LacZ; bottom right, DAPI stain). C, Medial and dorsal pairs of M71 glomeruli in X-gal stained olfactory bulbs from M71–IRES–tauLacZ mice. D, Glomerular surface area was larger in the acetophenone + shock trained group than in the homecage group (p < 0.05). E, Glomerular cross-sectional area was larger in the acetophenone-trained versus the homecage mice, *p < 0.05.
Figure 2.
Figure 2.
M71 glomerular size increases require associative learning. A, Glomerular cross-sectional area was larger in the acetophenone + shock group than either the acetophenone-alone or the homecage groups; *p < 0.01 for acetophenone + shock versus homecage; *p < 0.05 for acetophenone + shock versus acetophenone-alone. B, Mice learn an odor-shock association to both propanol and acetophenone and can discriminate between the two odors, p < 0.001. C, Glomerular cross-sectional areas were greater in the acetophenone + shock versus homecage, acetophenone-alone, and propanol-shock groups; *p < 0.05 for each group versus acetophenone + shock.
Figure 3.
Figure 3.
Associative learning leads to increases in olfactory sensory neuron number. A, Olfactory sensory neurons in the olfactory epithelium of an acetophenone + shock trained (top) and homecage mouse (bottom). B, More M71-LacZ+ olfactory sensory neurons were found in acetophenone-trained than homecage mice (p < 0.05). C, Glomerular size is positively correlated with increasing olfactory sensory neuron number (triangles, home cage; squares, acetophenone + shock; Pearson's correlation coefficient = 0.62, p < 0.05).
Figure 4.
Figure 4.
Long-lasting glomerular changes result from aversive and appetitive learning. A, Dorsal and medial M71 glomeruli in X-gal stained olfactory bulbs from acetophenone + shock paired mice trained in only 3 consecutive days compared with untrained (no odor) control mice examined 2.5 weeks after training. B, Glomerular area was greater in the 3 d and 3 weeks acetophenone + shock trained versus the homecage mice, *p < 0.05 versus homecage. C, M71 mice learned cocaine CPP equally well with either no odor, or acetophenone paired with the cocaine, *p < 0.05 versus pretrained. D, Glomerular area was greater in mice that were CPP-trained with acetophenone paired with cocaine, versus no odor paired with cocaine, *p < 0.05.

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