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The participation of cortical amygdala in innate, odour-driven behaviour.

Root CM, Denny CA, Hen R, Axel R - Nature (2014)

Bottom Line: Moreover, we use the promoter of the activity-dependent gene arc to express the photosensitive ion channel, channelrhodopsin, in neurons of the cortical amygdala activated by odours that elicit innate behaviours.Optical activation of these neurons leads to appropriate behaviours that recapitulate the responses to innate odours.These data indicate that the cortical amygdala plays a critical role in generating innate odour-driven behaviours but do not preclude its participation in learned olfactory behaviours.

View Article: PubMed Central - PubMed

Affiliation: Department of Neuroscience and the Howard Hughes Medical Institute, College of Physicians and Surgeons, Columbia University, New York, New York 10032, USA.

ABSTRACT
Innate behaviours are observed in naive animals without prior learning or experience, suggesting that the neural circuits that mediate these behaviours are genetically determined and stereotyped. The neural circuits that convey olfactory information from the sense organ to the cortical and subcortical olfactory centres have been anatomically defined, but the specific pathways responsible for innate responses to volatile odours have not been identified. Here we devise genetic strategies that demonstrate that a stereotyped neural circuit that transmits information from the olfactory bulb to cortical amygdala is necessary for innate aversive and appetitive behaviours. Moreover, we use the promoter of the activity-dependent gene arc to express the photosensitive ion channel, channelrhodopsin, in neurons of the cortical amygdala activated by odours that elicit innate behaviours. Optical activation of these neurons leads to appropriate behaviours that recapitulate the responses to innate odours. These data indicate that the cortical amygdala plays a critical role in generating innate odour-driven behaviours but do not preclude its participation in learned olfactory behaviours.

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Locomotor activity of mice during activation of odor responsive neurons within cortical amygdalaMice with odor-driven channelrhodopsin expression were tested in the open field assay where they received pulsed photoactivation upon entrance into the lower right quadrant. a-c, The trajectory graphs (top) show the position of representative animals with ChR2-eYFP in neurons activated by TMT (a), 2-phenylethanol (b) or isoamyl acetate (c). The raster plots (bottom) show quadrant occupancy over time. d, The percent time immobile in the absence and presence of photoactivation. Immobility is defined as velocity less than 1 cm/sec for at least 1 second. a-c, TMT (n=6), 2-phenylethanol (n=4) and isoamyl acetate (n=6); ***P < 0.001 paired t-test comparing with and without laser; error bars show SEM.
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Figure 12: Locomotor activity of mice during activation of odor responsive neurons within cortical amygdalaMice with odor-driven channelrhodopsin expression were tested in the open field assay where they received pulsed photoactivation upon entrance into the lower right quadrant. a-c, The trajectory graphs (top) show the position of representative animals with ChR2-eYFP in neurons activated by TMT (a), 2-phenylethanol (b) or isoamyl acetate (c). The raster plots (bottom) show quadrant occupancy over time. d, The percent time immobile in the absence and presence of photoactivation. Immobility is defined as velocity less than 1 cm/sec for at least 1 second. a-c, TMT (n=6), 2-phenylethanol (n=4) and isoamyl acetate (n=6); ***P < 0.001 paired t-test comparing with and without laser; error bars show SEM.

Mentions: Photoactivation of the cortical amygdala of mice expressing ChR2 after TMT exposure, resulted in avoidance of the optically stimulated quadrant (PI of −49±4.6, n=6) (Fig. 3d) and increased freezing as evidenced by increased immobility (Extended Data Fig. 8). In contrast, mice expressing ChR2 in neurons responsive to the innately attractive odor, 2-phenylethanol, exhibited significant attraction to the quadrant in which the mice received optical stimulation (PI of 42±6.4, n=4) (Fig. 3f). Mice expressing channelrhodopsin in neurons responsive to the neutral odor, isoamyl acetate, did not exhibit any discernible behavioral response upon optical stimulation (PI of 5.6±8.6, n=6) and explored each quadrant equally (Fig. 3e). In control mice, treatment with tamoxifen without odor exposure resulted in ChR2 expression in a very small subpopulation of neurons. These mice did not exhibit any behavioral bias upon photostimulation within a single quadrant (PI of −5.2±7.1, n=3) (Fig. 3g). These experiments demonstrate that odors that elicit innate behaviors of different valence activate different populations of neurons within the cortical amygdala. Moreover, photoactivation of these two distinct populations of neurons is sufficient to elicit an appropriate behavioral response. Thus, these neural representations reflect an essential component in a determined neural circuit wired to elicit an innate behavioral response to odors.


The participation of cortical amygdala in innate, odour-driven behaviour.

Root CM, Denny CA, Hen R, Axel R - Nature (2014)

Locomotor activity of mice during activation of odor responsive neurons within cortical amygdalaMice with odor-driven channelrhodopsin expression were tested in the open field assay where they received pulsed photoactivation upon entrance into the lower right quadrant. a-c, The trajectory graphs (top) show the position of representative animals with ChR2-eYFP in neurons activated by TMT (a), 2-phenylethanol (b) or isoamyl acetate (c). The raster plots (bottom) show quadrant occupancy over time. d, The percent time immobile in the absence and presence of photoactivation. Immobility is defined as velocity less than 1 cm/sec for at least 1 second. a-c, TMT (n=6), 2-phenylethanol (n=4) and isoamyl acetate (n=6); ***P < 0.001 paired t-test comparing with and without laser; error bars show SEM.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4231015&req=5

Figure 12: Locomotor activity of mice during activation of odor responsive neurons within cortical amygdalaMice with odor-driven channelrhodopsin expression were tested in the open field assay where they received pulsed photoactivation upon entrance into the lower right quadrant. a-c, The trajectory graphs (top) show the position of representative animals with ChR2-eYFP in neurons activated by TMT (a), 2-phenylethanol (b) or isoamyl acetate (c). The raster plots (bottom) show quadrant occupancy over time. d, The percent time immobile in the absence and presence of photoactivation. Immobility is defined as velocity less than 1 cm/sec for at least 1 second. a-c, TMT (n=6), 2-phenylethanol (n=4) and isoamyl acetate (n=6); ***P < 0.001 paired t-test comparing with and without laser; error bars show SEM.
Mentions: Photoactivation of the cortical amygdala of mice expressing ChR2 after TMT exposure, resulted in avoidance of the optically stimulated quadrant (PI of −49±4.6, n=6) (Fig. 3d) and increased freezing as evidenced by increased immobility (Extended Data Fig. 8). In contrast, mice expressing ChR2 in neurons responsive to the innately attractive odor, 2-phenylethanol, exhibited significant attraction to the quadrant in which the mice received optical stimulation (PI of 42±6.4, n=4) (Fig. 3f). Mice expressing channelrhodopsin in neurons responsive to the neutral odor, isoamyl acetate, did not exhibit any discernible behavioral response upon optical stimulation (PI of 5.6±8.6, n=6) and explored each quadrant equally (Fig. 3e). In control mice, treatment with tamoxifen without odor exposure resulted in ChR2 expression in a very small subpopulation of neurons. These mice did not exhibit any behavioral bias upon photostimulation within a single quadrant (PI of −5.2±7.1, n=3) (Fig. 3g). These experiments demonstrate that odors that elicit innate behaviors of different valence activate different populations of neurons within the cortical amygdala. Moreover, photoactivation of these two distinct populations of neurons is sufficient to elicit an appropriate behavioral response. Thus, these neural representations reflect an essential component in a determined neural circuit wired to elicit an innate behavioral response to odors.

Bottom Line: Moreover, we use the promoter of the activity-dependent gene arc to express the photosensitive ion channel, channelrhodopsin, in neurons of the cortical amygdala activated by odours that elicit innate behaviours.Optical activation of these neurons leads to appropriate behaviours that recapitulate the responses to innate odours.These data indicate that the cortical amygdala plays a critical role in generating innate odour-driven behaviours but do not preclude its participation in learned olfactory behaviours.

View Article: PubMed Central - PubMed

Affiliation: Department of Neuroscience and the Howard Hughes Medical Institute, College of Physicians and Surgeons, Columbia University, New York, New York 10032, USA.

ABSTRACT
Innate behaviours are observed in naive animals without prior learning or experience, suggesting that the neural circuits that mediate these behaviours are genetically determined and stereotyped. The neural circuits that convey olfactory information from the sense organ to the cortical and subcortical olfactory centres have been anatomically defined, but the specific pathways responsible for innate responses to volatile odours have not been identified. Here we devise genetic strategies that demonstrate that a stereotyped neural circuit that transmits information from the olfactory bulb to cortical amygdala is necessary for innate aversive and appetitive behaviours. Moreover, we use the promoter of the activity-dependent gene arc to express the photosensitive ion channel, channelrhodopsin, in neurons of the cortical amygdala activated by odours that elicit innate behaviours. Optical activation of these neurons leads to appropriate behaviours that recapitulate the responses to innate odours. These data indicate that the cortical amygdala plays a critical role in generating innate odour-driven behaviours but do not preclude its participation in learned olfactory behaviours.

Show MeSH
Related in: MedlinePlus