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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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The projections from the olfactory bulb to cortical amygdala are required for innate aversion and attraction to odorsa, Coronal section of a mouse olfactory bulb injected with AAV5-eNpHR3.0-eYFP. b, Magnified view of an olfactory bulb showing eNpHR3.0-eYFP expression in mitral cells. c, Coronal section depicting the placement of an optical fiber in cortical amygdala, above the axonal output from the olfactory bulb. Scale bar indicates 500 μm (a,c) and 100 μm (b). d,e, Mice were optically coupled to a yellow laser and tested in the behavioral assay for the response to TMT (d) or 2-phenylethanol (2PE) (e) with and without laser stimulation. The percent time each animal spent in the odor quadrant in the absence or presence of photoactivation. f, The mean performance index for mice exposed to TMT. The black bar indicates the average response of all mice to TMT in the absence of photoactivation, and the yellow bars indicate responses to TMT with photoactivation for different experimental animals. Bulb halo and CoA halo describe mice with halorhodopsin expression in the olfactory bulb and cortical amygdala, respectively. Optical fibers were placed above the bulb (n=3), cortical amygdala (CoA, n=11), olfactory tubercle (OT, n=7) or in piriform cortex (Pir, n=8) as denoted below site of injection. The last two bars on the right side have either halorhodopsin in the neurons of cortical amygdala (n=5), or receive no viral injection (n=4), and fibers implanted into cortical amygdala. g, The mean performance index for mice exposed to 2-phenylethanol in the absence and presence of photoactivation (n=6). f,g, *P < 0.05, **P < 0.01, ***P < 0.001 paired t-test comparing PI with and without laser for each group; error bars indicate SEM.
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Figure 2: The projections from the olfactory bulb to cortical amygdala are required for innate aversion and attraction to odorsa, Coronal section of a mouse olfactory bulb injected with AAV5-eNpHR3.0-eYFP. b, Magnified view of an olfactory bulb showing eNpHR3.0-eYFP expression in mitral cells. c, Coronal section depicting the placement of an optical fiber in cortical amygdala, above the axonal output from the olfactory bulb. Scale bar indicates 500 μm (a,c) and 100 μm (b). d,e, Mice were optically coupled to a yellow laser and tested in the behavioral assay for the response to TMT (d) or 2-phenylethanol (2PE) (e) with and without laser stimulation. The percent time each animal spent in the odor quadrant in the absence or presence of photoactivation. f, The mean performance index for mice exposed to TMT. The black bar indicates the average response of all mice to TMT in the absence of photoactivation, and the yellow bars indicate responses to TMT with photoactivation for different experimental animals. Bulb halo and CoA halo describe mice with halorhodopsin expression in the olfactory bulb and cortical amygdala, respectively. Optical fibers were placed above the bulb (n=3), cortical amygdala (CoA, n=11), olfactory tubercle (OT, n=7) or in piriform cortex (Pir, n=8) as denoted below site of injection. The last two bars on the right side have either halorhodopsin in the neurons of cortical amygdala (n=5), or receive no viral injection (n=4), and fibers implanted into cortical amygdala. g, The mean performance index for mice exposed to 2-phenylethanol in the absence and presence of photoactivation (n=6). f,g, *P < 0.05, **P < 0.01, ***P < 0.001 paired t-test comparing PI with and without laser for each group; error bars indicate SEM.

Mentions: Bilateral injection of an adeno-associated virus (AAV) encoding halorhodopsin fused to eYFP (AAV-syn-eNpHR3.0-eYFP) results in expression in the vast majority of mitral cells in the olfactory bulb (80%±7 SD; Fig. 2a,b). Intrinsic neurons within the bulb also express halorhodopsin-eYFP, but mitral and tufted cells provide the only feed-forward excitatory output to cortical centers. In initial experiments, we asked whether silencing of neurons within the olfactory bulb suppressed the innate behavior elicited by TMT. After bilateral infection, both olfactory bulbs were illuminated by introducing optical fibers coupled to a 561nm laser above the dorsal surface of the bulb. Previous experiments suggest that the glomeruli responsible for innate behavior are restricted to the dorsal bulb7. Mice were then introduced into the behavioral chamber in which TMT was present within one quadrant and innate aversion was examined in the absence or presence of 561nm illumination to silence bulbar activity. We observed that light-activated silencing of the olfactory bulb significantly suppressed the aversion to TMT with a reduction in the PI from −82±3.8 to −18±2.9 (n=3). These experiments demonstrate that these viral injections into the bulb result in halorhodopsin expression in neurons essential for innate aversive behavior.


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

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

The projections from the olfactory bulb to cortical amygdala are required for innate aversion and attraction to odorsa, Coronal section of a mouse olfactory bulb injected with AAV5-eNpHR3.0-eYFP. b, Magnified view of an olfactory bulb showing eNpHR3.0-eYFP expression in mitral cells. c, Coronal section depicting the placement of an optical fiber in cortical amygdala, above the axonal output from the olfactory bulb. Scale bar indicates 500 μm (a,c) and 100 μm (b). d,e, Mice were optically coupled to a yellow laser and tested in the behavioral assay for the response to TMT (d) or 2-phenylethanol (2PE) (e) with and without laser stimulation. The percent time each animal spent in the odor quadrant in the absence or presence of photoactivation. f, The mean performance index for mice exposed to TMT. The black bar indicates the average response of all mice to TMT in the absence of photoactivation, and the yellow bars indicate responses to TMT with photoactivation for different experimental animals. Bulb halo and CoA halo describe mice with halorhodopsin expression in the olfactory bulb and cortical amygdala, respectively. Optical fibers were placed above the bulb (n=3), cortical amygdala (CoA, n=11), olfactory tubercle (OT, n=7) or in piriform cortex (Pir, n=8) as denoted below site of injection. The last two bars on the right side have either halorhodopsin in the neurons of cortical amygdala (n=5), or receive no viral injection (n=4), and fibers implanted into cortical amygdala. g, The mean performance index for mice exposed to 2-phenylethanol in the absence and presence of photoactivation (n=6). f,g, *P < 0.05, **P < 0.01, ***P < 0.001 paired t-test comparing PI with and without laser for each group; error bars indicate SEM.
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Figure 2: The projections from the olfactory bulb to cortical amygdala are required for innate aversion and attraction to odorsa, Coronal section of a mouse olfactory bulb injected with AAV5-eNpHR3.0-eYFP. b, Magnified view of an olfactory bulb showing eNpHR3.0-eYFP expression in mitral cells. c, Coronal section depicting the placement of an optical fiber in cortical amygdala, above the axonal output from the olfactory bulb. Scale bar indicates 500 μm (a,c) and 100 μm (b). d,e, Mice were optically coupled to a yellow laser and tested in the behavioral assay for the response to TMT (d) or 2-phenylethanol (2PE) (e) with and without laser stimulation. The percent time each animal spent in the odor quadrant in the absence or presence of photoactivation. f, The mean performance index for mice exposed to TMT. The black bar indicates the average response of all mice to TMT in the absence of photoactivation, and the yellow bars indicate responses to TMT with photoactivation for different experimental animals. Bulb halo and CoA halo describe mice with halorhodopsin expression in the olfactory bulb and cortical amygdala, respectively. Optical fibers were placed above the bulb (n=3), cortical amygdala (CoA, n=11), olfactory tubercle (OT, n=7) or in piriform cortex (Pir, n=8) as denoted below site of injection. The last two bars on the right side have either halorhodopsin in the neurons of cortical amygdala (n=5), or receive no viral injection (n=4), and fibers implanted into cortical amygdala. g, The mean performance index for mice exposed to 2-phenylethanol in the absence and presence of photoactivation (n=6). f,g, *P < 0.05, **P < 0.01, ***P < 0.001 paired t-test comparing PI with and without laser for each group; error bars indicate SEM.
Mentions: Bilateral injection of an adeno-associated virus (AAV) encoding halorhodopsin fused to eYFP (AAV-syn-eNpHR3.0-eYFP) results in expression in the vast majority of mitral cells in the olfactory bulb (80%±7 SD; Fig. 2a,b). Intrinsic neurons within the bulb also express halorhodopsin-eYFP, but mitral and tufted cells provide the only feed-forward excitatory output to cortical centers. In initial experiments, we asked whether silencing of neurons within the olfactory bulb suppressed the innate behavior elicited by TMT. After bilateral infection, both olfactory bulbs were illuminated by introducing optical fibers coupled to a 561nm laser above the dorsal surface of the bulb. Previous experiments suggest that the glomeruli responsible for innate behavior are restricted to the dorsal bulb7. Mice were then introduced into the behavioral chamber in which TMT was present within one quadrant and innate aversion was examined in the absence or presence of 561nm illumination to silence bulbar activity. We observed that light-activated silencing of the olfactory bulb significantly suppressed the aversion to TMT with a reduction in the PI from −82±3.8 to −18±2.9 (n=3). These experiments demonstrate that these viral injections into the bulb result in halorhodopsin expression in neurons essential for innate aversive behavior.

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