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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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Location of optical fibers implanted in cortical amygdala for photoactivation of halorhodopsinSchematics show coronal sections throughout most of the region containing cortical amygdala. The posterolateral cortical amygdala is highlighted in gray and the location of bilaterally implanted fibers is indicated.
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Figure 6: Location of optical fibers implanted in cortical amygdala for photoactivation of halorhodopsinSchematics show coronal sections throughout most of the region containing cortical amygdala. The posterolateral cortical amygdala is highlighted in gray and the location of bilaterally implanted fibers is indicated.

Mentions: We then employed optical silencing of the individual targets18 of the olfactory bulb to identify the olfactory centers necessary to elicit innate behavior. Photostimulation of the cortical amygdala (Extended Data Fig. 2), for example, in mice expressing halorhodopsin in bulbar neurons should selectively silence bulbar input to this brain structure without affecting input to other olfactory centers. Mice were coupled to a 561nm laser and were placed in the four-field behavioral assay with TMT in a single quadrant. Each of eleven mice exhibited a striking reduction in the avoidance of the TMT quadrant upon bilateral illumination of the cortical amygdala (PI= −65±3.4 without photostimulation, and −7.9±8.4 upon optical silencing) (Fig. 2d). Further, silencing bulbar input significantly reduced the freezing behavior as evidenced by decreased bouts of inactivity (Extended Data Fig. 3). The inhibition of innate avoidance observed upon optical silencing of the cortical amygdala was reversible; robust avoidance re-emerged upon cessation of light-induced silencing (PI= −74±5.7). In control animals not injected with virus, aversive behavior was not impaired by photostimulation (Fig. 2f). We determined the efficacy of silencing upon illumination of bulbar axons by analyzing c-fos activity. We observe a 70% reduction in the frequency of cells activated by odor in cortical amygdala but not olfactory tubercle or piriform cortex (Extended Data Fig. 4). These results demonstrate that axonal silencing is sufficient and suggests that antidromic hyperpolarization is not responsible for the suppression of behavior.


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

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

Location of optical fibers implanted in cortical amygdala for photoactivation of halorhodopsinSchematics show coronal sections throughout most of the region containing cortical amygdala. The posterolateral cortical amygdala is highlighted in gray and the location of bilaterally implanted fibers is indicated.
© Copyright Policy
Related In: Results  -  Collection

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

Figure 6: Location of optical fibers implanted in cortical amygdala for photoactivation of halorhodopsinSchematics show coronal sections throughout most of the region containing cortical amygdala. The posterolateral cortical amygdala is highlighted in gray and the location of bilaterally implanted fibers is indicated.
Mentions: We then employed optical silencing of the individual targets18 of the olfactory bulb to identify the olfactory centers necessary to elicit innate behavior. Photostimulation of the cortical amygdala (Extended Data Fig. 2), for example, in mice expressing halorhodopsin in bulbar neurons should selectively silence bulbar input to this brain structure without affecting input to other olfactory centers. Mice were coupled to a 561nm laser and were placed in the four-field behavioral assay with TMT in a single quadrant. Each of eleven mice exhibited a striking reduction in the avoidance of the TMT quadrant upon bilateral illumination of the cortical amygdala (PI= −65±3.4 without photostimulation, and −7.9±8.4 upon optical silencing) (Fig. 2d). Further, silencing bulbar input significantly reduced the freezing behavior as evidenced by decreased bouts of inactivity (Extended Data Fig. 3). The inhibition of innate avoidance observed upon optical silencing of the cortical amygdala was reversible; robust avoidance re-emerged upon cessation of light-induced silencing (PI= −74±5.7). In control animals not injected with virus, aversive behavior was not impaired by photostimulation (Fig. 2f). We determined the efficacy of silencing upon illumination of bulbar axons by analyzing c-fos activity. We observe a 70% reduction in the frequency of cells activated by odor in cortical amygdala but not olfactory tubercle or piriform cortex (Extended Data Fig. 4). These results demonstrate that axonal silencing is sufficient and suggests that antidromic hyperpolarization is not responsible for the suppression of 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