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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 with Optical suppression in cortical amygdalaa,b Mice with halorhodopsin in the olfactory bulb and optical fibers in cortical amygdala were optically coupled to a yellow laser and tested in the behavioral assay for the response to TMT (a) or 2-phenylethanol (2PE) (b) with and without laser stimulation. The position of a representative mouse during a ten minute period in the presence of TMT (a) or 2-phenylethanol (b) either in the absence (left) or presence (right) of photoactivation during the ten minute behavioral testing. Raster plots show quadrant occupancy over time for each animal (a, n=11; b, n=6). c,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. c, Response to TMT in mice receiving photostimulation of halorhodopsin in 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 cortical amygdala (COA, n=11), olfactory tubercle (OT, n=7) or in piriform cortex (Pir, n=8) as denoted below site of injection. Control animals received no viral injection, and fibers implanted into cortical amygdala (n=4). d, The percent immobility for mice exposed to 2-phenylethanol in the absence and presence of photoactivation of bulbar axons in cortical amygdala (n=6). c,d, *P < 0.05, ***P < 0.001 paired t-test comparing with and without laser; error bars show SEM.
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Figure 7: Locomotor activity of mice with Optical suppression in cortical amygdalaa,b Mice with halorhodopsin in the olfactory bulb and optical fibers in cortical amygdala were optically coupled to a yellow laser and tested in the behavioral assay for the response to TMT (a) or 2-phenylethanol (2PE) (b) with and without laser stimulation. The position of a representative mouse during a ten minute period in the presence of TMT (a) or 2-phenylethanol (b) either in the absence (left) or presence (right) of photoactivation during the ten minute behavioral testing. Raster plots show quadrant occupancy over time for each animal (a, n=11; b, n=6). c,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. c, Response to TMT in mice receiving photostimulation of halorhodopsin in 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 cortical amygdala (COA, n=11), olfactory tubercle (OT, n=7) or in piriform cortex (Pir, n=8) as denoted below site of injection. Control animals received no viral injection, and fibers implanted into cortical amygdala (n=4). d, The percent immobility for mice exposed to 2-phenylethanol in the absence and presence of photoactivation of bulbar axons in cortical amygdala (n=6). c,d, *P < 0.05, ***P < 0.001 paired t-test comparing with and without laser; error bars show SEM.

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)

Locomotor activity of mice with Optical suppression in cortical amygdalaa,b Mice with halorhodopsin in the olfactory bulb and optical fibers in cortical amygdala were optically coupled to a yellow laser and tested in the behavioral assay for the response to TMT (a) or 2-phenylethanol (2PE) (b) with and without laser stimulation. The position of a representative mouse during a ten minute period in the presence of TMT (a) or 2-phenylethanol (b) either in the absence (left) or presence (right) of photoactivation during the ten minute behavioral testing. Raster plots show quadrant occupancy over time for each animal (a, n=11; b, n=6). c,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. c, Response to TMT in mice receiving photostimulation of halorhodopsin in 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 cortical amygdala (COA, n=11), olfactory tubercle (OT, n=7) or in piriform cortex (Pir, n=8) as denoted below site of injection. Control animals received no viral injection, and fibers implanted into cortical amygdala (n=4). d, The percent immobility for mice exposed to 2-phenylethanol in the absence and presence of photoactivation of bulbar axons in cortical amygdala (n=6). c,d, *P < 0.05, ***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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Figure 7: Locomotor activity of mice with Optical suppression in cortical amygdalaa,b Mice with halorhodopsin in the olfactory bulb and optical fibers in cortical amygdala were optically coupled to a yellow laser and tested in the behavioral assay for the response to TMT (a) or 2-phenylethanol (2PE) (b) with and without laser stimulation. The position of a representative mouse during a ten minute period in the presence of TMT (a) or 2-phenylethanol (b) either in the absence (left) or presence (right) of photoactivation during the ten minute behavioral testing. Raster plots show quadrant occupancy over time for each animal (a, n=11; b, n=6). c,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. c, Response to TMT in mice receiving photostimulation of halorhodopsin in 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 cortical amygdala (COA, n=11), olfactory tubercle (OT, n=7) or in piriform cortex (Pir, n=8) as denoted below site of injection. Control animals received no viral injection, and fibers implanted into cortical amygdala (n=4). d, The percent immobility for mice exposed to 2-phenylethanol in the absence and presence of photoactivation of bulbar axons in cortical amygdala (n=6). c,d, *P < 0.05, ***P < 0.001 paired t-test comparing with and without laser; error bars show SEM.
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
Related in: MedlinePlus