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Processing of visually evoked innate fear by a non-canonical thalamic pathway.

Wei P, Liu N, Zhang Z, Liu X, Tang Y, He X, Wu B, Zhou Z, Liu Y, Li J, Zhang Y, Zhou X, Xu L, Chen L, Bi G, Hu X, Xu F, Wang L - Nat Commun (2015)

Bottom Line: Our results demonstrate that neurons in the superior colliculus (SC) are essential for a variety of acute and persistent defensive responses to overhead looming stimuli.Optogenetic mapping revealed that SC projections to the lateral posterior nucleus (LP) of the thalamus, a non-canonical polymodal sensory relay, are sufficient to mimic visually evoked fear responses.Our results reveal a novel collicular-thalamic-Amg circuit important for innate defensive responses to visual threats.

View Article: PubMed Central - PubMed

Affiliation: Shenzhen Key Lab of Neuropsychiatric Modulation and Collaborative Innovation Center for Brain Science, CAS Center for Excellence in Brain Science, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China.

ABSTRACT
The ability of animals to respond to life-threatening stimuli is essential for survival. Although vision provides one of the major sensory inputs for detecting threats across animal species, the circuitry underlying defensive responses to visual stimuli remains poorly defined. Here, we investigate the circuitry underlying innate defensive behaviours elicited by predator-like visual stimuli in mice. Our results demonstrate that neurons in the superior colliculus (SC) are essential for a variety of acute and persistent defensive responses to overhead looming stimuli. Optogenetic mapping revealed that SC projections to the lateral posterior nucleus (LP) of the thalamus, a non-canonical polymodal sensory relay, are sufficient to mimic visually evoked fear responses. In vivo electrophysiology experiments identified a di-synaptic circuit from SC through LP to the lateral amygdale (Amg), and lesions of the Amg blocked the full range of visually evoked defensive responses. Our results reveal a novel collicular-thalamic-Amg circuit important for innate defensive responses to visual threats.

No MeSH data available.


Related in: MedlinePlus

Activation of the LA is temporally correlated with the UF elicited by applying the US to the ILSCm.Schematic (a) and photograph (b) of the two-site multi-channel optrode system. The inset in b shows the tip of the optrode (white box). (c) PSTHs of two example neurons from the ILSCm and LA show different firing patterns in response to the US in the ILSCm (1-s bins). The red line represents the estimation of the expected baseline rate and the grey shaded area represents the confidence limit of 99%. (d) Z-scored population PSTH of responsive neurons from the ILSCm (red) and LA (green) (100-ms bins), shaded areas represent the s.e.m. The blue bar indicates the optical stimulation, red bar indicates the period of excitation of ILSCm neurons (n=7 cells, compared with the pre-event reference period, P<0.01 by right-tailed t-test), and green bar indicates the period of excitation of LA neurons (n=11 cells). (e) The normalized post-stimulation mean firing rates of responsive LA neurons (green) show a significant adaptation after each trial (n=11 cells, main effect P<0.001 by repeated one-way ANOVA). Contrarily, the firing rates of responsive ILSCm neurons (red) did not adapt across trials (n=7 cells, main effect P=0.96 by repeated one-way ANOVA). (f) The ILSCm and LA example neuron activity (top; scaled by the hot colour map) were aligned with the FS with time (the bottom red bars represent the freezing state). Values are represented as mean±s.d.
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f4: Activation of the LA is temporally correlated with the UF elicited by applying the US to the ILSCm.Schematic (a) and photograph (b) of the two-site multi-channel optrode system. The inset in b shows the tip of the optrode (white box). (c) PSTHs of two example neurons from the ILSCm and LA show different firing patterns in response to the US in the ILSCm (1-s bins). The red line represents the estimation of the expected baseline rate and the grey shaded area represents the confidence limit of 99%. (d) Z-scored population PSTH of responsive neurons from the ILSCm (red) and LA (green) (100-ms bins), shaded areas represent the s.e.m. The blue bar indicates the optical stimulation, red bar indicates the period of excitation of ILSCm neurons (n=7 cells, compared with the pre-event reference period, P<0.01 by right-tailed t-test), and green bar indicates the period of excitation of LA neurons (n=11 cells). (e) The normalized post-stimulation mean firing rates of responsive LA neurons (green) show a significant adaptation after each trial (n=11 cells, main effect P<0.001 by repeated one-way ANOVA). Contrarily, the firing rates of responsive ILSCm neurons (red) did not adapt across trials (n=7 cells, main effect P=0.96 by repeated one-way ANOVA). (f) The ILSCm and LA example neuron activity (top; scaled by the hot colour map) were aligned with the FS with time (the bottom red bars represent the freezing state). Values are represented as mean±s.d.

Mentions: In freely behaving mice, we aimed to identify the specific functional mechanism of the ILSCm-LA circuitry by which optical stimulation modulates the neural network activities. We developed a novel two-site multi-channel optrode system for simultaneous recording and light delivery in freely moving mice (Supplementary Fig. 7a) and applied this to stimulate and record in ILSCm, and simultaneous recording from LA (Fig. 4a,b and Supplementary Fig. 7e,f). In mice exhibiting prolonged UF elicited by the US applied to the ChR2:ILSCm mice (n=3), 20 and 40 single-unit spikes were recorded in the ILSCm and LA, respectively (Supplementary Fig. 7b,c). Under direct light-evoked responses, 7 of the 20 local ILSCm cells were found to fire immediately following the pulsed laser, with an average latency of 3.0±1.5 ms, and the cells showed transient excitation during the US (Fig. 4c,d). In addition, 11 of the 40 LA cells were activated by the pulsed-laser stimulation, with a latency distribution comparable to that found in anesthetized mice (Supplementary Fig. 7d,g), and these cells showed sustained post stimulation excitation (Fig. 4c,d). Intriguingly, LA neuronal activation showed adaptation in firing rates among the US trials, whereas ILSCm neuronal activation was invariant (Fig. 4e). By comparing the time courses of the physiological activities and behavioural responses, it was discovered that the activation of LA neurons, rather than that of ILSCm neurons, temporally correlated with the US-elicited UF in ChR2:ILSCm mice (Fig. 4f and Supplementary Fig. 8). These results suggest that activation of the ILSCm represents an ‘on switch' for the brain's defensive system, whereas sustained LA activation is responsible for prolonged freezing in animals.


Processing of visually evoked innate fear by a non-canonical thalamic pathway.

Wei P, Liu N, Zhang Z, Liu X, Tang Y, He X, Wu B, Zhou Z, Liu Y, Li J, Zhang Y, Zhou X, Xu L, Chen L, Bi G, Hu X, Xu F, Wang L - Nat Commun (2015)

Activation of the LA is temporally correlated with the UF elicited by applying the US to the ILSCm.Schematic (a) and photograph (b) of the two-site multi-channel optrode system. The inset in b shows the tip of the optrode (white box). (c) PSTHs of two example neurons from the ILSCm and LA show different firing patterns in response to the US in the ILSCm (1-s bins). The red line represents the estimation of the expected baseline rate and the grey shaded area represents the confidence limit of 99%. (d) Z-scored population PSTH of responsive neurons from the ILSCm (red) and LA (green) (100-ms bins), shaded areas represent the s.e.m. The blue bar indicates the optical stimulation, red bar indicates the period of excitation of ILSCm neurons (n=7 cells, compared with the pre-event reference period, P<0.01 by right-tailed t-test), and green bar indicates the period of excitation of LA neurons (n=11 cells). (e) The normalized post-stimulation mean firing rates of responsive LA neurons (green) show a significant adaptation after each trial (n=11 cells, main effect P<0.001 by repeated one-way ANOVA). Contrarily, the firing rates of responsive ILSCm neurons (red) did not adapt across trials (n=7 cells, main effect P=0.96 by repeated one-way ANOVA). (f) The ILSCm and LA example neuron activity (top; scaled by the hot colour map) were aligned with the FS with time (the bottom red bars represent the freezing state). Values are represented as mean±s.d.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4403372&req=5

f4: Activation of the LA is temporally correlated with the UF elicited by applying the US to the ILSCm.Schematic (a) and photograph (b) of the two-site multi-channel optrode system. The inset in b shows the tip of the optrode (white box). (c) PSTHs of two example neurons from the ILSCm and LA show different firing patterns in response to the US in the ILSCm (1-s bins). The red line represents the estimation of the expected baseline rate and the grey shaded area represents the confidence limit of 99%. (d) Z-scored population PSTH of responsive neurons from the ILSCm (red) and LA (green) (100-ms bins), shaded areas represent the s.e.m. The blue bar indicates the optical stimulation, red bar indicates the period of excitation of ILSCm neurons (n=7 cells, compared with the pre-event reference period, P<0.01 by right-tailed t-test), and green bar indicates the period of excitation of LA neurons (n=11 cells). (e) The normalized post-stimulation mean firing rates of responsive LA neurons (green) show a significant adaptation after each trial (n=11 cells, main effect P<0.001 by repeated one-way ANOVA). Contrarily, the firing rates of responsive ILSCm neurons (red) did not adapt across trials (n=7 cells, main effect P=0.96 by repeated one-way ANOVA). (f) The ILSCm and LA example neuron activity (top; scaled by the hot colour map) were aligned with the FS with time (the bottom red bars represent the freezing state). Values are represented as mean±s.d.
Mentions: In freely behaving mice, we aimed to identify the specific functional mechanism of the ILSCm-LA circuitry by which optical stimulation modulates the neural network activities. We developed a novel two-site multi-channel optrode system for simultaneous recording and light delivery in freely moving mice (Supplementary Fig. 7a) and applied this to stimulate and record in ILSCm, and simultaneous recording from LA (Fig. 4a,b and Supplementary Fig. 7e,f). In mice exhibiting prolonged UF elicited by the US applied to the ChR2:ILSCm mice (n=3), 20 and 40 single-unit spikes were recorded in the ILSCm and LA, respectively (Supplementary Fig. 7b,c). Under direct light-evoked responses, 7 of the 20 local ILSCm cells were found to fire immediately following the pulsed laser, with an average latency of 3.0±1.5 ms, and the cells showed transient excitation during the US (Fig. 4c,d). In addition, 11 of the 40 LA cells were activated by the pulsed-laser stimulation, with a latency distribution comparable to that found in anesthetized mice (Supplementary Fig. 7d,g), and these cells showed sustained post stimulation excitation (Fig. 4c,d). Intriguingly, LA neuronal activation showed adaptation in firing rates among the US trials, whereas ILSCm neuronal activation was invariant (Fig. 4e). By comparing the time courses of the physiological activities and behavioural responses, it was discovered that the activation of LA neurons, rather than that of ILSCm neurons, temporally correlated with the US-elicited UF in ChR2:ILSCm mice (Fig. 4f and Supplementary Fig. 8). These results suggest that activation of the ILSCm represents an ‘on switch' for the brain's defensive system, whereas sustained LA activation is responsible for prolonged freezing in animals.

Bottom Line: Our results demonstrate that neurons in the superior colliculus (SC) are essential for a variety of acute and persistent defensive responses to overhead looming stimuli.Optogenetic mapping revealed that SC projections to the lateral posterior nucleus (LP) of the thalamus, a non-canonical polymodal sensory relay, are sufficient to mimic visually evoked fear responses.Our results reveal a novel collicular-thalamic-Amg circuit important for innate defensive responses to visual threats.

View Article: PubMed Central - PubMed

Affiliation: Shenzhen Key Lab of Neuropsychiatric Modulation and Collaborative Innovation Center for Brain Science, CAS Center for Excellence in Brain Science, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China.

ABSTRACT
The ability of animals to respond to life-threatening stimuli is essential for survival. Although vision provides one of the major sensory inputs for detecting threats across animal species, the circuitry underlying defensive responses to visual stimuli remains poorly defined. Here, we investigate the circuitry underlying innate defensive behaviours elicited by predator-like visual stimuli in mice. Our results demonstrate that neurons in the superior colliculus (SC) are essential for a variety of acute and persistent defensive responses to overhead looming stimuli. Optogenetic mapping revealed that SC projections to the lateral posterior nucleus (LP) of the thalamus, a non-canonical polymodal sensory relay, are sufficient to mimic visually evoked fear responses. In vivo electrophysiology experiments identified a di-synaptic circuit from SC through LP to the lateral amygdale (Amg), and lesions of the Amg blocked the full range of visually evoked defensive responses. Our results reveal a novel collicular-thalamic-Amg circuit important for innate defensive responses to visual threats.

No MeSH data available.


Related in: MedlinePlus