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Featured ArticleArticles, Development/Plasticity/Repair

Selective Suppression of Plasticity in Amygdala Inputs from Temporal Association Cortex by the External Capsule

Alexei Morozov, Daniel Sukato and Wataru Ito
Journal of Neuroscience 5 January 2011, 31 (1) 339-345; DOI: https://doi.org/10.1523/JNEUROSCI.5537-10.2011
Alexei Morozov
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Daniel Sukato
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Wataru Ito
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  • Figure 1.
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    Figure 1.

    ChR2-Venus-expressing axons from TeA pass through EC and innervate LA. A , A representative slice containing TeA infected with ChR2-AAV. Left, Bright-field image. Middle, Fluorescence image (YFP) of the corresponding rectangle area; yellow dotted line indicates medial boundary of the external capsule. Right, Overlay of YFP-expressing areas at injection sites from 6 animals. B , A postrecording fixed LA slice under bright field illumination (left) and fluorescence (right, YFP). Recording was made from neurons within the yellow dotted triangle area. C , Confocal images of YFP-expressing fibers around EC from a mouse injected with ChR2-AAV in TeA. Magnified image represents yellow rectangular area containing LA EC.

  • Figure 2.
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    Figure 2.

    EC suppresses LTP in TeA–LA pathway. A , Experimental scheme for recording responses to optical stimulation of TeA axons in LA. B , Top, Response in a putative paracapsular interneuron to a 100 pA current step. Magnified time-scale spikes are shown on the right. Bottom, EPSPs evoked by blue light pulses (light blue arrow) with 2×, 4×, and 8× intensity of the threshold energy. Peak of action potential at 8× intensity is truncated. Light blue arrow indicates light pulse. C , Left, Bright-field/fluorescence (YFP) images of a slice with a cut separating EC from LA. Recording area is indicated by a yellow dot triangle. Middle, Examples of EPSPs evoked by blue light pulses with 2×, 4×, and 8× intensity of the threshold energy. Right, Input–output analysis of EPSPs. D , Top, LTP induction protocol. Left, LTP in TeA–LA pathway; insets represent averaged EPSPs before (1) and after (2) induction as indicated by thick bars (5 min each). Right, Summary for the LTP. *p < 0.05, ***p < 0.001. Error bars represent SEM. Number of cells is shown in parentheses.

  • Figure 3.
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    Figure 3.

    Transection of EC shifts balance between inhibition and excitation in PNs toward excitation during activation of TeA fibers. A , EPSP/IPSP sequences evoked in PNs at −50 mV resting membrane potential (Control: gray trace) by blue light pulses (light blue arrow) with 4× intensity of the threshold energy are blocked by CNQX and AP-5 (CNQX+AP-5: black trace). Each trace is an average of five consecutive traces. B , Determination of I/E index for responses in PNs (left) and INs (right) from intact and transected slices. Top, Examples of mixed EPSP/IPSP response obtained in the absence of PTX (black line), excitatory response isolated in the presence of 100 μm PTX (blue line), and inhibitory component (red line) obtained by subtraction of the excitatory response from the mixed response. Shaded areas under the curves correspond to the time intervals of 5, 10, and 50 ms from EPSP onset. All responses are shown normalized to the EPSP amplitude at 5 ms (indicated by horizontal dashed line). Bottom, Summary diagram for the corresponding I/E indices. Number of cells is shown in parentheses. *p < 0.05. Error bars represent SEM.

  • Figure 4.
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    Figure 4.

    ChR2-Venus-expressing axons from ACC innervate LA but bypass EC. A , A representative slice containing ACC infected with ChR2-AAV. Top left, Bright-field image. Lower left, Fluorescence image (YFP) of the corresponding rectangle area. Right, Overlay of YFP-expressing areas at injection sites from 8 animals. B , Coronal sections of LA under bright-field illumination (top) and fluorescence (YFP) (bottom). Numbers at bottom indicate distance from the bregma. Yellow dotted line depicts EC. C , Left, Confocal images of YFP-expressing fibers around EC from a mouse injected with ChR2-AAV in ACC. Magnified image represents yellow rectangular areas containing LA EC. Right, Relative YFP fluorescence in EC of mice injected with ChR2-AAV into either ACC or TeA. Number of animals is shown in parentheses. ***p < 0.001. Error bars represent SEM.

  • Figure 5.
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    Figure 5.

    LTP in ACC–LA pathway does not require inhibition of GABAA receptor-mediated transmission. A , Experimental scheme. B , Left, LTP in ACC–LA pathway, insets represent averaged EPSPs before (1) and after (2) induction as indicated by thick bars (5 min each). Right, Summary for the LTP. Number of cells is shown in parentheses. **p < 0.01, ***p < 0.001. Error bars represent SEM.

  • Figure 6.
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    Figure 6.

    Transection of EC does not change the balance between inhibition and excitation in PNs during activation of ACC fibers. A , EPSP/IPSP sequences evoked in PNs at −50 mV resting membrane potential (Control: gray trace) by blue light pulses (light blue arrow) with 4× intensity of the threshold energy are blocked by CNQX and AP-5 (CNQX+AP-5: black trace). Each trace is an average of five consecutive traces. B , Determination of I/E index for responses in PNs in intact and transected slices. Left, Examples of mixed EPSP/IPSP response obtained in the absence of PTX (black line), excitatory response isolated in the presence of 100 μm PTX (blue line), and inhibitory component (red line) obtained by subtraction of the excitatory response from the mixed response. Shaded areas under the curves correspond to the time intervals of 5, 10, and 50 ms from EPSP onset. All responses are shown normalized to the EPSP amplitude at 5 ms (indicated by horizontal dashed line). Right, Summary diagram for the corresponding I/E indices. Number of cells is shown in parentheses. Error bars represent SEM.

  • Figure 7.
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    Figure 7.

    Schematic representation of potential inhibitory mechanisms recruited through EC. Left, According to scenario 1, fibers from TeA (green lines) fire paracapsular GABAergic neurons (pI), which provide feedforward inhibition of PN (P) inside LA. According to scenario 2, fibers from TeA activate hypothetical glutamatergic relay cells (R). The relay cells recruit GABAergic neurons inside LA (I), which increase inhibition in LA PNs. Right, Transection of EC eliminates both inhibitory mechanisms but does not prevent photoactivation of TeA fibers, which contain ChR2.

Tables

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    Table 1.

    Properties of EPSP responses to photostimulation of TeA fibers

    PN/intact EC (n = 9)PN/transected EC (n = 8)IN/intact EC (n = 8)IN/transected EC (n = 9)
    Onset latency (ms)3.26 ± 0.163.49 ± 0.213.81 ± 0.383.10 ± 0.15
    Time of peak (ms)17.93 ± 4.0013.69 ± 0.7715.01 ± 1.4115.06 ± 1.40
    Peak amplitude (mV)14.89 ± 3.5214.01 ± 3.4526.66 ± 5.9820.68 ± 2.77
    Maximum rise slope (mV/ms)3.64 ± 0.684.03 ± 0.805.59 ± 1.164.78 ± 0.34
    Time of maximum rise slope (ms)5.12 ± 0.255.97 ± 0.736.75 ± 0.995.23 ± 0.73
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    Table 2.

    Properties of EPSP responses in LA PNs to photostimulation of ACC fibers

    Intact EC (n = 9)Transected EC (n = 9)
    Onset latency (ms)3.06 ± 0.183.07 ± 0.08
    Time of peak (ms)16.94 ± 2.3216.23 ± 1.24
    Peak amplitude (mV)6.59 ± 1.005.66 ± 0.83
    Maximum rise slope (mV/ms)2.10 ± 0.271.99 ± 0.22
    Time of maximum rise slope (ms)4.98 ± 0.344.53 ± 0.13
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The Journal of Neuroscience: 31 (1)
Journal of Neuroscience
Vol. 31, Issue 1
5 Jan 2011
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Selective Suppression of Plasticity in Amygdala Inputs from Temporal Association Cortex by the External Capsule
Alexei Morozov, Daniel Sukato, Wataru Ito
Journal of Neuroscience 5 January 2011, 31 (1) 339-345; DOI: 10.1523/JNEUROSCI.5537-10.2011

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Selective Suppression of Plasticity in Amygdala Inputs from Temporal Association Cortex by the External Capsule
Alexei Morozov, Daniel Sukato, Wataru Ito
Journal of Neuroscience 5 January 2011, 31 (1) 339-345; DOI: 10.1523/JNEUROSCI.5537-10.2011
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