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Research ArticleNew Research, Sensory and Motor Systems

Intracortical Circuits in Thalamorecipient Layers of Auditory Cortex Refine after Visual Deprivation

Xiangying Meng, Joseph P. Y. Kao, Hey-Kyoung Lee and Patrick O. Kanold
eNeuro 3 April 2017, 4 (2) ENEURO.0092-17.2017; DOI: https://doi.org/10.1523/ENEURO.0092-17.2017
Xiangying Meng
1Department of Biology, University of Maryland, College Park, MD 20742
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Joseph P. Y. Kao
2Center for Biomedical Engineering and Technology, and Department of Physiology, University of Maryland School of Medicine, Baltimore, MD 21201
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Hey-Kyoung Lee
1Department of Biology, University of Maryland, College Park, MD 20742
3Department of Neuroscience, Mind/Brain Institute, Johns Hopkins University, Baltimore, MD 21218
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Patrick O. Kanold
1Department of Biology, University of Maryland, College Park, MD 20742
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  • Figure 1.
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    Figure 1.

    LSPS to map intracortical connections to L4 cells. A, Left, infrared image of brain slice with patch pipette on L4 neuron. Stimulation grid is indicated by blue dots. Right, schematic of LSPS experiment. Whole-cell patch-clamp recordings are made from L4 neurons. Cells are held at –70 and 0 mV. Laser pulses (355 nm) are targeted to an array of locations in the slice. Traces on right, activated cells fire action potentials (top), and if a connection exists to the patched L4 neuron, evoked EPSCs and IPSCs are recorded (bottom). B, The relative position of patched cells within L4. 0 refers to the border with L5 and 100 refers to the border with L3. Cells were sampled from the middle of layer 4 in NR and DE animals (p = 3.05 × 10–1). C, Whole-cell voltage clamp recordings at holding potentials of −70 mV (top) or 0 mV (bottom) distinguish between photostimulation-evoked excitatory and inhibitory currents. Shown are traces obtained with photostimulation at different locations. Solid blue line indicates time of photostimulation; dashed blue line marks 8-ms poststimulus, which is the minimal latency for synaptic responses. D, Traces obtained by LSPS when holding one L4 neuron at −70 and 0 mV, respectively. Traces showing large-amplitude direct responses are shown in black. The responses that have latencies between 8 and 50 ms are shown in red. Otherwise, the traces are shown in blue. E, Pseudocolor maps show PSC charge at each stimulus location for the example cell in D. Direct responses indicated were set to zero (overlaid by black area). White filled circle marks the soma location. Horizontal bars indicate layer borders.

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    Figure 2.

    Interlaminar cortical excitatory connections to L4 cells refine with DE. A, Schematic of LSPS experiment. Whole-cell patch-clamp recordings are made from L4 neurons. Cells are held at –70 mV. Laser pulses (355 nm) are targeted to an array of locations in the slice. Traces on right, activated cells fire action potentials (top), and if a connection exists to the patched L4 neuron, evoked EPSCs are recorded (bottom). B, Average maps (aligned to soma, white circle) of connection probability for excitatory connections in NR (left) and DE (right) animals. Connection probability is encoded according to the pseudocolor scale. White horizontal lines indicate averaged laminar borders and are 100 μm long. Traces at the right of the DE panel the laminar marginal distributions (red for NR and black for DE). Traces at the bottom of the DE panel are the columnar marginal distributions. Note that NR and DE maps and distributions appear different. C, Distributions of area of input originating from L2/3 (top), L4 (middle), and L5/6 (bottom) of NR (red) or DE (black) animals. *, p < 0.05. The p values for the total area from L2/3, L4, and L5/6 are 0.02 (NR: mean = 3.8 × 104 μm2, std = 2.2 × 104 μm2; DE: mean = 2.4 × 104 μm2, std = 1.4 × 104 μm2), 0.74 (NR: mean = 2.1 × 104 μm2, std = 1.0 × 104 μm2; DE: mean = 2.2 × 104 μm2, std = 1.3 × 104 μm2), and 0.32 (NR: mean = 3.6 × 104 μm2, std = 2.1 × 104 μm2; DE: mean = 2.9 × 104 μm2, std = 2.4 × 104 μm2), respectively. D, Distributions of the distance of 80% of input to each L4 cell originating from L2/3 (top), L4 (middle), and L5/6 (bottom) of NR (red) or DE (black) animals. We calculated the laminar radius that covers 80% of inputs inside each layer and plotted the CDFs of the radius. *, p < 0.05. All comparisons were done with Wilcoxon rank-sum test or Student’s t test. The p values for the average 80% distance from L2/3, L4, and L5/6 are 0.028 (NR: mean = 179.2 μm, std = 51 μm; DE: mean = 143.6 μm, std = 52.3 μm), 0.40 (NR: mean = 239.4 μm, std = 58.7 μm; DE: mean = 225.2 μm, std = 49.9 μm), and 0.39 (NR: mean = 233.5 μm, std = 79.8 μm; DE: mean = 212.2 μm, std = 81.0 μm), respectively.

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    Figure 3.

    Interlaminar cortical inhibitory connections to L4 cells refine. A, Schematic of LSPS experiment. Whole-cell patch-clamp recordings are made from L4 neurons. Cells are held at 0 mV. Laser pulses (355 nm) are targeted to an array of locations in the slice. Traces on right, activated cells fire action potentials (top), and if a connection exists to the patched L4 neuron, evoked IPSCs are recorded (bottom). B, Average maps (aligned to soma, white circle) of connection probability for inhibitory connections in NR (left) and DE (right) animals. Connection probability is encoded according to the pseudocolor scale. White horizontal lines indicate averaged laminar borders and are 100 μm long. Traces at the right of the DE panel are the laminar marginal distributions (red for NR and black for DE). Traces at the bottom of the DE panel are the columnar marginal distributions. Note that NR and DE maps and distributions appear different. C, Distributions of area of input originating from L2/3 (top), L4 (middle), and L5/6 (bottom) of NR (red) or DE (black) animals. *, p < 0.05. The p values for the total area from L2/3, L4, and L5/6 are 0.02 (NR: mean = 7.3 × 104 μm2, std = 2.9 × 104 μm2; DE: mean = 5.1 × 104 μm2, std = 2.5 × 104 μm2), 0.82 (NR: mean = 2.8 × 104 μm2, std = 1.5 × 104 μm2; DE: mean = 2.7 × 104 μm2, std = 1.7 × 104 μm2), and 0.14 (NR: mean = 3.5 × 104 μm2, std = 1.8 × 104 μm2; DE: mean = 2.6 × 104 μm2, std = 2.41 × 104 μm2), respectively. D, Distributions of the distance of 80% of input to each L4 cell originating from L2/3 (top), L4 (middle), and L5/6 (bottom) of NR (red) or DE (black) animals. *, p < 0.05. All comparisons were done with Wilcoxon rank-sum test or Student’s t test. The p values for the average 80% distance from L2/3, L4, and L5/6 are 0.34 (NR: mean = 190.4 μm, std = 42.7 μm; DE: mean = 204.0 μm, std = 56.2 μm), 0.95 (NR: mean = 209.3 μm, std = 41.0 μm; DE: mean = 208.4 μm, std = 56.2 μm), and 0.74 (NR: mean = 237.9 μm, std = 74.7 μm; DE: mean = 228.6 μm, std = 108.8 μm), respectively.

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    Figure 4.

    The EPSC and IPSC charge of interlaminar cortical connections to L4 cells decreases. A, Average maps (aligned to soma, white circle) of connection strength (transferred charge) for excitatory inputs in NR (left) and DE (right) animals. Averages are calculated only for stimulation sites that evoked responses in >10% of cells in our sample. Connection strength is encoded according to the pseudocolor scale. White horizontal lines indicate averaged laminar borders and are 100 μm long. Traces at the right of DE panel are the laminar marginal distributions (red for NR and black for DE). Traces at the bottom of the DE panel are the columnar marginal distributions. Note that NR and DE maps and distributions appear different. B, Distributions of total (left) and mean EPSC (right) input charge originating from L2/3 (top), L4 (middle), and L5/6 (bottom) of NR (red) or DE (black) animals. *, p < 0.05; ***, p < 0.01. The p values for the total charge from L2/3, L4, and L5/6 are 0.06 (NR: mean = 71 pC, std = 52.6 pC; DE: mean = 42.6 pC, std = 42.4 pC), 0.17 (NR: mean = 25 pC, std = 19.5 pC; DE: mean = 35.2 pC, std = 29.7 pC), and 0.37 (NR: mean = 18.5 pC, std = 15.6 pC; DE: mean = 15.8 pC, std = 17.3 pC), respectively. The p values for the mean EPSC charge from L23, L4, and L5/6 are 8.1 × 10−4 (NR: mean = 2.59 pC, std = 1.23 pC; DE: mean = 1.46 pC, std = 0.6 pC), 0.73 (NR: mean = 1.45 pC, std = 0.8 pC; DE: mean = 1.36 pC, std = 0.91 pC), and 0.02 (NR: mean = 0.63 pC, std = 0.33 pC; DE: mean = 0.45 pC, std = 0.28 pC), respectively. All comparisons were done with Wilcoxon rank-sum test or Student’s t test. C, Distributions of fractional EPSC charge originating from L2/3 (top), L4 (middle), and L5/6 (bottom) for cells from NR (red) or DE (black) animals. L2/3: p = 0.015 (NR: mean = 0.62, std = 0.18; DE: mean = 0.47, std = 0.21), L4: p = 0.002 (NR: mean = 0.22, std = 0.13; DE: mean = 0.37, std = 0.15), and L5/6: p = 0.67 (NR: mean = 0.16, std = 0.1; DE: mean = 0.17, std = 0.11). D, Average maps (aligned to soma, white circle) of connection strength (transferred charge) for inhibitory inputs in NR (left) and DE (right) animals. Averages are calculated only for stimulation sites that evoked responses in >10% of cells in our sample. Note that NR and DE maps and distributions appear different. E, Distributions of total (left) and mean (right) IPSC input charge originating from L2/3 (top), L4 (middle), and L5/6 (bottom) of NR (red) or DE (black) animals. *, p < 0.05; ***, p < 0.01. The p values of the total IPSC charge from L2/3, L4, and L5/6 are 0.11 (NR: mean = 413.8 pC, std = 265.7 pC; DE: mean = 285.2 pC, std = 227.7 pC), 0.37 (NR: mean = 87.4 pC, std = 94.3 pC; DE: mean = 115.3 pC, std = 104 pC), and 0.41 (NR: mean = 51.4 pC, std = 63.7 pC; DE: mean = 37.2 pC, std = 35.1 pC), respectively. The p values of the mean IPSC charge from L23, L4, and L5/6 are 1.2 × 10−3 (NR: mean = 7.01 pC, std = 2.69 pC; DE: mean = 4.35 pC, std = 1.87 pC), 0.67 (NR: mean = 3.71 pC, std = 2.53 pC; DE: mean = 3.42 pC, std = 1.33 pC), and 0.67 (NR: mean = 1.58 pC, std = 0.88 pC; DE: mean = 1.44 pC, std = 01.13 pC), respectively. All comparisons were done with Wilcoxon rank-sum test or Student’s t test. F, Distributions of fractional IPSC charge originating from L2/3 (top), L4 (middle), and L5/6 (bottom) for cells from NR (red) or DE (black) animals: p = 0.001 (NR: mean = 0.76, std = 0.1; DE: mean = 0.64, std = 0.14), L4: p = 4.12*10−5 (NR: mean = 0.15, std = 0.07; DE: mean = 0.28, std = 0.11), and L5/6: p = 0.961 (NR: mean = 0.08, std = 0.05; DE: mean = 0.09, std = 0.06).

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    Figure 5.

    The EPSC and IPSC peak amplitude of interlaminar cortical connections to L4 cells decreases. A, Average maps (aligned to soma, white circle) of peak amplitude for excitatory inputs in NR (left) and DE (right) animals. Averages are calculated only for stimulation sites that evoked responses in >10% of cells in our sample. Peak amplitude is encoded according to the pseudocolor scale. White horizontal lines indicate averaged laminar borders and are 100 μm long. Traces at the right of the DE panel are the laminar marginal distributions (red for NR and black for DE). Traces at the bottom of the DE panel are the columnar marginal distributions. Note that NR and DE maps and distributions appear different. B, Distributions of total (left) and mean (right) EPSC peak amplitude originating from L2/3 (top), L4 (middle), and L5/6 (bottom) of NR (red) or DE (black) animals. *, p < 0.05; **, p < 0.01. The p values for the total peak from L2/3, L4, and L5/6 are 0.25 (NR: mean = 1.89 ×103 pA, std = 1.55 × 103 pA; DE: mean = 1.38 × 103 pA, std = 1.22 × 103 pA), 0.24 (NR: mean = 9.05 × 102 pA, std = 6.81 × 102 pA; DE: mean = 1.17 × 103 pA, std = 8.23 × 102 pA), and 0.99 (NR: mean = 1.11 × 103 pA, std = 8.39 × 102 pA; DE: mean = 1.11 × 103 pA, std = 9.98 × 102 pA), respectively. The p values for the mean peak from L2/3, L4, and L5/6 are 0.02 (NR: mean = 63.4 pA, std = 24.3 pA; DE: mean = 47.4 pA, std = 16.9 pA), 0.42 (NR: mean = 49.4 pA, std = 16.8 pA; DE: mean = 45.7 pA, std = 11.1 pA), and 0.2 (NR: mean = 35.4 pA, std = 8.15 pA; DE: mean = 32.3 pA, std = 6.85 pA), respectively. All comparisons were done with Wilcoxon rank-sum test or Student’s t test. C, Distributions of fractional EPSC amplitude originating from L2/3 (top), L4 (middle), and L5/6 (bottom) for cells from NR (red) or DE (black) animals. L2/3: p = 0.03 (NR: mean = 0.50, std = 0.18; DE: mean = 0.37, std = 0.18), L4: p = 0.009 (NR: mean = 0.23, std = 0.12; DE: mean = 0.33, std = 0.10), and L5/6: p = 0.5(NR: mean = 0.26, std = 0.12; DE: mean = 0.29, std = 0.14). D, Average maps (aligned to soma, white circle) of connection strength (transferred peak) for inhibitory inputs in NR (left) and DE (right) animals. Averages are calculated only for stimulation sites that evoked responses in >10% of cells in our sample. Traces at the right of the DE panel are the laminar marginal distributions (red for NR and black for DE). Traces at the bottom of the DE panel are the columnar marginal distributions. Note that NR and DE maps and distributions appear different. E, Distributions of total (left) and mean (right) IPSC peak amplitude originating from L2/3 (top), L4 (middle), and L5/6 (bottom) of NR (red) or DE (black) animals. *, p < 0.05; ***, p < 0.01. The p values for the total peak from L23, L4, and L5/6 are 0.22 (NR: mean = 6.74 ×103 pA, std = 3.83 × 103 pA; DE: mean = 5.24 × 103 pA, std = 3.85 × 103 pA), 0.28 (NR: mean = 2.01 × 103 pA, std = 1.63 × 103 pA; DE: mean = 2.69 × 103 pA, std = 2.40 × 103 pA), and 0.91 (NR: mean = 1.23 × 103 pA, std = 1.10 × 103 pA; DE: mean = 1.19 × 103 pA, std = 1.02 × 103 pA), respectively. The p values for the mean peak from L23, L4, and L5/6 are 0.004 (NR: mean = 118 pA, std = 38.4 pA; DE: mean = 82.8 pA, std = 30.9 pA), 0.42 (NR: mean = 90.1 pA, std = 46.0 pA; DE: mean = 79.8 pA, std = 27.3 pA), and 0.86 (NR: mean = 41.5 pA, std = 18.3 pA; DE: mean = 40.5 pA, std = 15.5 pA), respectively. All comparisons were done with Wilcoxon rank-sum test or Student’s t test. F, Distributions of fractional IPSC amplitude originating from L2/3 (top), L4 (middle), and L5/6 (bottom) for cells from NR (red) or DE (black) animals. L2/3: p = 4.7 × 10−3 (NR: mean = 0.68, std = 0.10; DE: mean = 0.57, std = 0.13), L4: p = 2.95 × 10−4 (NR: mean = 0.20, std = 0.07; DE: mean = 0.30, std = 0.09), and L5/6: p = 0.83 (NR: mean = 0.12, std = 0.06; DE: mean = 0.12, std = 0.07). All comparisons were done with Wilcoxon rank-sum test or Student’s t test.

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    Figure 6.

    The balance of excitation and inhibition of L2/3 inputs to L4 is reduced. Cumulative distributions (CDFs) of excitation/inhibition (EI) area ratio (left), charge ratio (middle), and peak amplitude ratio (right) from L2/3 (top), L4 (middle), and L5/6 (bottom) in NR and DE cells. The charge ratio of L2/3 inputs decreased after DE (EI area ratio: L2/3: p = 0.2, L4: p = 0.53, L5/6: p = 0.55; EI charge ratio: L2/3: p = 0.007, L4: p = 0.26, L5/6: p = 0.08; EI amplitude ratio: L2/3: p = 0.12, L4: p = 0.29, L5/6: p = 0.90). All comparisons were done with Wilcoxon rank-sum test or Student’s t test.

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Intracortical Circuits in Thalamorecipient Layers of Auditory Cortex Refine after Visual Deprivation
Xiangying Meng, Joseph P. Y. Kao, Hey-Kyoung Lee, Patrick O. Kanold
eNeuro 3 April 2017, 4 (2) ENEURO.0092-17.2017; DOI: 10.1523/ENEURO.0092-17.2017

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Intracortical Circuits in Thalamorecipient Layers of Auditory Cortex Refine after Visual Deprivation
Xiangying Meng, Joseph P. Y. Kao, Hey-Kyoung Lee, Patrick O. Kanold
eNeuro 3 April 2017, 4 (2) ENEURO.0092-17.2017; DOI: 10.1523/ENEURO.0092-17.2017
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Keywords

  • auditory cortex
  • intracortical
  • dark exposure
  • visual deprivation
  • crossmodal
  • mouse
  • refinement
  • plasticity
  • layer 4

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