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

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ABSTRACT

Sensory cortices do not work in isolation. The functional responses of neurons in primary sensory cortices can be affected by activity from other modalities. For example, short-term visual deprivations, or dark exposure (DE), leads to enhanced neuronal responses and frequency selectivity to sounds in layer 4 (L4) of primary auditory cortex (A1). Circuit changes within A1 likely underlie these changes. Prior studies revealed that DE enhanced thalamocortical transmission to L4 in A1. Because the frequency selectivity of L4 neurons is determined by both thalamocortical and intracortical inputs, changes in intralaminar circuits to L4 neurons might also contribute to improved sound responses. We thus investigated in mouse A1 whether intracortical circuits to L4 cells changed after DE. Using in vitro whole-cell patch recordings in thalamocortical slices from mouse auditory cortex, we show that DE can lead to refinement of interlaminar excitatory as well as inhibitory connections from L2/3 to L4 cells, manifested as a weakening of these connections. The circuit refinement is present along the tonotopic axis, indicating reduced integration along the tonotopic axis. Thus, cross-modal influences may alter the spectral and temporal processing of sensory stimuli in multiple cortical layers by refinement of thalamocortical and intracortical circuits.

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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 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).

Mentions: Circuit changes can involve changes in connection probability as well as changes in synaptic strength. Therefore, we next investigated whether the strength of events evoked from each layer changed after DE. Because synaptic events can change in amplitude as well as duration, we calculated both charge and peak amplitude of the evoked EPSCs. We found that the mean EPSC charge, as well as EPSC amplitude of events originating from L2/3 and L5/6, decreased after DE (Figs. 4A, B and 5A, B). Because the amplitude of events originating in L4 did not change, the fractional charge L4 cells received from within L4 as opposed to interlaminar inputs increased (Figs. 4C and 5C). The laminar changes in IPSC strength after DE mirrored the changes in EPSC strength. The average charge and amplitude of uncaging evoked IPSC was decreased in L2/3 after DE (Figs. 4D, E and 5D, E), leading to a relative increase in input from L4 (Figs. 4F and 5F). Together, these results demonstrate a weakening of interlaminar excitatory and inhibitory inputs from L2/3 to L4 neurons after DE.


Intracortical Circuits in Thalamorecipient Layers of Auditory Cortex Refine after Visual Deprivation
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 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).
Mentions: Circuit changes can involve changes in connection probability as well as changes in synaptic strength. Therefore, we next investigated whether the strength of events evoked from each layer changed after DE. Because synaptic events can change in amplitude as well as duration, we calculated both charge and peak amplitude of the evoked EPSCs. We found that the mean EPSC charge, as well as EPSC amplitude of events originating from L2/3 and L5/6, decreased after DE (Figs. 4A, B and 5A, B). Because the amplitude of events originating in L4 did not change, the fractional charge L4 cells received from within L4 as opposed to interlaminar inputs increased (Figs. 4C and 5C). The laminar changes in IPSC strength after DE mirrored the changes in EPSC strength. The average charge and amplitude of uncaging evoked IPSC was decreased in L2/3 after DE (Figs. 4D, E and 5D, E), leading to a relative increase in input from L4 (Figs. 4F and 5F). Together, these results demonstrate a weakening of interlaminar excitatory and inhibitory inputs from L2/3 to L4 neurons after DE.

View Article: PubMed Central - HTML - PubMed

ABSTRACT

Sensory cortices do not work in isolation. The functional responses of neurons in primary sensory cortices can be affected by activity from other modalities. For example, short-term visual deprivations, or dark exposure (DE), leads to enhanced neuronal responses and frequency selectivity to sounds in layer 4 (L4) of primary auditory cortex (A1). Circuit changes within A1 likely underlie these changes. Prior studies revealed that DE enhanced thalamocortical transmission to L4 in A1. Because the frequency selectivity of L4 neurons is determined by both thalamocortical and intracortical inputs, changes in intralaminar circuits to L4 neurons might also contribute to improved sound responses. We thus investigated in mouse A1 whether intracortical circuits to L4 cells changed after DE. Using in vitro whole-cell patch recordings in thalamocortical slices from mouse auditory cortex, we show that DE can lead to refinement of interlaminar excitatory as well as inhibitory connections from L2/3 to L4 cells, manifested as a weakening of these connections. The circuit refinement is present along the tonotopic axis, indicating reduced integration along the tonotopic axis. Thus, cross-modal influences may alter the spectral and temporal processing of sensory stimuli in multiple cortical layers by refinement of thalamocortical and intracortical circuits.

No MeSH data available.


Related in: MedlinePlus