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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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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 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.

Mentions: We mapped L4 cells (n = 46 cells) in A1 and examined the connection pattern of excitatory inputs. L4 cells in normal reared animals (NR, n = 27 cells) received excitatory input from within L4 as well as from L2/3 and L5/6 (Fig. 1D, E), consistent with prior studies (Barbour and Callaway, 2008; Zhao et al., 2009; Kratz and Manis, 2015). To analyze connectivity pattern changes over the population of cells, individual LSPS maps were aligned to the cell body position and averaged; the result is a spatial map of connection probability (Fig. 2A,B). These maps showed that L4 cells were connected to other L4 cells up to 500 μm apart. Because our thalamocortical slices contain the tonotopic axis, this indicates that L4 cells can integrate inputs that are more than one octave above or below the cell’s best frequency (BF).


Intracortical Circuits in Thalamorecipient Layers of Auditory Cortex Refine after Visual Deprivation
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 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.
Mentions: We mapped L4 cells (n = 46 cells) in A1 and examined the connection pattern of excitatory inputs. L4 cells in normal reared animals (NR, n = 27 cells) received excitatory input from within L4 as well as from L2/3 and L5/6 (Fig. 1D, E), consistent with prior studies (Barbour and Callaway, 2008; Zhao et al., 2009; Kratz and Manis, 2015). To analyze connectivity pattern changes over the population of cells, individual LSPS maps were aligned to the cell body position and averaged; the result is a spatial map of connection probability (Fig. 2A,B). These maps showed that L4 cells were connected to other L4 cells up to 500 μm apart. Because our thalamocortical slices contain the tonotopic axis, this indicates that L4 cells can integrate inputs that are more than one octave above or below the cell’s best frequency (BF).

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