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Developmental regulation of spatio-temporal patterns of cortical circuit activation.

Griffen TC, Wang L, Fontanini A, Maffei A - Front Cell Neurosci (2013)

Bottom Line: However, while from eye opening to the peak of the critical period, the amplitude and persistence of the voltage signal decrease, peak activation is reached more quickly and the interlaminar gain increases with age.The lateral spread of activation within layers remains unchanged throughout the time window under analysis.Signals become more efficiently propagated across layers through developmentally regulated changes in interlaminar gain.

View Article: PubMed Central - PubMed

Affiliation: Program in Neuroscience, Stony Brook University Stony Brook, NY, USA ; Medical Scientist Training Program, Stony Brook University Stony Brook, NY, USA.

ABSTRACT
Neural circuits are refined in an experience-dependent manner during early postnatal development. How development modulates the spatio-temporal propagation of activity through cortical circuits is poorly understood. Here we use voltage-sensitive dye imaging (VSD) to show that there are significant changes in the spatio-temporal patterns of intracortical signals in primary visual cortex (V1) from postnatal day 13 (P13), eye opening, to P28, the peak of the critical period for rodent visual cortical plasticity. Upon direct stimulation of layer 4 (L4), activity spreads to L2/3 and to L5 at all ages. However, while from eye opening to the peak of the critical period, the amplitude and persistence of the voltage signal decrease, peak activation is reached more quickly and the interlaminar gain increases with age. The lateral spread of activation within layers remains unchanged throughout the time window under analysis. These developmental changes in spatio-temporal patterns of intracortical circuit activation are mediated by differences in the contributions of excitatory and inhibitory synaptic components. Our results demonstrate that after eye opening the circuit in V1 is refined through a progression of changes that shape the spatio-temporal patterns of circuit activation. Signals become more efficiently propagated across layers through developmentally regulated changes in interlaminar gain.

No MeSH data available.


Related in: MedlinePlus

Developmental reduction in cortical activation. (A) Representative sample VSD images at 0, 2.5, 5, 10, 20, and 30 ms from L4 stimulation for each age group. Images were cropped to better visualize the activated region (from 60 × 88 to 45 × 50 pixels, 20 μm per pixel). Top left panel: White boxes: ROIs quantified in panel (C), Figures 2, 3, 5, 6, and 7. Vertical white dashed line: ROI quantified in panel (B). Horizontal white dashed lines: ROIs quantified in Figure 4. (B) Time course of the ΔF/F measured by line scans perpendicular to the pial surface. Blue: P14. Red: P20. Orange: P27. Error bars: ± SEM. (C) Top: Time course of optical signals measured from ROIs in L4, L2/3, and L5 from 10 ms before stimulation to 50 ms after stimulation on the left. The gray box indicates TFS 0 to 15 ms, which is shown amplified in the traces on the right to highlight changes in the time to peak. Blue: P14. Red: P20. Orange: P27. Light gray line: 0.0 ΔF/F. Bottom: Peak ΔF/F measured from ROIs in L4, L2/3, and L5. Blue: P14. Red: P20. Orange: P27. Error bars: ± SEM. Dark bars indicate significant changes, p < 0.05.
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Figure 1: Developmental reduction in cortical activation. (A) Representative sample VSD images at 0, 2.5, 5, 10, 20, and 30 ms from L4 stimulation for each age group. Images were cropped to better visualize the activated region (from 60 × 88 to 45 × 50 pixels, 20 μm per pixel). Top left panel: White boxes: ROIs quantified in panel (C), Figures 2, 3, 5, 6, and 7. Vertical white dashed line: ROI quantified in panel (B). Horizontal white dashed lines: ROIs quantified in Figure 4. (B) Time course of the ΔF/F measured by line scans perpendicular to the pial surface. Blue: P14. Red: P20. Orange: P27. Error bars: ± SEM. (C) Top: Time course of optical signals measured from ROIs in L4, L2/3, and L5 from 10 ms before stimulation to 50 ms after stimulation on the left. The gray box indicates TFS 0 to 15 ms, which is shown amplified in the traces on the right to highlight changes in the time to peak. Blue: P14. Red: P20. Orange: P27. Light gray line: 0.0 ΔF/F. Bottom: Peak ΔF/F measured from ROIs in L4, L2/3, and L5. Blue: P14. Red: P20. Orange: P27. Error bars: ± SEM. Dark bars indicate significant changes, p < 0.05.

Mentions: Interlaminar spread of the VSD signal was analyzed with line scans 3 pixels wide (60 μm) from the pial surface to a depth of 1000 μm (50 pixels) positioned next to the stimulating electrode and perpendicular to the pia (Figure 1A). Regions of interest (ROIs) 2 × 2 pixels (40 × 40 μm) were selected to analyze the time course of activation in L4, L2/3, and L5 over 50 ms as follows: the L2/3 ROI was placed at the point of maximal activation in L2/3. The L4 ROI was placed as close to the stimulating electrode as possible while avoiding the stimulation artifact from the electrode. The L5 ROI was placed 600 μm below the pial surface (Figure 1A). All three ROIs were aligned vertically, perpendicular to the pial surface. Threshold for signal detection was set at ±2 standard deviations from the baseline. Signals not reaching threshold were set to 0 ΔF/F for analysis.


Developmental regulation of spatio-temporal patterns of cortical circuit activation.

Griffen TC, Wang L, Fontanini A, Maffei A - Front Cell Neurosci (2013)

Developmental reduction in cortical activation. (A) Representative sample VSD images at 0, 2.5, 5, 10, 20, and 30 ms from L4 stimulation for each age group. Images were cropped to better visualize the activated region (from 60 × 88 to 45 × 50 pixels, 20 μm per pixel). Top left panel: White boxes: ROIs quantified in panel (C), Figures 2, 3, 5, 6, and 7. Vertical white dashed line: ROI quantified in panel (B). Horizontal white dashed lines: ROIs quantified in Figure 4. (B) Time course of the ΔF/F measured by line scans perpendicular to the pial surface. Blue: P14. Red: P20. Orange: P27. Error bars: ± SEM. (C) Top: Time course of optical signals measured from ROIs in L4, L2/3, and L5 from 10 ms before stimulation to 50 ms after stimulation on the left. The gray box indicates TFS 0 to 15 ms, which is shown amplified in the traces on the right to highlight changes in the time to peak. Blue: P14. Red: P20. Orange: P27. Light gray line: 0.0 ΔF/F. Bottom: Peak ΔF/F measured from ROIs in L4, L2/3, and L5. Blue: P14. Red: P20. Orange: P27. Error bars: ± SEM. Dark bars indicate significant changes, p < 0.05.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Figure 1: Developmental reduction in cortical activation. (A) Representative sample VSD images at 0, 2.5, 5, 10, 20, and 30 ms from L4 stimulation for each age group. Images were cropped to better visualize the activated region (from 60 × 88 to 45 × 50 pixels, 20 μm per pixel). Top left panel: White boxes: ROIs quantified in panel (C), Figures 2, 3, 5, 6, and 7. Vertical white dashed line: ROI quantified in panel (B). Horizontal white dashed lines: ROIs quantified in Figure 4. (B) Time course of the ΔF/F measured by line scans perpendicular to the pial surface. Blue: P14. Red: P20. Orange: P27. Error bars: ± SEM. (C) Top: Time course of optical signals measured from ROIs in L4, L2/3, and L5 from 10 ms before stimulation to 50 ms after stimulation on the left. The gray box indicates TFS 0 to 15 ms, which is shown amplified in the traces on the right to highlight changes in the time to peak. Blue: P14. Red: P20. Orange: P27. Light gray line: 0.0 ΔF/F. Bottom: Peak ΔF/F measured from ROIs in L4, L2/3, and L5. Blue: P14. Red: P20. Orange: P27. Error bars: ± SEM. Dark bars indicate significant changes, p < 0.05.
Mentions: Interlaminar spread of the VSD signal was analyzed with line scans 3 pixels wide (60 μm) from the pial surface to a depth of 1000 μm (50 pixels) positioned next to the stimulating electrode and perpendicular to the pia (Figure 1A). Regions of interest (ROIs) 2 × 2 pixels (40 × 40 μm) were selected to analyze the time course of activation in L4, L2/3, and L5 over 50 ms as follows: the L2/3 ROI was placed at the point of maximal activation in L2/3. The L4 ROI was placed as close to the stimulating electrode as possible while avoiding the stimulation artifact from the electrode. The L5 ROI was placed 600 μm below the pial surface (Figure 1A). All three ROIs were aligned vertically, perpendicular to the pial surface. Threshold for signal detection was set at ±2 standard deviations from the baseline. Signals not reaching threshold were set to 0 ΔF/F for analysis.

Bottom Line: However, while from eye opening to the peak of the critical period, the amplitude and persistence of the voltage signal decrease, peak activation is reached more quickly and the interlaminar gain increases with age.The lateral spread of activation within layers remains unchanged throughout the time window under analysis.Signals become more efficiently propagated across layers through developmentally regulated changes in interlaminar gain.

View Article: PubMed Central - PubMed

Affiliation: Program in Neuroscience, Stony Brook University Stony Brook, NY, USA ; Medical Scientist Training Program, Stony Brook University Stony Brook, NY, USA.

ABSTRACT
Neural circuits are refined in an experience-dependent manner during early postnatal development. How development modulates the spatio-temporal propagation of activity through cortical circuits is poorly understood. Here we use voltage-sensitive dye imaging (VSD) to show that there are significant changes in the spatio-temporal patterns of intracortical signals in primary visual cortex (V1) from postnatal day 13 (P13), eye opening, to P28, the peak of the critical period for rodent visual cortical plasticity. Upon direct stimulation of layer 4 (L4), activity spreads to L2/3 and to L5 at all ages. However, while from eye opening to the peak of the critical period, the amplitude and persistence of the voltage signal decrease, peak activation is reached more quickly and the interlaminar gain increases with age. The lateral spread of activation within layers remains unchanged throughout the time window under analysis. These developmental changes in spatio-temporal patterns of intracortical circuit activation are mediated by differences in the contributions of excitatory and inhibitory synaptic components. Our results demonstrate that after eye opening the circuit in V1 is refined through a progression of changes that shape the spatio-temporal patterns of circuit activation. Signals become more efficiently propagated across layers through developmentally regulated changes in interlaminar gain.

No MeSH data available.


Related in: MedlinePlus