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Low-noise encoding of active touch by layer 4 in the somatosensory cortex.

Hires SA, Gutnisky DA, Yu J, O'Connor DH, Svoboda K - Elife (2015)

Bottom Line: The amount of irreducible internal noise in spike trains, an important constraint on models of cortical networks, has been difficult to estimate, since behavior and brain state must be precisely controlled or tracked.The variance of touch responses was smaller than expected from Poisson processes, often reaching the theoretical minimum.Layer 4 spike trains thus reflect the millisecond-timescale structure of tactile input with little noise.

View Article: PubMed Central - PubMed

Affiliation: Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States.

ABSTRACT
Cortical spike trains often appear noisy, with the timing and number of spikes varying across repetitions of stimuli. Spiking variability can arise from internal (behavioral state, unreliable neurons, or chaotic dynamics in neural circuits) and external (uncontrolled behavior or sensory stimuli) sources. The amount of irreducible internal noise in spike trains, an important constraint on models of cortical networks, has been difficult to estimate, since behavior and brain state must be precisely controlled or tracked. We recorded from excitatory barrel cortex neurons in layer 4 during active behavior, where mice control tactile input through learned whisker movements. Touch was the dominant sensorimotor feature, with >70% spikes occurring in millisecond timescale epochs after touch onset. The variance of touch responses was smaller than expected from Poisson processes, often reaching the theoretical minimum. Layer 4 spike trains thus reflect the millisecond-timescale structure of tactile input with little noise.

No MeSH data available.


Response characteristics of all L4 recordings outside of C2 and L5 recordings near C2.(A) Peri-stimulus time histogram aligned to first touch onsets (left) or all touch onsets (right) in a session. Touch spike windows computed from all touches for each cell (blue). Red scale bar 0.05 spikes/ms. (B) Peri-stimulus spike histogram aligned to preferred whisking phase with whisking spike window (green). (C) Average spike rates for twelve phase bins (black) for each cell with sinusoidal fit (grey). Red scale bar 0.5 spikes/s for L4 cells, 2 spikes/s for L5 cells. (D) Histogram of interspike intervals during each recording session. Depth is manipulator reading from pia.DOI:http://dx.doi.org/10.7554/eLife.06619.011
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fig3s2: Response characteristics of all L4 recordings outside of C2 and L5 recordings near C2.(A) Peri-stimulus time histogram aligned to first touch onsets (left) or all touch onsets (right) in a session. Touch spike windows computed from all touches for each cell (blue). Red scale bar 0.05 spikes/ms. (B) Peri-stimulus spike histogram aligned to preferred whisking phase with whisking spike window (green). (C) Average spike rates for twelve phase bins (black) for each cell with sinusoidal fit (grey). Red scale bar 0.5 spikes/s for L4 cells, 2 spikes/s for L5 cells. (D) Histogram of interspike intervals during each recording session. Depth is manipulator reading from pia.DOI:http://dx.doi.org/10.7554/eLife.06619.011

Mentions: The temporally precise spiking after touch was restricted to L4 neurons in the principal barrel. Neurons recorded in the C2 barrel column showed brief responses to touch (Figure 2A–C; Figure 3—figure supplement 1; Table 1). In L4, but outside of C2, touch responses were much weaker (first touch, p = 1.4e-5; later touches, p = 6.32e-6; Wilcoxon rank sum). Layer 5 neurons near C2 had much higher firing rates, with touch responses that were more diverse (Figure 2B; Figure 3—figure supplement 2; Table 1). Modulation by whisking phase was not significantly different between L4 neurons inside and outside the C2 barrel (p = 0.68), but both were significantly more phase modulated than L5 (p = 4.3e-5 and p = 0.012 respectively, Wilcoxon rank sum) (Figure 2—figure supplement 1). There were no significant changes in firing rate between whisking and non-whisking across the L4 population (L4 inside C2, p = 0.75; L4 outside C2, p = 0.92), whereas L5 showed a modest, but significant increase with whisking (p = 0.019, Wilcoxon signed rank).10.7554/eLife.06619.007Figure 2.Neural responses to behavioral variables across three populations.


Low-noise encoding of active touch by layer 4 in the somatosensory cortex.

Hires SA, Gutnisky DA, Yu J, O'Connor DH, Svoboda K - Elife (2015)

Response characteristics of all L4 recordings outside of C2 and L5 recordings near C2.(A) Peri-stimulus time histogram aligned to first touch onsets (left) or all touch onsets (right) in a session. Touch spike windows computed from all touches for each cell (blue). Red scale bar 0.05 spikes/ms. (B) Peri-stimulus spike histogram aligned to preferred whisking phase with whisking spike window (green). (C) Average spike rates for twelve phase bins (black) for each cell with sinusoidal fit (grey). Red scale bar 0.5 spikes/s for L4 cells, 2 spikes/s for L5 cells. (D) Histogram of interspike intervals during each recording session. Depth is manipulator reading from pia.DOI:http://dx.doi.org/10.7554/eLife.06619.011
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4525079&req=5

fig3s2: Response characteristics of all L4 recordings outside of C2 and L5 recordings near C2.(A) Peri-stimulus time histogram aligned to first touch onsets (left) or all touch onsets (right) in a session. Touch spike windows computed from all touches for each cell (blue). Red scale bar 0.05 spikes/ms. (B) Peri-stimulus spike histogram aligned to preferred whisking phase with whisking spike window (green). (C) Average spike rates for twelve phase bins (black) for each cell with sinusoidal fit (grey). Red scale bar 0.5 spikes/s for L4 cells, 2 spikes/s for L5 cells. (D) Histogram of interspike intervals during each recording session. Depth is manipulator reading from pia.DOI:http://dx.doi.org/10.7554/eLife.06619.011
Mentions: The temporally precise spiking after touch was restricted to L4 neurons in the principal barrel. Neurons recorded in the C2 barrel column showed brief responses to touch (Figure 2A–C; Figure 3—figure supplement 1; Table 1). In L4, but outside of C2, touch responses were much weaker (first touch, p = 1.4e-5; later touches, p = 6.32e-6; Wilcoxon rank sum). Layer 5 neurons near C2 had much higher firing rates, with touch responses that were more diverse (Figure 2B; Figure 3—figure supplement 2; Table 1). Modulation by whisking phase was not significantly different between L4 neurons inside and outside the C2 barrel (p = 0.68), but both were significantly more phase modulated than L5 (p = 4.3e-5 and p = 0.012 respectively, Wilcoxon rank sum) (Figure 2—figure supplement 1). There were no significant changes in firing rate between whisking and non-whisking across the L4 population (L4 inside C2, p = 0.75; L4 outside C2, p = 0.92), whereas L5 showed a modest, but significant increase with whisking (p = 0.019, Wilcoxon signed rank).10.7554/eLife.06619.007Figure 2.Neural responses to behavioral variables across three populations.

Bottom Line: The amount of irreducible internal noise in spike trains, an important constraint on models of cortical networks, has been difficult to estimate, since behavior and brain state must be precisely controlled or tracked.The variance of touch responses was smaller than expected from Poisson processes, often reaching the theoretical minimum.Layer 4 spike trains thus reflect the millisecond-timescale structure of tactile input with little noise.

View Article: PubMed Central - PubMed

Affiliation: Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States.

ABSTRACT
Cortical spike trains often appear noisy, with the timing and number of spikes varying across repetitions of stimuli. Spiking variability can arise from internal (behavioral state, unreliable neurons, or chaotic dynamics in neural circuits) and external (uncontrolled behavior or sensory stimuli) sources. The amount of irreducible internal noise in spike trains, an important constraint on models of cortical networks, has been difficult to estimate, since behavior and brain state must be precisely controlled or tracked. We recorded from excitatory barrel cortex neurons in layer 4 during active behavior, where mice control tactile input through learned whisker movements. Touch was the dominant sensorimotor feature, with >70% spikes occurring in millisecond timescale epochs after touch onset. The variance of touch responses was smaller than expected from Poisson processes, often reaching the theoretical minimum. Layer 4 spike trains thus reflect the millisecond-timescale structure of tactile input with little noise.

No MeSH data available.