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Research ArticleResearch Article: New Research, Sensory and Motor Systems

Interhemispheric Callosal Projections Sharpen Frequency Tuning and Enforce Response Fidelity in Primary Auditory Cortex

Bernard J. Slater and Jeffry S. Isaacson
eNeuro 7 August 2020, 7 (4) ENEURO.0256-20.2020; DOI: https://doi.org/10.1523/ENEURO.0256-20.2020
Bernard J. Slater
Center for Neural Circuits and Behavior and Department of Neurosciences, University of California, San Diego, La Jolla, CA 92093
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Jeffry S. Isaacson
Center for Neural Circuits and Behavior and Department of Neurosciences, University of California, San Diego, La Jolla, CA 92093
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    Figure 1.

    Optogenetic activation of cortical callosal inputs evokes excitation and inhibition in A1 of awake mice. A1, left, Experiment schematic, wild-type C57Bl6 mice. Right, Intrinsic imaging showing responses to 3-, 10-, and 30-kHz pure tones overlaid on an image of the vasculature. Areas indicated are A1, AAF, and A2. Scale bar = 500 μm. A2, left, Coronal section showing ChR2 expression (green) within A1 of the injected left hemisphere (Inj) and DiI-labeled recording electrode tract (red) in contralateral A1 (Rec). Dense ChR2 expression is also present in the MGB of the injected hemisphere. Scale bar = 1 mm. Right, Blow-up of recording site in the right hemisphere shows expression of ChR2-expressing fibers throughout all cortical layers. WM = white matter. Scale bar = 250 μm. Dashed lines show A1 border inferred from the same coronal planes according to Franklin and Paxinos (2008). B, FS (red) and RS (black) units are identified by plotting spike trough to peak time versus full width at half maximum (FWHM). Inset, Average waveforms of FS and RS units. Scale bar = 250 μs, 20 μV. C, Average normalized peristimulus time histogram (PSTH) of RS (black) and FS (red) units shows that brief LED illumination (bar) drives a transient increase followed by a decrease in firing rate. D, Activation of callosal inputs increases activity of some RS cells, but inhibition is more widespread. D1, Individual RS unit spike raster and PSTH showing that ChR2 activation of callosal fibers (blue shading) inhibits firing. Gray shading indicates measurement period used to calculate modulation index. D2, RS unit strongly activated by callosal input. D3, left, Modulation index of units significantly activated (red) or inhibited (blue) across all layers. Open circles indicate units without significant effect and points marked 1 and 2 represent units in D1, D2, respectively. Right, Pie charts indicate proportion of units excited (red), inhibited (blue), or not significantly modulated (gray) in each layer. E, Activation of callosal inputs activates FS cells across all layers. Two representative FS units are plotted in E1, E2. E3, Modulation index of FS units across all cell layers are illustrated as for RS cells in D3.

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    Figure 2.

    Cortical callosal inputs preferentially excite PV cells and drive strong feedforward inhibition. A1, L2/3 PV cells receive stronger callosal fiber-evoked EPSCs and have a larger E/I ratio than L2/3 pyramidal cells. Top, Recording configuration. Middle, Simultaneous voltage-clamp recording of L2/3 pyramidal cell (Pyr) and PV cell showing EPSCs (inward currents, −70 mV) and IPSCs (outward currents, +10 mV) evoked by brief LED illumination (blue bars) of ChR2-expressing callosal fibers. Bottom, Summary of EPSC peak amplitudes and E/I ratios for recorded pairs. Black lines, individual cell pairs. Red circles, mean ±SEM. A2, L5 PV cells receive stronger callosal fiber-evoked EPSCs and have a larger E/I ratio than L5 pyramidal cells. A3, L5 PV cells receive stronger callosal fiber-evoked EPSCs and have a larger E/I ratio than L2/3 PV cells. B, SOM cells in L2/3 (B1) and L5 (B2) receive weaker callosal fiber-evoked EPSCs than neighboring pyramidal cells. C, VIP cells in L2/3 (C1) receive weaker callosal fiber-evoked EPSCs than neighboring pyramidal cells. The strength of callosal input-evoked EPSCs in L5 VIP cells (C2) and pyramidal cells are similar.

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    Figure 3.

    Acute optogenetic silencing of interhemispheric cortical input causes a sustained increase in spontaneous activity in most layers of A1. A, Local activation of ChR2-expressing interneurons silences RS cell activity. A1, Recording configuration. A2, Spike raster (top) and peristimulus time histogram (PSTH; bottom) show strong activation of a representative FS unit by an ipsilateral LED pulse train (blue bars). A3, Spike raster (top) and PSTH (bottom) show strong suppression of simultaneously recorded RS unit. A4, Summary of ipsilateral LED-evoked suppression of RS activity (n = 34 units, 2 mice). B, Activation of ChR2-expressing interneurons in one hemisphere leads to transient inhibition followed by excitation in contralateral A1. B1, Recording configuration. B2, left, Coronal section showing ChR2 expression (green) within A1 of the injected left hemisphere (Inj) and DiI-labeled recording electrode tract (red) in contralateral A1 (Rec). Right, Blow-up of recording site. WM = white matter. C, Average normalized PSTH of RS (black) and FS (red) units shows that sustained LED illumination (bar) drives transient decrease and sustained increase in firing. Shading, ±SEM D, Inactivation of A1 causes sustained increase in activity of RS units in layers 1–5 of contralateral A1. D1, Individual L5 RS unit spike raster and PSTH showing that silencing contralateral A1 (blue shading) enhances firing. Gray shading indicates measurement period used to calculate modulation index. D2, L6 RS unit with sustained suppression during silencing of contralateral A1. D3, left, Modulation index of units significantly activated (red) or inhibited (blue) across all layers. Open circles indicate units without significant effect and cells marked 1 and 2 represent units in D1, D2, respectively. Right, Pie charts indicate proportion of units excited (red), inhibited (blue), or not significantly modulated (gray) in each layer. E, Silencing contralateral A1 causes a rapid and sustained decrease in firing in deep layer FS cells, as well as a sustained firing increase in upper layer FS cells. Representative L2/3 and L5 FS unit are plotted in E1, E2, respectively. E3, Modulation index of FS units across all cell layers are illustrated as in D3.

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    Figure 4.

    Silencing interhemispheric cortical input degrades the fidelity and frequency tuning of tone-evoked responses in A1. A, Recording configuration. B, Silencing contralateral A1 linearly modulates tone evoked activity via a combination of additive and divisive operations. B1, Peristimulus time histograms (PSTHs) of tone-evoked responses from a representative RS unit to four frequencies (black bars) under control conditions (black line) and during contralateral silencing (blue line) on interleaved trials. Blue bars, LED pulse train. Gray, measurement windows for tone-evoked firing rate. B2, Plot of firing rates during tones (n = 9 frequencies) with the LED on versus LED off of the cell in B1. Line is linear fit: slope = 0.73, y-intercept = 12.63, r2 = 0.96. C, Silencing callosal input exerts divisive and additive actions on tone-evoked activity across cortical layers. C1, Slopes derived from linear fits to individual RS units with significant tone-evoked activity in each cortical layer. Blue circles, slope significantly <1. Red circles, slope significantly >1. Open circles, no significant change in slope. Pie charts represent fraction of cells in each layer with divisive (blue, slope <1), multiplicative (red, slope >1), or no significant effect (gray, NS). C2, Y-intercepts derived from linear fits to same RS units in C1. Blue circles, y-intercept significantly less than 0. Red circles, y-intercept significantly >0. Open circles, y-intercept not significantly different from 0. Pie charts represent fraction of cells in each layer with additive (red, y-intercept >0), subtractive (blue, y-intercept <0), or no significant effect (gray, NS). D1, d’ of RS units with LED off versus LED on shows that cortical silencing reduces response detectability. D2, Cortical silencing “flattens” frequency tuning curves. Average tuning curves of RS units centered to their BF under control conditions (black) and during contralateral cortical silencing (blue). Asterisks indicate frequencies with significant difference (paired t test, Holm–Bonferroni corrected).

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Interhemispheric Callosal Projections Sharpen Frequency Tuning and Enforce Response Fidelity in Primary Auditory Cortex
Bernard J. Slater, Jeffry S. Isaacson
eNeuro 7 August 2020, 7 (4) ENEURO.0256-20.2020; DOI: 10.1523/ENEURO.0256-20.2020

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Interhemispheric Callosal Projections Sharpen Frequency Tuning and Enforce Response Fidelity in Primary Auditory Cortex
Bernard J. Slater, Jeffry S. Isaacson
eNeuro 7 August 2020, 7 (4) ENEURO.0256-20.2020; DOI: 10.1523/ENEURO.0256-20.2020
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Keywords

  • callosal
  • electrophysiology
  • interneuron
  • neural circuits
  • optogenetic
  • sensory coding

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