Feedback optimizes neural coding and perception of natural stimuli

6 figures and 1 additional file

Figures

(A) Schematic of the experimental setup showing the awake-behaving preparation where a stimulus (left) is presented to the animal while neural (upper middle) and behavioral (upper right) responses are recorded simultaneously.

The stimuli consisted of amplitude modulations of the animal’s own EOD: shown are an example AM waveform (blue), its envelope (red), and the full signal received by the animal (cyan) with their …

https://doi.org/10.7554/eLife.38935.002
Principle of whitening by which the neural tuning curve (center) increases in order to effectively compensate for the decaying power spectrum of natural envelope stimuli (left), such that the resulting response power is independent of frequency (i.e., ‘whitened’, right).
https://doi.org/10.7554/eLife.38935.003
Summary of the different manipulations that were performed to either completely or selectively inactivate feedback input onto ELL pyramidal cells.

In all cases, neural recordings were obtained from pyramidal cells within the ipsilateral ELL. (A) Schematic showing a method to inactivate both the direct and the indirect feedback pathways (i.e., …

https://doi.org/10.7554/eLife.38935.004
Figure 4 with 3 supplements
Feedback input enhances and optimizes information transmission via whitening.

Results are shown before and after complete feedback inactivation was achieved via injection of lidocaine into nP. (A) Top: sinusoidal envelope waveform (red). Middle: time dependent firing rate …

https://doi.org/10.7554/eLife.38935.005
Figure 4—figure supplement 1
Complete feedback inactivation does not affect ELL pyramidal cell responses to AMs.

(A) Spike-triggered average (STA) of the noisy AM stimulus waveform before (black) and after (purple) complete feedback inactivation for a typical ON-type pyramidal cell. (B) Population-averaged STA …

https://doi.org/10.7554/eLife.38935.006
Figure 4—figure supplement 2
Sham complete feedback inactivation achieved by injecting saline bilaterally into nP has no effect on behavior and ELL pyramidal cell tuning properties, as well as optimized coding of natural stimuli.

(A) Top: sinusoidal envelope waveform (red). Middle: time dependent firing rate from a typical ELL pyramidal cell before (black) and after (beige) saline application. Bottom: spiking activity from …

https://doi.org/10.7554/eLife.38935.007
Figure 4—figure supplement 3
Contralateral feedback inactivation achieved by injecting lidocaine into the contralateral nP gives rise to effects qualitatively similar to those observed when injecting lidocaine bilaterally when recording from pyramidal cells within the ipsilateral ELL.

(A) Top: sinusoidal envelope waveform (red). Middle: time dependent firing rate from a typical ELL pyramidal cell before (black) and after (purple) contralateral lidocaine application. Bottom: …

https://doi.org/10.7554/eLife.38935.008
Figure 5 with 3 supplements
Direct feedback input enhances while indirect input optimizes neural responses.

Results are shown before and after indirect feedback inactivation was achieved via bilateral injection of lidocaine into the PET. Data obtained from ELL pyramidal neurons were pooled as there are no …

https://doi.org/10.7554/eLife.38935.009
Figure 5—figure supplement 1
Indirect feedback inactivation achieved by injecting lidocaine bilaterally into PET increases ELL pyramidal cell responses to AMs, consistent with previous results (Bastian, 1986b).

(A) Spike-triggered average (STA) of the noisy AM stimulus waveform from an example ELL pyramidal cell before (black) and after (orange) lidocaine injection. (B) Population-averaged STA amplitude …

https://doi.org/10.7554/eLife.38935.010
Figure 5—figure supplement 2
Indirect feedback inactivation achieved by injecting CNQX within the ELL molecular layer gives rise to effects on ELL pyramidal cell responses to envelopes that are qualitatively similar to those observed when injecting lidocaine into PET.

(A) Top: sinusoidal envelope waveform (red). Middle: time dependent firing rate from a typical ELL pyramidal cell before (black) and after (orange) CNQX application. Bottom: spiking activity from …

https://doi.org/10.7554/eLife.38935.011
Figure 5—figure supplement 3
Indirect feedback inactivation achieved by injecting CNQX within the ELL molecular layer increases ELL pyramidal cell responses to AMs, consistent with previous results (Bastian et al., 2004; Clarke and Maler, 2017).

(A) Spike-triggered average (STA) of the noisy AM stimulus waveform from an example ELL pyramidal cell before (black) and after (orange) CNQX injection. (B) Population-averaged STA amplitude was …

https://doi.org/10.7554/eLife.38935.012
Figure 6 with 1 supplement
nP neurons projecting indirectly to ELL display tuning properties that are optimized to natural stimulus statistics.

(A) Recordings were obtained from either Stellate (St) or multipolar (MP) cells within nP. (B) Top: sinusoidal envelope waveform (red). Bottom: Time dependent firing from typical nP stellate (brown) …

https://doi.org/10.7554/eLife.38935.013
Figure 6—figure supplement 1
Distinguishing between nP stellate and multipolar cells using previously characterized differences in their electrophysiological properties.

(A) Brown: AM frequency tuning curve for nP stellate cells. Note that the tuning curve rapidly drops off at higher frequencies > 32 Hz due to a lack of spiking responses to those frequencies. Orange:

https://doi.org/10.7554/eLife.38935.014

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