Optogenetically induced low-frequency correlations impair perception

  1. Anirvan Nandy  Is a corresponding author
  2. Jonathan J Nassi
  3. Monika P Jadi
  4. John Reynolds
  1. The Salk Institute for Biological Studies, United States
  2. Yale University, United States
11 figures and 1 additional file

Figures

Surface Optogenetics and electrophysiology through an artificial dura.

(A) Schematic of an artificial dura (AD) chamber. A portion of the native dura mater (red) is resected and replaced with a silicone based optically clear artificial dura (AD). The optical clarity of …

https://doi.org/10.7554/eLife.35123.002
Figure 2 with 5 supplements
Optogenetically-induced low-frequency correlations cause a frequency- and spatially-selective impairment in an attention-demanding orientation discrimination task.

(A) Attention task: While the monkey maintained fixation, two oriented Gabor stimuli (schematized as oriented bars) flashed on and off simultaneously at two spatial locations: one at the RF of the …

https://doi.org/10.7554/eLife.35123.003
Figure 2—figure supplement 1
Orientation tuning properties at opsin injection sites.

Orientation tuning plots of single units and multi-unit activity at the different cortical injection sites (two in monkey A, one in monkey C) were fitted with ellipses (least-squares fit). The …

https://doi.org/10.7554/eLife.35123.004
Figure 2—figure supplement 2
Behavioral performance.

(A) Left panel: example behavioral session showing performance (hit rate) as a function of task difficulty (size of orientation change) for the baseline condition (no optical stimulation). Square …

https://doi.org/10.7554/eLife.35123.005
Figure 2—figure supplement 3
Behavioral changes with optical stimulation.

(A) Change in psychometric function slope due to low-frequency optical stimulation when the monkey was attending in to the site of optical stimulation. The solid line represents the mean of the …

https://doi.org/10.7554/eLife.35123.008
Figure 2—figure supplement 4
Other control conditions.

(A) Stimulation at a non-opsin site does not perturb behavior. (B) Stimulation with optical fiber outside the brain (with the opto-physiology chamber closed) does not perturb behavior.

https://doi.org/10.7554/eLife.35123.006
Figure 2—figure supplement 5
Irradiance response curves.

Response of two neurons to presentations of a visual stimulus and simultaneous optical stimulation. The visual stimulus was a 20% contrast Gabor stimulus presented for 200ms. The optical stimulation …

https://doi.org/10.7554/eLife.35123.007
Optical stimulation at low- and high-frequencies induces low- and high-frequency correlated activity.

(A) Consistent with earlier reports (Mitchell et al., 2009), attention reduces baseline spike-count correlations at low frequencies (200ms counting window, p=0.02; left panel, white versus gray bar) but …

https://doi.org/10.7554/eLife.35123.009
Figure 4 with 5 supplements
Low-frequency stimulation induces phase-locking without increasing firing rates.

(A) Peri-stimulus time histograms (PSTH) of two example units for the different experimental conditions. Both units show a robust firing rate modulation due to attention (solid versus dashed lines) …

https://doi.org/10.7554/eLife.35123.010
Figure 4—figure supplement 1
Comparison of spike rates between baseline and optical stimulation.

Comparison of spike rates between the optical stimulation conditions (low-frequency: left panels; high-frequency: right panels) and the baseline condition for a 200 ms pre-stimulus period (top …

https://doi.org/10.7554/eLife.35123.011
Figure 4—figure supplement 2
Phase-locking to optical stimulation.

(A) Phase plots for an example unit showing the distribution of spiking activity with respect to the phase of the low-frequency (5Hz, left) and high-frequency (20Hz, right) optical stimulation. In …

https://doi.org/10.7554/eLife.35123.012
Figure 4—figure supplement 3
Behavioral performance is not affected by optical stimulation phase.

(A) Phase plots showing the distribution of target stimulus onset times with respect to the phase of the low-frequency (5 Hz, left) and high-frequency (20 Hz, right) optical stimulation. Mean ± s.e.m…

https://doi.org/10.7554/eLife.35123.013
Figure 4—figure supplement 4
Optical stimulation does not change orientation tuning.

Orientation tuning curves for the neuronal population with and without optical stimulation (left panel, low-frequency stimulation condition, n=68 units; right panel, high-frequency stimulation …

https://doi.org/10.7554/eLife.35123.014
Figure 4—figure supplement 5
Optical stimulation does not cause frequency-specific adaptation.

(A) Responses evoked by the first four non-target stimuli, for trials in which attention was cued to the stimuli appearing at the opsin site. Responses were averaged and normalized for each neuron …

https://doi.org/10.7554/eLife.35123.015
Optical modulation of neural discriminability correlates with behavioral perturbations.

(A) Schematic of neural discriminability analysis. The responses of a hypothetical set of 3 neurons to target (green) and non-target (magenta) stimuli are depicted as point clouds. Each dot …

https://doi.org/10.7554/eLife.35123.016
Figure 6 with 2 supplements
Low-frequency sub-threshold stimulation induces coherent activity in a computational model of E-I neurons.

(A) Schematic of a local conductance-based E-I network with mutually coupled excitatory (E) and inhibitory (I) units. A fraction (50%) of the E units are sensitive to 'optical' stimulation. Wee, …

https://doi.org/10.7554/eLife.35123.017
Figure 6—figure supplement 1
Induction of coherent activity in the E-I model is robust across network and stimulation parameters - I.

(A)-(B) same as Figure 6A-B. (C) Spike-spike coherence modulation index (SSC MI; see Figure 6D) as a function of varying the self-coupling parameters Wee and Wii, keeping the other two parameters …

https://doi.org/10.7554/eLife.35123.018
Figure 6—figure supplement 2
Induction of coherent activity in the E-I model is robust across network and stimulation parameters - II.

(A) Spike-spike coherence modulation index (SSC MI; see Figure 6D) as a function of varying the cross-coupling parameters Wie and Wei, keeping the other two parameters fixed (Wee=16, Wii=-1). (B) SSC MI as a …

https://doi.org/10.7554/eLife.35123.019
Author response image 1
Author response image 2
Examples of behavioral sessions without optogenetic stimulation.

The red asterisks mark behavioral sessions where the baseline orientation (orientation of the non-target stimuli) was either horizontal or vertical.

Author response image 3
Phase dependence of spike-count correlations for both low- (left panel, 200ms counting window) and high-frequency correlations (right pane, 50ms counting window) for the low-frequency optical stimulation condition.
Author response image 4
Author response image 5

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