Premature vision drives aberrant development of response properties in primary visual cortex
- Department of Biology, Brandeis University, United States
- Volen Center for Complex Systems, Brandeis University, United States
- Sloan-Swartz Center for Theoretical Neurobiology, Brandeis University, United States
Figures
Figure 1
Recording schematics, experimental timeline, and electrode track reconstructions.
(A) Recording schematics: EO1contra cells were those recorded in monocular cortex contralateral to a single prematurely opened eye. EO1ipsi cells were those recorded in monocular cortex ipsilateral to a single prematurely opened eye. Dots schematize ocular dominance columns. (B) EO2 cells were those recorded in monocular cortex after both eyes were opened prematurely. (C) Control cells were those recorded in monocular cortex after both eyes were allowed to open naturally. (D) Experimental timeline. Animals that experienced premature vision had one eye or both eyes opened on P25. All animals experienced a period outside of the nest in the form of daily 2 hr handling sessions beginning on P25 and ending on P28, allowing unguided viewing of the laboratory environment through prematurely opened eyes or low resolution experience through closed lids. Electrophysiological recording took place between P55-68, at a time when the critical period for ocular dominance was closing or closed (Issa et al., 1999). (E) Electrode track reconstructions showing penetrations (bright spots at right/posterior) along the posterior cortical surface, in monocular V1 (Law et al., 1988; White et al., 1999). Following the recording, the recording electrode was removed and replaced with a marking electrode coated in DiI.
Figure 2
Early eye opening produced only minor changes in orientation and direction selectivity index values: (A) Example direction tuning curves of individual EO1contra cells measured after the close of the critical period.
Direction tuning curves are shown for stimulation at the optimal temporal frequency. Direction tuning curves look coarsely normal. Vertical scale bar represents 10 spikes per second (standard indicated in italics) unless otherwise indicated. The dashed line shows mean response to blank / control stimuli. Number indicates 1-DCV value. (B) Same, for EO2 cells (C) Same, for EO1ipsi cells: (D) Same, for control cells (E) Orientation tuning curves of individual EO1contra cells, measured in different epochs and in some different animals than the direction tuning curves. Temporal frequency was 2 Hz, and the spatial frequency was optimal for each cell. Numbers indicate orientation selectivity index values 1-CV. (F) EO2 cells G: EO1ipsi cells (H) control cells (I) Results of a linear mixed effects analysis of direction selectivity index values, as assessed by (1-DCV), for all cells and conditions in the study. Each small column shows the cells for an individual animal. Yellow lines indicate random effect values for each animal. Gray lines indicate condition means and standard errors of the mean from the linear mixed effect model. Animals within a group have been sorted by mean index value. Condition coefficients that differ significantly from 0 are indicated with * (p<0.05), and conditions compared are indicated by comparison bars. See text for p values. (J) Same for orientation selectivity index values (1-CV) . EO1contra and EO2 cells exhibited slightly higher orientation selectivity index values than control animals, while EO1ipsi cells exhibited slightly lower direction selectivity values than other conditions.
Figure 3 with 1 supplement
Premature eye opening altered temporal frequency tuning after maturity.
Representative temporal frequency tuning curves recorded from single cells: (A) EO1contra: cells contralateral to a single prematurely opened eye. Several cells exhibited strong responses at the lowest temporal frequency tested (that is, several exhibited low-pass tuning). Temporal frequency was reported at each cell’s overall preferred direction (assessed over all temporal frequencies). Number indicates bandwidth in octaves. -∞ is low-pass. Vertical scale bar indicates firing rate (20 spikes/sec standard in italics unless otherwise noted). (B) EO2: cells recorded in an animal with both eyes prematurely opened. Again, many cells exhibited low-pass responses. (C) EO1ipsi: cells ipsilateral to a single prematurely opened eye. (D) Control: cells recorded in animals that opened both eyes naturally. (E) Linear mixed effects model plot of median temporal frequency preference; linear mixed effects plotted as in Figure 2. Median temporal frequency preference was slightly higher in EO1ipsi cells than other cells. (F) Temporal frequency low-pass index values were significantly elevated in EO1contra cells, indicating stronger responses to the lowest temporal frequency tested. (G) No differences were observed in high pass index values. (H) Bandwidth of the rectified response. (I) Bandwidth of the absolute value of responses. Cells in animals that experienced early eye opening exhibited wider bandwidths (less selectivity) than control animals. See text for numbers and p-values.
Figure 3—figure supplement 1
Premature eye opening alters L50 and H50 values.
(A) Temporal frequency L50 values across the experimental conditions. E01contra cells exhibited significantly lower L50 values than control animals (p<0.002, LMEM). (B) EO2 cells, by contrast, exhibited widened bandwidths by showing increased H50 values (p<0.004, LMEM). (C) Considering the absolute value of the temporal frequency response (where deviations above or below background firing rates contributed to response), EO1contra cells again exhibited significantly lower L50 values compared to control cells (p<0.00029, LMEM). EO1ipsi cells exhibited a slight increase in L50 values (p<0.0148, LMEM). (D) EO1ipsi cells showed a substantial increase in absolute H50 cutoff values (p<0.00169, LMEM).
Figure 4
Premature eye opening had very small impacts on spatial frequency tuning.
(A) Example spatial frequency tuning curves in EO1contra cells. (B) Same for EO2 cells. (C) Same for EO1ipsi cells. (D) Same for control cells. (E) Spatial frequency peak preferences for all cells, animals, and experimental groups (same linear mixed effect model plot layout as Figure 2). (F) Spatial frequency low-pass index values. EO1ipsi cells exhibit a slightly significant (p<0.499) decrease in low-pass index but differences across groups were small. (G) High pass index values for spatial frequency; differences were modest across groups although cells with strong high-pass responses were more common in EO2 cells. (H) Spatial frequency bandwidth, in octaves. Most cells exhibited low-pass profiles and had infinite bandwidth, and no differences were noted across the groups. (I) Spatial frequency bandwidth for absolute response.
Figure 5
Premature eye opening altered response suppression below baseline and spontaneous activity of V1 neurons.
(A) Maximum firing rates of cells to visual stimulation were unchanged across experimental conditions. (B) Response suppression rates, defined as the largest reduction in responses to visual stimulation below background firing rates, were substantially bigger in EO1ipsi, EO1contra, and EO2 cells, indicating that responses below baseline were features of the stimulus response in many of these cells. (C) Background firing rates. Responses of cells during presentation of control stimuli, where the screen remained gray for the same duration as our typical visual stimuli. EO1ipsi, EO1contra, and EO2 cells showed greatly and significantly elevated firing rates compared to controls. See text for numbers.
Tables
Key resources table
| Reagent type (species) or resource | Designation | Source or reference | Identifiers | Additional information |
|---|---|---|---|---|
| Biological sample (Ferret) | Ferret | Marshall Bio-Resources | Mustelo putorius furo | Female ferrets used |
| Antibody | Rabbit anti-NeuN, Alexa Fluor 488 conjugated | Millipore | Cat# ABN78A4 | Dilution: 1:300 |
| Chemical compound, drug | Ketamine | Patterson Veterinary | 07-890-8598 | 20 mg kg⁻¹ im |
| Chemical compound, drug | Isoflurane Covetrus | Covetrus | 029405 | 1.5–3% in N₂O/O₂ mixture for surgery |
| Chemical compound, drug | Isoflurane Covetrus | Covetrus | 061843 | Infused into wound margins |
| Chemical compound, drug | Dexamethasone | Patterson Veterinary | 07-808-8194 | 0.5 mg kg⁻¹ im |
| Chemical compound, drug | Atropine | Patterson Veterinary | 07-869-6061 | 0.16–0.8 mg kg⁻¹ im |
| Chemical compound, drug | Gallamine triethiodide | Sigma Aldrich | G8134-25G | 10–30 mg kg⁻¹ h⁻¹ |
| Chemical compound, drug | Sodium pentobarbital (Euthasol) | Patterson Veterinary | 07-805-9296 | 200 mg/kg, IP |
| Chemical compound, drug | DiI | Sigma Aldrich | 42364–100 MG | Used for electrode track reconstruction (DiCarlo et al., 1996) |
| Chemical compound, drug | Paraformaldehyde | Sigma Aldrich | P6148-1KG | 4% in 0.1 M PBS |
| Chemical compound, drug | Triton-X 100 | Sigma Aldrich | 9002-93-1 | 0.3% in PBS |
| Chemical compound, drug | Fluoromount-G | Southern Biotech | 0100–20 | |
| Software, algorithm | MATLAB | MathWorks | RRID:SCR_001622 | Used for stimulus creation and data analysis |
| Software, algorithm | Psychophysics Toolbox | Brainard, 1997; Pelli, 1997 | RRID:SCR_002881 | Used for visual stimuli display |
| Software, algorithm | Spike2 | Cambridge Electronic Design | RRID:SCR_000903 | Used for stimulus timing acquisition |
| Software, algorithm | JRClust | Jun et al., 2017 | Used for offline spike sorting in Matlab | |
| Software, algorithm | fitlme | Matlab | N/A | Used for linear mixed-effects modeling |
| Software, algorithm | Neuroscience Data Interface (NDI) | García Murillo et al., 2022 | RRID:SCR_023368 | Data management and sharing |
| Other | Multichannel electrodes | Plexon | Plexon S probes | 32 channels, 50 µm spacing |
| Other | Amplifier/Digitizer | Intan Technologies | RHD2000 system | |
| Other | Data acquisition board | Cambridge Electronic Design | Micro1401 | |
| Other | Manipulator | Sutter Instruments | MP-285 | |
| Other | CRT Monitor | Sony | GDM-520 | 21-inch, 800x600, 100 Hz |
| Other | Ophthalmoscope | Heine | Heine Omega 600 | |
| Other | Ophthalmic Lens | Volk | 78D or 90D lens | |
| Other | Sliding Microtome | Leica | SM2010R | |
| Other | Fluorescent Microscope | Keyence | BX-Z 710 | |
| Other | Brandeis Light Microscopy Core Facility | Brandeis University | RRID:SCR_025892 | Houses SM2010R and BX-Z 710 |
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Premature vision drives aberrant development of response properties in primary visual cortex
eLife 14:RP106513.
https://doi.org/10.7554/eLife.106513.3
