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. 2013 Nov 6;33(45):17789-96.
doi: 10.1523/JNEUROSCI.1500-13.2013.

Visual acuity development and plasticity in the absence of sensory experience

Erin Kang  1 , Severine Durand, Jocelyn J LeBlanc, Takao K Hensch, Chinfei Chen, Michela Fagiolini
Affiliations

Visual acuity development and plasticity in the absence of sensory experience

Erin Kang et al. J Neurosci. .

Abstract

Visual circuits mature and are refined by sensory experience. However, significant gaps remain in our understanding how deprivation influences the development of visual acuity in mice. Here, we perform a longitudinal study assessing the effects of chronic deprivation on the development of the mouse subcortical and cortical visual circuits using a combination of behavioral optomotor testing, in vivo visual evoked responses (VEP) and single-unit cortical recordings. As previously reported, orientation tuning was degraded and onset of ocular dominance plasticity was delayed and remained open in chronically deprived mice. Surprisingly, we found that the development of optomotor threshold and VEP acuity can occur in an experience-independent manner, although at a significantly slower rate. Moreover, monocular deprivation elicited amblyopia only during a discrete period of development in the dark. The rate of recovery of optomotor threshold upon exposure of deprived mice to light confirmed a maturational transition regardless of visual input. Together our results revealed a dissociable developmental trajectory for visual receptive-field properties in dark-reared mice suggesting a differential role for spontaneous activity within thalamocortical and intracortical circuits.

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Figures

Figure 1.
Figure 1.
Sample orientation selectivity plots showing the response of a binocular visual cortical neuron to the stimulation of the contralateral (left plot) and ipsilateral (right plot) eye. Twelve different orientations spaced 30 degrees apart were shown. The ocular dominance score for this cell was −0.015 and the cell would be classified as a 4 on the 1–7 ocular dominance scale, meaning that the cell responded equally strong to stimulation of both eyes.
Figure 2.
Figure 2.
Development of optomotor threshold and visual acuity is delayed by CDR. A, Representative examples of VEPs in response to alternating gratings of different spatial frequencies in a LR and CDR mouse at P34–P35 (left) and P55–P65 (right), respectively. VEP amplitudes decrease with increasing spatial frequency of stimulus and become undistinguishable from response to a blank field (noise). Visual acuity is calculated by linear extrapolation (log coordinates) to 0 μV of the last 4 data points. B, Left, Both optomotor threshold and VEP acuity were significantly reduced in CDR (gray) compared with LR (white) mice at postnatal day P34–P35 (OPT: n = 7–12 mice, ***p < 0.001; VEP: n = 4–5 mice, **p = 0.002). B, Right, Both optomotor threshold and VEP acuity reached LR levels by in CRD (gray) compared with LR (white) mice at postnatal day P55–P65 (OPT: n = 10–12 mice; VEP: n = 11 mice, p = 0.37).
Figure 3.
Figure 3.
Development of optomotor threshold. The developmental trajectory of optomotor responses is delayed in CDR (black circle) compared with LR mice (open circles) reaching the adult LR level only after P55 (LR vs CDR, ***p < 0.001 for P18, P25, and P27; **p < 0.01 for P34/35, P45). LR and CDR conditions are significantly different by two-way ANOVA [taking a random subset of equal data points at ages P18, P20, P25, P27, P45, P54; the p value for interaction, age and visual condition (LR vs CDR) are all <0.0001].
Figure 4.
Figure 4.
Onset of critical period for OD plasticity is delayed in CDR mice. A, Both LR and DR exhibit the typical response bias toward contralateral eye input (ocular dominance Groups 1–3) in the binocular zone of mice (χ2 test, p = 0.13, LR vs CDR, 210 and 172 cells; 8 and 6 mice respectively). OD distribution is robustly shifted in favor of the ipsilateral open eye (Groups 5–7) following MD during the CP but not in adulthood in LR mice (χ2 test, p < 0.0001, LR vs LR + MD, 246 cells, 10 mice; p = 0.42, vs Adult LR + MD, 92 cells, 3 mice). On the contrary, CDR mice do not display a significant OD shift toward the open ipsilateral eye at the peak of CP (χ2 test, p = 0.37, CDR vs CDR + MD, 106 cells, 4 mice; p < 0.0001; vs adult CDR+, 148, 5 mice, respectively) but they do instead in adulthood (χ2 test, p < 0.0001, CDR vs adult CDR + MD, 172 and 148 cells; 6 and 5 mice; p < 0.0001; adult CDR + MD vs adult LR + MD, 148 and 92 cells; 5 and 3 mice, respectively). B, CBI over postnatal development in LR and CDR mice. Histograms are quantified as a weighted average (CBI) which ranges from 0 to 1 for complete ipsilateral or contralateral eye dominance, respectively. One week after eye opening at P13–P14, sensitivity to brief MD rapidly appears and persists for ∼10 d, as measured by single unit recordings. The immature pre-CP phase is extended by CDR such that the overall profile is delayed to yield plasticity starting from P33 (t test, vs LR: p = 0.15, CDR + P27MD, 106 cells, 4 mice; p < 0.002, CDR + P33MD, 82 cells, 3 mice; p < 0.003, CDR + P55MD, 148 cells, 5 mice) until adulthood when mice are exposed for the first time to light. Shaded region is the range of nondeprived LR mice. Some error bars are smaller than symbol size. (t test p < 0.01; CDR + 2 d light + MD, 151 cells, 5 mice; p < 0.04, CDR + 4 d light + MD, 88 cells, 3 mice; p = 0.8, CDR + 15 d light + MD, 81 cells, 3 mice vs LR, respectively).
Figure 5.
Figure 5.
Uncoordinated maturation of receptive field properties in CDR mice. Effects of 4 d MD on acuity (VEPs) during development (A) and in the adult (B). Comparison of MD to control in P24–P30 mice: LR (n = 5–7, **p = 0.01), CDR animals (n = 6–9); in P44–P49 mice: LR (n = 4–7), CDR (n = 4–5, *p = 0.02); and in the adult LR (n = 5); CDR animals (n = 7–12). C, Orientation selectivity index is significantly reduced in CDR mice (n = 80 cells) when compared with LR mice (n = 67 cells; Kolmogorov–Smirnov test, p = 0.01). Inset, Examples of orientation tuning curve for high (0.71) and low OSI (0.0853) visual cortical neurons in CDR mice.
Figure 6.
Figure 6.
Exposure to light triggers rapid maturation of visual function in CDR mice. A, Mean OPT response of CDR mice upon exposure to light at different ages. B, Comparison of sigmoidal (red) versus double exponential (gray) fits to the time course of OPT threshold during normal development (left, LR) and for CDR mice after exposure to light at P27 (right, CDR P27). χ2 = 40, 23, 2.2, 54, 2.45, 21.6 vs 123.6, 18.4, 4.2, 57, 5, 2.74, 2.38 for sigmoidal vs double exponential fit, respectively, for the following conditions: LR, P18 CDR, P20 CDR, P27 CDR, P34 CDR, and P45 CDR. C, T1/2 of maturation from different ages.
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