Experience-dependent specialization of receptive field surround for selective coding of natural scenes

Abstract

At eye opening, neurons in primary visual cortex (V1) are selective for stimulus features, but circuits continue to refine in an experience-dependent manner for some weeks thereafter. How these changes contribute to the coding of visual features embedded in complex natural scenes remains unknown. Here we show that normal visual experience after eye opening is required for V1 neurons to develop a sensitivity for the statistical structure of natural stimuli extending beyond the boundaries of their receptive fields (RFs), which leads to improvements in coding efficiency for full-field natural scenes (increased selectivity and information rate). These improvements are mediated by an experience-dependent increase in the effectiveness of natural surround stimuli to hyperpolarize the membrane potential specifically during RF-stimulus epochs triggering action potentials. We suggest that neural circuits underlying surround modulation are shaped by the statistical structure of visual input, which leads to more selective coding of features in natural scenes.

Figure 1

Surround-Induced Increases in Response Suppression and Selectivity Are Present in Immature V1 but Are More Pronounced in Mature V1 (A) Schematic depicting whole-cell patch-clamp recordings of neurons in the monocular region of primary visual cortex (V1) of anesthetized mice. The size of the receptive field (RF) and the influence of the surround were determined by presentation of a naturalistic movie to the contralateral eye, by varying the size of the center (aperture) and surrounding (annulus) stimuli. (B) Averaged normalized size-tuning functions of V1 neurons in mature and immature mice. The mean normalized firing rates (±SEM) at aperture sizes relative to optimal RF size (“1”) are shown for apertured (RF only) and corresponding annulus (surround only) stimuli. Only neurons with similar increments in aperture size were included for this analysis (mature, n = 18; immature, n = 17). (C) Example whole-cell recording from a neuron in mature V1 during stimulation of RF or RF + natural surround. Voltage traces of a single repetition are shown with spike-dot-raster and spike-histogram of ten repetitions overlaid underneath the trace. Lower panels show metrics derived from this example recording, including mean firing rate (±SEM, left panel), selectivity index (middle panel), and mutual information/spike (right panel). (D) Example whole-cell recording from a neuron in immature V1 (postnatal day 18) during stimulation of the RF and RF + natural surround. Conventions as in (C). (E) Mean aperture (RF) diameter (±SEM) for all neurons recorded in mature (29.9° ± 10°; n = 21) and immature mice (35.3° ± 18°, n = 18) was not significantly different (p = 0.26, t test). (F–H) Mean population changes (%± SEM) in firing rate (F), selectivity (G), and mutual information/spike (H) during RF + natural surround stimulation normalized to RF stimulation for mature (black symbols) and immature (white symbols) mice. p values refer to differences in mean change across age groups (t test).

Figure 2

Neurons Are Sensitive to Natural Stimulus Statistics in the RF Surround in Mature, but Not in Immature, V1 (A) Example whole-cell recording from a layer 2/3 neuron in V1 of a mature mouse (postnatal day 36) during stimulation of the RF (left panel, blue trace), RF + natural surround (middle panel, green trace), and RF + phase-randomized surround (right panel, magenta trace). Conventions as in Figure 1C. (B) Firing rates during the three stimulus conditions (left panel), and changes (%) in firing rate (right panel) during stimulation of the RF + natural surround (green) or RF + phase-randomized surround (magenta) relative to stimulating the RF center in mature mice. Mean firing rates for each cell are shown by connected open circles. Horizontal bars denote group mean values. (C and D) Changes (%) in selectivity (C) and information/spike (D) during stimulation of the RF + natural surround (green) or RF + phase-randomized surround (magenta) relative to stimulating the RF center in mature mice (n = 21 cells; p values, paired t test). (E) Example whole-cell recording from a L2/3 neuron in immature V1 (postnatal day 16). Conventions as in (A). (F) Firing rate during the three stimulus conditions (left panel), and changes (%) in firing rate (right panel) during stimulation of the RF + natural surround (green) or RF + phase-randomized surround (magenta) relative to stimulating the RF center in immature mice (n = 13 cells). (G and H) Changes (%) in selectivity (G) and information/spike (H) during stimulation of the RF + natural surround (green) or RF + phase-randomized surround (magenta) relative to stimulating the RF center in immature mice. (n = 13 cells; p values, paired t test).

Figure 3

Natural and Phase-Randomized Surround Stimulation Elicits Significantly Different Hyperpolarization during RF Spiking Events in Mature, but Not Immature, V1 (A) Example recording from a L2/3 neuron in mature V1 (postnatal day 36) during presentation of the same movie sequence confined to the RF (blue) or when costimulating the surround with natural (green) or phase-randomized (magenta) movie. (B) The median Vm of mature V1 neurons (n = 21) during stimulation of the RF (blue), RF + natural surround (green) and RF + phase-randomized surround (magenta) was significantly different (RF, −62.8 mV; RF + natural surround, −61.6 mV; RF + phase-randomized surround, −60.9 mV; p = 9 × 10⁻⁶; Friedman’s test). Black mark inside colored box denote median values, while the box edges denote the 25th and 75th percentiles and the whiskers extending to the most extreme data points. (C) ΔVm obtained by subtracting the example traces in (A) after removal of spikes. (D) Median ΔVm during RF + natural surround stimulation (green) was significantly more negative than during RF + phase-randomized surround stimulation (magenta) (arrows denote population medians, p = 0.027, Wilcoxon sign-rank test). Firing rate suppression was strongly correlated with the median ΔVm (r = 0.37, p = 0.016). (E) Average ΔVm (±SEM) as a function of the Vm_RF (bin size 5 mV). ΔVm values in each bin were averaged after normalizing to the spike threshold for each cell. (F) Example recording from a L2/3 neuron in immature V1 (postnatal day 16) during presentation of the same movie sequence confined to the RF (blue) or when costimulating the surround with natural (green) or phase-randomized (magenta) movie. (G) ΔVm obtained by subtracting the example traces in (F) after removal of spikes. (H) The median Vm of immature V1 neurons (n = 18) during stimulation of the RF (blue), RF + natural surround (green) and RF + phase-randomized surround (magenta) was significantly different (RF, –60.1 mV; RF + natural surround, –59.6 mV; RF + phase-randomized surround, –59.1 mV; p = 0.017; Friedman’s test). (I) The median ΔVm during RF + natural surround stimulation (green) and during RF + phase-randomized surround stimulation (magenta) was not significantly different (population medians indicated by arrows, p = 0.6, Wilcoxon sign-rank test). Firing rate suppression was not correlated with the mean ΔVm (r = 0.27, p = 0.11). (J) Average ΔVm as a function of the Vm_RF (bin size 5 mV). ΔVm values in each bin were averaged after normalizing to the spike threshold for each cell in immature mice.

Figure 4

GABAergic Inhibition Contributes to Dependency of ΔVm on Vm_RF (A) Example recording with elevated [Cl⁻] of the internal solution from a V1 neuron in a mature mouse during presentation of the same movie sequence confined to the RF (blue) or during costimulation of the surround with natural (green) or phase-randomized (magenta) movies. Lower panel shows the ΔVm for the two surround conditions. (B) Elevated [Cl⁻] (open circles, n = 7) causes a rightward shift in the relationship between ΔVm and Vm_RF over the entire data range for both RF + natural (green) and RF + phase-randomized surround (magenta) conditions. See text for a detailed description. Data with normal [Cl⁻] are replotted from Figure 3E. (C) Example targeted whole-cell recording from a parvalbumin (PV)-positive interneuron in V1 from a mature PV-GFP mouse during stimulation of the RF (left panel, blue trace), RF + natural surround (middle panel, green trace), and RF + phase-randomized surround (right panel, magenta trace). Conventions as in Figure 2A. Scale bar, 20 mV. The black trace shows the action potential waveform of the example cell. Scale bar, 1 ms. (D) Example targeted whole-cell recording from a somatostatin (SOM) positive interneuron in V1 from a mature GIN mouse. Conventions as in (C). (E) Firing rates of individual parvalbumin (PV, n = 18) and somatostatin (SOM, n = 18) interneurons during stimulation of the RF center (blue), RF + natural surround (green) or RF + phase-randomized surround (magenta) in mature mice. Surround stimulation resulted in slight but significant decreases in firing rates (p values of paired comparisons given in the panel, Wilcoxon signed rank test). Conventions as in Figure 2. (F) Comparison of relative firing rates (% of firing rate during RF stimulation) of putative pyramidal cells (Pyr, n = 21), PV (n = 18), and SOM (n = 18) interneurons during costimulation of the surround with either RF + natural (green, left panel) or RF + phase-randomized (magenta, right panel) movies. PV and SOM neurons were significantly less suppressed during either surround condition compared to Pyr cells (p values of comparisons given in the panel, Mann-Whitney U test).

Figure 5

Precisely Timed Hyperpolarization Prior to RF Spiking Events Mediates Selective Surround Suppression (A) ΔVm as a function of the time before a spike during RF stimulation in mature mice. The mean ΔVm (±SEM) is plotted for the corresponding times (bin = 50 ms) during RF + natural (green) and RF + phase-randomized surround (magenta) conditions. ΔVm was significantly different between the surround conditions (F_interaction = 143, p < 0.00001, two-way ANOVA). (B) ΔVm as a function of the time before a spike during RF stimulation in immature mice. ΔVm was significantly different between the surround conditions (F_interaction = 103, p < 0.00001, two-way ANOVA). (C) Quantification of differences in ΔVm between RF + natural and RF + phase-randomized surround conditions in mature (solid lines) and immature (dashed lines) mice. Differences in ΔVm between surround conditions were consistently larger for mature mice, both when analyzed relative to Vm_RF (black, compare Figures 3E and 3J) and relative to time of RF spike (yellow, compare A and B). Note that only in mature mice differences in ΔVm between RF + natural and RF + phase-randomized surround conditions were large at times prior RF spiking (yellow solid line, p = 0.0004, t test) and increased with increasing depolarization of Vm_RF (black solid line, p = 0.006, t test). Thus, these differences in ΔVm might underlie the increased firing rate suppression during RF + natural surround stimulation. (D–G) Same conventions as in Figure 3B. (D) In mature V1, natural surround stimulation reduced the likelihood for large-amplitude synaptic events to trigger a spike in mature V1 (RF versus RF + natural surround, p = 1 × 10⁻⁵; RF + natural surround versus RF + phase-randomized surround, p = 0.01; Mann-Whitney U test). (E) In immature V1, the likelihood for large-amplitude synaptic events to trigger a spike was not significantly different across conditions (p = 0.19, Kruskal-Wallis test across all three conditions). (F) In mature V1, large-amplitude, depolarizing synaptic events were similarly frequent across stimulation conditions (p = 0.34; Kruskal-Wallis test across all three conditions). (G) In immature V1, large-amplitude, depolarizing synaptic events were similarly frequent across stimulation conditions (p = 0.59; Kruskal-Wallis test across all three conditions).

Figure 6

Dark-Rearing Prevents the Emergence of Preference for Natural Surround Stimuli (A) Responses from an example neuron in dark-reared, mature V1 during stimulation of the RF (blue trace), RF + natural surround (green trace), and RF + phase-randomized surround (magenta trace). (B) Analysis of spiking responses of neurons recorded in dark-reared mice. Same conventions as in Figures 2A and 2B. (C–F) Analysis of subthreshold responses of V1 neurons recorded in dark-reared mice. Same conventions as in Figures 3A–3D. (D) The median membrane depolarisation of V1 neurons in dark-reared mice (n = 19) during stimulation of RF (blue), RF + natural surround (green), or RF + phase-randomized surround (magenta) was not significantly different (RF, −60.5 mV; RF + natural surround, −60.8 mV; RF + phase-randomized surround, –59.7 mV; p = 0.33; Friedman’s test). (F) ΔVm during RF + natural surround (green) and during RF + phase-randomized surround (magenta) stimulation was not significantly different (medians indicated by arrows, p = 0.21, Wilcoxon sign-rank-test). Firing rate suppression was correlated with the median ΔVm (r = –0.54, p = 0.0005). (G) ΔVm as a function of the mean Vm depolarization during RF stimulation (bin size 5 mV) normalized to the spike threshold for each cell. ΔVm during RF + natural surround (green) and during RF + phase-randomized surround (magenta) stimulation were similar. (H) ΔVm as a function of the time before the firing of a spike during RF stimulation in dark-reared mice. ΔVm during RF + natural (green) and RF + phase-randomized (magenta) surround conditions were highly similar. (I) In dark-reared, mature V1, the likelihood for large-amplitude events to trigger a spike was not significantly different across conditions (p = 0.18, Kruskal-Wallis test across all three conditions). (J) In dark-reared, mature V1, large-amplitude, depolarizing synaptic events were similarly frequent across stimulation conditions (p = 0.82; Kruskal-Wallis test across all three conditions).