Abstract
Images are processed in the primary visual cortex by neurons that encode different stimulus orientations and spatial phases. In primates and carnivores, neighboring cortical neurons share similar orientation preferences, but spatial phases were thought to be randomly distributed. We discovered a columnar organization for spatial phase in cats that shares similarities with the columnar organization for orientation. For both orientation and phase, the mean difference across vertically aligned neurons was less than one-fourth of a cycle. Cortical neurons showed threefold more diversity in phase than orientation preference; however, the average phase of local neuronal populations was similar through the depth of layer 4. We conclude that columnar organization for visual space is not only defined by the spatial location of the stimulus, but also by absolute phase. Taken together with previous findings, our results suggest that this phase-visuotopy is responsible for the emergence of orientation maps.
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Acknowledgements
We are grateful to G. DeAngelis, D. Ringach, K. Miller, B. Backus and S. Bloomfield for their valuable suggestions on improving the manuscript. This work was supported by the US National Institutes of Health (EY005253, J.M.A.) and a DFG Research Fellowship (KR 4062/1-1, J.K.).
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Y.W., J.J., J.K., R.L., S.J.K. and J.M.A. conducted the experiments and data analysis. Y.W., J.J. and J.M.A. wrote the manuscript.
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Integrated supplementary information
Supplementary Figure 1 Contrast polarity of single layer 4 neurons.
Same as figure 3 but for single neurons.
Supplementary Figure 2 The population receptive of thalamic afferents making monosynaptic connection in an orientation column biases the cortical population towards a specific spatial phase and preferred orientation.
a. Receptive fields of afferents from the Lateral Geniculate Nucleus (LGN) making monosynaptic connection with the same cortical orientation domain (data taken from ref. 7 ON: red, OFF: blue). b. The population average receptive field calculated by ON-OFF subtraction resembles a cortical simple receptive field with a specific orientation (horizontal) and a specific spatial phase (ON subregion flanked by OFF subregions). Because the LGN afferents spread through the depth of cortical layer 4 and make connections with multiple cortical neurons, we predicted that the receptive field phase of the cortical multiunit activity should remain constant through the depth of cortical layer 4. However, because individual cortical neurons make monosynaptic connections with a subset of the LGN afferents, we predicted that the spatial phase from individual neurons should be more diverse. c. Possible receptive fields of individual cortical neurons obtained by sampling a subset of the receptive fields illustrated in a. Notice that some of these potential individual neurons can have opposite phases (e.g. cells 1 and 3).
Supplementary Figure 3 Comparison of absolute and relative phase diversity in a cortical orientation domain.
a. Absolute phase was estimated from Gabor fits constrained by the average spatial envelope, orientation and spatial frequency of each layer 4 receptive field. Relative phase was estimated from Gabor fits only constrained by the average orientation and spatial frequency (the position of the spatial envelope varied). b. The diversity was smaller for absolute phase than relative phase (0.28 vs. 1.29 rad, P < 0.0001, two-sided Wilcoxon-rank-sum test, n = 26) when selecting the receptive fields that were best fit for absolute phase (R1 > 0.5). Each circle represents phase diversity within a single cortical orientation column (n = 26 columns). c. The diversity was still significantly smaller for absolute phase than relative phase (0.58 vs. 0.93 rad, P = 0.0061, two-sided Wilcoxon-rank-sum test, n = 33) when selecting receptive fields that were best fit for relative phase (R1 > 0.5). Notice that the differences reported in b and c may simply reflect the fact that the fits were more constrained for absolute phase than relative phase. Methods related with this supplementary figure. To directly compare the diversity of absolute and relative phase through the depth of layer 4, we fitted the receptive fields with constrained Gabor functions. First, we fitted all receptive fields with a regular Gabor function and estimated the average spatial frequency and orientation through the depth of layer 4. These values were then used to constrain both the absolute and relative phase of the Gabor fits for all the layer 4 receptive fields. To measure the diversity of absolute phase through the depth of layer 4, we constrained the Gabor fits such that the receptive field envelope, i.e. the 2D Gauss of the Gabor, was the same for all layer 4 receptive fields. The receptive field envelope was calculated by fitting a 2D Gauss to the average population receptive field of all recording sites within the same orientation domain (each receptive field participating in the average was computed in absolute value to avoid any cancelation between overlapping ON and OFF subfields). To measure the diversity of relative phase through the depth of layer 4, we constrained the Gabor fits only by the average spatial frequency and orientation of all receptive fields through the depth of layer 4. The phase diversity was then calculated by averaging the phase differences between receptive fields through the depth of layer 4. We included only those recordings in which we had more than 6 pairs of receptive fields. Because poor fits could make the phase diversity appear artificially larger, we performed two types of analysis. In the first analysis, we compared absolute and relative phase diversity with receptive fields that were well fit (R1 > 0.5) for absolute phase regardless of their goodness of fit for relative phase. In the second analysis, we compared absolute and relative phase diversity with receptive fields that were well fit (R1 > 0.5) for relative phase regardless of their goodness of fit for absolute phase. In the two analyses, the average diversity was significantly smaller for absolute phase than relative phase.
Supplementary Figure 4 In some cortical domains, phase preference at high spatial frequencies remained constant through >1 mm of cortical depth.
a. Multiunit response to a sequence of gratings with different orientations (n = 88), spatial frequencies (n = 41) and phases (n = 4), each presented for 16.6 msec. The panel figure shows a matrix of responses to 11 different spatial frequency ranges (labels in Y axis show mean for each range) recorded at 16 different depths (X axis) in a cortical orientation domain (average orientation difference through the depth of the cortex: 12.1 deg). Each set of histograms within the matrix shows responses to 4 different phases (0, 90, 180 and 270) averaged across all orientations for each combination of spatial frequency and phase. Only responses with good signal to noise are shown (peak response > 3.5 times the baseline). The peak response was defined as the mean rate between 20 to 70 msec after the stimulus onset. The baseline was defined as the mean rate between 70 msec and 150 msec after the stimulus onset and between –50 msec and 20 msec around the stimulus onset. The responses are shown as peri-stimulus time histograms (PSTHs) from –50 msec to 150 msec around the stimulus onset. The PSTHs were calculated with 1-msec bins and smoothed with a boxcar filter of 10 msec. PSTHs in red illustrate the preferred phase response at the highest spatial frequency for each cortical depth. b. Preferred phase responses to the highest spatial frequency measured through the depth of the cortex. With exception of the recordings from one superficial electrode, all recordings had the same phase preference at their highest spatial frequency. c. The number of all possible paired recordings that showed no phase difference in this orientation domain was higher than those that showed a difference (n = 105 vs 15, p < 0.001, Chi square test).
Supplementary Figure 5 Partial segregation of ON and OFF receptive fields from thalamic inputs to a cortical orientation column.
Distribution of distances between ON and OFF receptive fields from geniculate afferents making monosynaptic connections within the same orientation column (re-plotted from Fig. 5c of7, using the diameter of the smaller LGN receptive field center within each pair as a unit). Distances between receptive fields of the same contrast polarity (ON-ON or OFF-OFF) are shown in black and those between receptive fields of different contrast polarity (ON-OFF) in magenta. The two distributions were significantly different (P < 0.001, two-sided Wilcoxon-rank-sum test).
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Wang, Y., Jin, J., Kremkow, J. et al. Columnar organization of spatial phase in visual cortex. Nat Neurosci 18, 97–103 (2015). https://doi.org/10.1038/nn.3878
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DOI: https://doi.org/10.1038/nn.3878
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