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Principles underlying sensory map topography in primary visual cortex

Abstract

The primary visual cortex contains a detailed map of the visual scene, which is represented according to multiple stimulus dimensions including spatial location, ocular dominance and stimulus orientation. The maps for spatial location and ocular dominance arise from the spatial arrangement of thalamic afferent axons in the cortex. However, the origins of the other maps remain unclear. Here we show that the cortical maps for orientation, direction and retinal disparity in the cat (Felis catus) are all strongly related to the organization of the map for spatial location of light (ON) and dark (OFF) stimuli, an organization that we show is OFF-dominated, OFF-centric and runs orthogonal to ocular dominance columns. Because this ON–OFF organization originates from the clustering of ON and OFF thalamic afferents in the visual cortex, we conclude that all main features of visual cortical topography, including orientation, direction and retinal disparity, follow a common organizing principle that arranges thalamic axons with similar retinotopy and ON–OFF polarity in neighbouring cortical regions.

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Figure 1: Recording from the horizontal dimension of visual cortex.
Figure 2: Topographic organization of ON and OFF cortical domains.
Figure 3: Cortical topographic relationships between ON–OFF, retinotopy and orientation preference.
Figure 4: Changes in retinotopy explain changes in orientation and direction preference throughout the cortex.
Figure 5: Principles underlying sensory map topography in primary visual cortex.

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Acknowledgements

We thank R. Lashgari, S. Komban, M. Jansen, C. Pons and E. Koch for helping collect data in some experiments; H. Swadlow, Q. Zaidi and R. Mazade for comments on the manuscript; and A. Movshon for lending some experimental equipment. This work was supported by the US National Institutes of Health (EY005253, J.M.A.), a DFG Research Fellowship (KR 4062/1-1, J.K.) and Humboldt-Universität zu Berlin in the framework of the Excellence Initiative of the BMBF and DFG (J.K.).

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J.K., J.J., Y.W. and J.M.A. conducted the experiments and data analysis. J.K., J.J. and J.M.A. wrote the manuscript.

Corresponding author

Correspondence to Jose M. Alonso.

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The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 Measurements of ON–OFF responses and ocular dominance columns.

a, ON and OFF receptive fields were mapped with light (ON) and dark (OFF) sparse noise and calculated from the response to the stimulus onset (grey shaded area). b, Horizontal penetrations that ran for more than 1.2 mm through a monocular band were assumed to be nearly parallel to ocular dominance columns (top) and those that alternated between monocular responses for left and right eyes were assumed to be nearly orthogonal to ocular dominance columns (bottom). Receptive fields normalized for ocular dominance. Icons on the left illustrate ocular dominance columns for contralateral (C) and ipsilateral (I) eyes (arrow illustrates horizontal penetration). Each receptive field box has a side of 27°.

Extended Data Figure 2 ON–OFF domains are matched across eyes.

a, Integrating the ON–OFF receptive fields over 0.7 mm of horizontal cortical distance reveals ON and OFF receptive field subregions that are segregated in visual space and well matched between eyes. Notice the excellent binocular match of the receptive field subregions measured with light spots (left, two subregions displaced vertically in both eyes), and dark spots (middle left, one central subregion in both eyes). The ON–OFF receptive field difference also shows an excellent binocular match (middle right), so the ON–OFF segregation can still be seen after combining the receptive fields of the two eyes (right). b, Integrating the ON–OFF receptive fields over a much longer distance (1.6 mm of cortex, different horizontal penetration) still reveals separate receptive field subregions with excellent binocular match. The 1.6-mm-average receptive fields of the left and right eyes have both two ON subregions that are displaced diagonally and retinotopically matched (left). They also have two OFF subregions that are also displaced diagonally and retinotopically matched between the two eyes (middle left). A hint of the ON subregions can still be seen in the ON–OFF receptive field difference (middle right) and receptive field of both eyes combined (right), even if the receptive fields were averaged over 1.6 mm of cortex. Each square box framing a receptive field has a side of 16.2°.

Extended Data Figure 3 The OFF pathway might also anchor retinotopy in the primary visual cortex of the macaque.

ON–OFF retinotopy measured along 0.3 mm of horizontal cortical distance in macaque primary visual cortex (n = 1 monkey). As in the cat, changes in OFF retinotopy are more restricted than changes in ON retinotopy in the receptive fields of both eyes. Panels labelled ‘average’ show receptive fields averaged across cortical distance separately for each eye and both eyes. Plots labelled ‘retinotopy’ show the retinotopy of the receptive field pixel that generated the strongest ON (red) or OFF (blue) response, shown separately for each eye and both eyes. Each square box framing a receptive field has a side of 12°.

Extended Data Figure 4 Periodic changes in orientation preference.

a, Colour map showing normalized frequency of orientation difference between paired recordings measured at different cortical distances within a single horizontal penetration (same as Fig. 3k left). b, Difference in orientation preference between all possible paired recordings measured within the same horizontal penetration as in a (n = 496 paired comparisons, n = 1 animal). c, Same as a but for multiple recording sites obtained from multiple penetrations (n = 20,672 paired comparisons, n = 36 animals).

Extended Data Figure 5 Additional examples of horizontal recordings showing a correlation between changes in ON–OFF retinotopy and orientation preference.

a, Horizontal recording through 0.9 mm of cortex. From top to bottom, the first three panel rows show series of OFF, ON and ON–OFF receptive fields (left) and receptive fields averaged across horizontal cortical distance (right). The bottom row shows the orientation or direction tuning (left) and the retinotopy (Retinot.) of the strongest response within each receptive field (right; ON, red; OFF, blue). The small circles in the orientation plots illustrate the preferred orientation predicted from the ON–OFF receptive field. b, c, Horizontal recordings through binocular regions of length 0.5 mm (b) and 0.7 mm (c). Notice the accurate binocular match in ON–OFF retinotopy between the two eyes and also the striking binocular similarity in orientation preference, direction preference and orientation and direction selectivity. Each receptive field box has a side of 27° (a), 23° (b) or 23.6° (c).

Extended Data Figure 6 Example of a horizontal penetration in which we recorded from several single neurons separated from each other by 0.1 mm.

Format is similar to Fig. 4a and Extended Data Fig. 5a. The only difference is that the receptive fields and orientation plots were obtained from single neurons instead of multiunit activity. The last row shows spike waveforms from each single neuron (average and s.d.). Each square box framing a receptive field has a side of 23°.

Extended Data Figure 7 Example of a cortical region in which OFF retinotopy rotates around ON retinotopy.

The figure shows a series of receptive fields mapped with dark (OFF) and light stimuli (ON) and the ON–OFF receptive field difference. The last receptive field on the right for each row shows the average of all receptive fields across 0.8 mm of cortical distance. The plot on the right shows the retinotopy of the ON (red) and OFF (blue) receptive fields. Cortical regions where OFF retinotopy rotated around ON retinotopy were more difficult to find than regions where ON retinotopy rotated around OFF retinotopy. To estimate the relative frequency of ON and OFF retinotopy rotations, we measured the distance between the retinotopic centre of mass of single horizontal penetrations for each ON or OFF receptive field (81 penetrations with receptive field measurements from at least five recording sites per penetration). We then calculated a ratio of the average distances, as (ON − OFF)/(ON + OFF), and used a ratio of 0.5 as an arbitrary threshold to classify a penetration as OFF-anchored (ON rotates around OFF) or ON-anchored (OFF rotates around ON). Based on this criterion, there were 3.75 more OFF-anchored than ON-anchored penetrations (15 versus 4 penetrations, respectively; n = 17 animals). Each square box framing a receptive field has a side of 19.4°.

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Kremkow, J., Jin, J., Wang, Y. et al. Principles underlying sensory map topography in primary visual cortex. Nature 533, 52–57 (2016). https://doi.org/10.1038/nature17936

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