We have created encoding manifolds to reveal the overall responses of a brain area to a variety of stimuli. Encoding manifolds organize response properties globally: each point on an encoding manifold is a neuron, and nearby neurons respond similarly to the stimulus ensemble in time. We previously found, using a large stimulus ensemble including optic flows, that encoding manifolds for the retina were highly clustered, with each cluster corresponding to a different ganglion cell type. In contrast, the topology of the V1 manifold was continuous. Now, using responses of individual neurons from the Allen Institute Visual Coding-Neuropixels dataset in the mouse, we infer encoding manifolds for V1 and for five higher cortical visual areas (VISam, VISal, VISpm, VISlm, and VISrl). We show here that the encoding manifold topology computed only from responses to various grating stimuli is also continuous, not only for V1 but also for the higher visual areas, with smooth coordinates spanning it that include, among others, orientation selectivity and firing-rate magnitude. Surprisingly, the encoding manifold for gratings also provides information about natural scene responses. To investigate whether neurons respond more strongly to gratings or natural scenes, we plot the log ratio of natural scene responses to grating responses (mean firing rates) on the encoding manifold. This reveals a global coordinate axis organizing neurons' preferences between these two stimuli. This coordinate is orthogonal (i.e., uncorrelated) to that organizing firing rate magnitudes in VISp. Analyzing layer responses, a preference for gratings is concentrated in layer 6, whereas preference for natural scenes tends to be higher in layers 2/3 and 4. We also find that preference for natural scenes dominates the responses of neurons that prefer low (0.02 cpd) and high (0.32 cpd) spatial frequencies, rather than intermediate ones (0.04 to 0.16 cpd). Conclusion: while gratings seem limited and natural scenes unconstrained, machine learning algorithms can reveal subtle relationships between them beyond linear techniques.
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Large-scale calcium imaging reveals a systematic V4 map for encoding natural scenes
Biological visual systems have evolved to process natural scenes. A full understanding of visual cortical functions requires a comprehensive characterization of how neuronal populations in each visual area encode natural scenes. Here, we utilized widefield calcium imaging to record V4 cortical response to tens of thousands of natural images in male macaques. Using this large dataset, we developed a deep-learning digital twin of V4 that allowed us tomap the natural image preferences of the neural population at 100-μmscale. This detailed map revealed a diverse set of functional domains in V4, each encoding distinct natural image features. We validated these model predictions using additional widefield imaging and single-cell resolution two-photon imaging. Feature attribution analysis revealed that these domains lie along a continuum from preferring spatially localized shape features to preferring spatially dispersed surface features. These results provide insights into the organizing principles that govern natural scene encoding in V4.
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- Award ID(s):
- 1816568
- PAR ID:
- 10536576
- Publisher / Repository:
- Nature
- Date Published:
- Journal Name:
- Nature Communications
- Volume:
- 15
- Issue:
- 1
- ISSN:
- 2041-1723
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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