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1. Adaptation optimizes sensory encoding for future stimuli

   https://doi.org/10.1371/journal.pcbi.1012746  

   Mao, Jiang; Rothkopf, Constantin A; Stocker, Alan A (January 2025, PLOS Computational Biology)

   Graham, Lyle J (Ed.)

   Sensory neurons continually adapt their response characteristics according to recent stimulus history. However, it is unclear how such a reactive process can benefit the organism. Here, we test the hypothesis that adaptation actually acts proactively in the sense that it optimally adjusts sensory encoding for future stimuli. We first quantified human subjects’ ability to discriminate visual orientation under different adaptation conditions. Using an information theoretic analysis, we found that adaptation leads to a reallocation of coding resources such that encoding accuracy peaks at the mean orientation of the adaptor while total coding capacity remains constant. We then asked whether this characteristic change in encoding accuracy is predicted by the temporal statistics of natural visual input. Analyzing the retinal input of freely behaving human subjects showed that the distribution of local visual orientations in the retinal input stream indeed peaks at the mean orientation of the preceding input history (i.e., the adaptor). We further tested our hypothesis by analyzing the internal sensory representations of a recurrent neural network trained to predict the next frame of natural scene videos (PredNet). Simulating our human adaptation experiment with PredNet, we found that the network exhibited the same change in encoding accuracy as observed in human subjects. Taken together, our results suggest that adaptation-induced changes in encoding accuracy prepare the visual system for future stimuli. 

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2. Encoding manifolds constructed from grating responses organize responses to natural scenes in cortical visual areas

   https://doi.org/10.1101/2024.10.24.620089  

   Dyballa, Luciano; Field, Greg D; Stryker, Michael P; Zucker, Steven W (October 2024, bioRxiv.org)

   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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3. Natural scene sampling reveals reliable coarse-scale orientation tuning in human V1

   https://doi.org/10.1038/s41467-022-34134-7  

   Roth, Zvi N.; Kay, Kendrick; Merriam, Elisha P. (December 2022, Nature Communications)

   Abstract Orientation selectivity in primate visual cortex is organized into cortical columns. Since cortical columns are at a finer spatial scale than the sampling resolution of standard BOLD fMRI measurements, analysis approaches have been proposed to peer past these spatial resolution limitations. It was recently found that these methods are predominantly sensitive to stimulus vignetting - a form of selectivity arising from an interaction of the oriented stimulus with the aperture edge. Beyond vignetting, it is not clear whether orientation-selective neural responses are detectable in BOLD measurements. Here, we leverage a dataset of visual cortical responses measured using high-field 7T fMRI. Fitting these responses using image-computable models, we compensate for vignetting and nonetheless find reliable tuning for orientation. Results further reveal a coarse-scale map of orientation preference that may constitute the neural basis for known perceptual anisotropies. These findings settle a long-standing debate in human neuroscience, and provide insights into functional organization principles of visual cortex. 

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4. Cortical layer–specific critical dynamics triggering perception

   https://doi.org/10.1126/science.aaw5202  

   Marshel, James H.; Kim, Yoon Seok; Machado, Timothy A.; Quirin, Sean; Benson, Brandon; Kadmon, Jonathan; Raja, Cephra; Chibukhchyan, Adelaida; Ramakrishnan, Charu; Inoue, Masatoshi; et al (August 2019, Science)

   Perceptual experiences may arise from neuronal activity patterns in mammalian neocortex. We probed mouse neocortex during visual discrimination using a red-shifted channelrhodopsin (ChRmine, discovered through structure-guided genome mining) alongside multiplexed multiphoton-holography (MultiSLM), achieving control of individually specified neurons spanning large cortical volumes with millisecond precision. Stimulating a critical number of stimulus-orientation-selective neurons drove widespread recruitment of functionally related neurons, a process enhanced by (but not requiring) orientation-discrimination task learning. Optogenetic targeting of orientation-selective ensembles elicited correct behavioral discrimination. Cortical layer–specific dynamics were apparent, as emergent neuronal activity asymmetrically propagated from layer 2/3 to layer 5, and smaller layer 5 ensembles were as effective as larger layer 2/3 ensembles in eliciting orientation discrimination behavior. Population dynamics emerging after optogenetic stimulation both correctly predicted behavior and resembled natural internal representations of visual stimuli at cellular resolution over volumes of cortex. 

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5. Radial Bias Alters Perceived Object Orientation

   https://doi.org/10.1177/09567976221110243  

   Menceloglu, Melisa; Nakayama, Ken; Song, Joo-Hyun (October 2022, Psychological Science)

   Orientation sensitivity is a fundamental property of the visual system, but not all orientations are created equal. For instance, radially oriented stimuli, aligned with a line intersecting the center of gaze, produce greater activity throughout the visual cortex and are associated with greater perceptual sensitivity compared with other orientations. Here, we discuss a robust visual illusion that is likely related to this preference. Using a continuous response measure, participants ( N = 36 adults) indicated the gap position in a peripheral Landolt C placed in one of eight orientations and eight locations along four meridians (vertical, horizontal, 45°, 135°). The error distributions revealed that the perceived gap was attracted toward the radial axis. For instance, the gap in a regular C would often be wrongly perceived as tilted 45° corresponding to the oblique meridian where it was placed. These findings demonstrate an unsuspected early-vision influence on the perceived orientation of an object. 

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