Variations in photoreceptor throughput to mouse visual cortex and the unique effects on tuning

ABSTRACTVisual input to primary visual cortex (V1) depends on highly adaptive filtering in the retina. In turn, isolation of V1 computations to study cortical circuits requires control over retinal adaption and its corresponding spatio-temporal-chromatic output. Here, we first measure the balance of input to V1 from the three main photoreceptor opsins – M-opsin, S-opsin, and rhodopsin – as a function of light adaption and retinotopy. Results show that V1 is rod-mediated in common laboratory settings, yet cone-mediated in natural daylight, as evidenced by exclusive sensitivity to UV wavelengths via cone S-opsin in the upper visual field. Next, we show that cone-mediated V1 responds to 2.5-fold higher temporal frequencies than rod-mediated V1. Furthermore, cone-mediated V1 has smaller RFs, yet similar spatial frequency tuning. V1 responses in rod-deficient (Gnat1−/−) mice confirm that the effects are due to differences in photoreceptor contribution. This study provides foundation for using mouse V1 to study cortical circuits.

Local organization of spatial frequency tuning dynamics in the cat visual areas 17 and 18

In cat area 17/18, we found that a local pool of neurons with similar spatial frequency (SF) tunings shows diverse but organized dynamics. Our results suggest that, in the presence of organized tuning diversity within an SF domain, the cortical SF organization remains stable over response time in these areas. Laminar analysis suggests that intracortical mechanisms contribute to generating SF dynamics inside the input layer but do not further shape it outside this layer.

Effects of Experience on Spatial Frequency Tuning in the Visual System: Behavioral, Visuocortical, and Alpha-band Responses

Using electrophysiology and a classic fear conditioning paradigm, this work examined adaptive visuocortical changes in spatial frequency tuning in a sample of 50 undergraduate students. High-density EEG was recorded while participants viewed 400 total trials of individually presented Gabor patches of 10 different spatial frequencies. Patches were flickered to produce sweep steady-state visual evoked potentials (ssVEPs) at a temporal frequency of 13.33 Hz, with stimulus contrast ramping up from 0% to 41% Michelson over the course of each 2800-msec trial. During the final 200 trials, a selected range of Gabor stimuli (either the lowest or highest spatial frequencies, manipulated between participants) were paired with an aversive 90-dB white noise auditory stimulus. Changes in spatial frequency tuning from before to after conditioning for paired and unpaired gratings were evaluated at the behavioral and electrophysiological level. Specifically, ssVEP amplitude changes were evaluated for lateral inhibition and generalization trends, whereas change in alpha band (8–12 Hz) activity was tested for a generalization trend across spatial frequencies, using permutation-controlled F contrasts. Overall time courses of the sweep ssVEP amplitude envelope and alpha-band power were orthogonal, and ssVEPs proved insensitive to spatial frequency conditioning. Alpha reduction (blocking) was most pronounced when viewing fear-conditioned spatial frequencies, with blocking decreasing along the gradient of spatial frequencies preceding conditioned frequencies, indicating generalization across spatial frequencies. Results suggest that alpha power reduction—conceptually linked to engagement of attention and alertness/arousal mechanisms—to fear-conditioned stimuli operates independently of low-level spatial frequency processing (indexed by ssVEPs) in primary visual cortex.

Population spatial frequency tuning in human early visual cortex

Neurons within early visual cortex are selective for basic image statistics, including spatial frequency. However, these neurons are thought to act as band-pass filters, with the window of spatial frequency sensitivity varying across the visual field and across visual areas. Although a handful of previous functional (f)MRI studies have examined human spatial frequency sensitivity using conventional designs and analysis methods, these measurements are time consuming and fail to capture the precision of spatial frequency tuning (bandwidth). In this study, we introduce a model-driven approach to fMRI analyses that allows for fast and efficient estimation of population spatial frequency tuning (pSFT) for individual voxels. Blood oxygen level-dependent (BOLD) responses within early visual cortex were acquired while subjects viewed a series of full-field stimuli that swept through a large range of spatial frequency content. Each stimulus was generated by band-pass filtering white noise with a central frequency that changed periodically between a minimum of 0.5 cycles/degree (cpd) and a maximum of 12 cpd. To estimate the underlying frequency tuning of each voxel, we assumed a log-Gaussian pSFT and optimized the parameters of this function by comparing our model output against the measured BOLD time series. Consistent with previous studies, our results show that an increase in eccentricity within each visual area is accompanied by a drop in the peak spatial frequency of the pSFT. Moreover, we found that pSFT bandwidth depends on eccentricity and is correlated with the pSFT peak; populations with lower peaks possess broader bandwidths in logarithmic scale, whereas in linear scale this relationship is reversed. NEW & NOTEWORTHY Spatial frequency selectivity is a hallmark property of early visuocortical neurons, and mapping these sensitivities gives us crucial insight into the hierarchical organization of information within visual areas. Due to technical obstacles, we lack a comprehensive picture of the properties of this sensitivity in humans. Here, we introduce a new method, coined population spatial frequency tuning mapping, which circumvents the limitations of the conventional neuroimaging methods, yielding a fuller visuocortical map of spatial frequency sensitivity.

Experience-dependent development of visual sensitivity in larval zebrafish

The zebrafish (Danio rerio) is a popular vertebrate model for studying visual development, especially at the larval stage. For many vertebrates, post-natal visual experience is essential to fine-tune visual development, but it is unknown how experience shapes larval zebrafish vision. Zebrafish swim with a moving texture; in the wild, this innate optomotor response (OMR) stabilises larvae in moving water, but it can be exploited in the laboratory to assess zebrafish visual function. Here, we compared spatial-frequency tuning inferred from OMR between visually naïve and experienced larvae from 5 to 7 days post-fertilisation. We also examined development of synaptic connections between neurons by quantifying post-synaptic density 95 (PSD-95) in larval retinae. PSD-95 is closely associated with N-methyl-D-aspartate (NMDA) receptors, the neurotransmitter-receptor proteins underlying experience-dependent visual development. We found that rather than following an experience-independent genetic programme, developmental changes in visual spatial-frequency tuning at the larval stage required visual experience. Exposure to motion evoking OMR yielded no greater improvement than exposure to static form, suggesting that increased sensitivity as indexed by OMR was driven not by motor practice but by visual experience itself. PSD-95 density varied with visual sensitivity, suggesting that experience may have up-regulated clustering of PSD-95 for synaptic maturation in visual development.