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. 2020 Dec 1;24(1):101882.
doi: 10.1016/j.isci.2020.101882. eCollection 2021 Jan 22.

Spatial clustering of orientation preference in primary visual cortex of the large rodent agouti

Dardo N Ferreiro  1 , Sergio A Conde-Ocazionez  1   2 , João H N Patriota  1 , Luã C Souza  1 , Moacir F Oliveira  3 , Fred Wolf  4   5   6   7 , Kerstin E Schmidt  1
Affiliations

Spatial clustering of orientation preference in primary visual cortex of the large rodent agouti

Dardo N Ferreiro et al. iScience. .

Abstract

All rodents investigated so far possess orientation-selective neurons in the primary visual cortex (V1) but - in contrast to carnivores and primates - no evidence of periodic maps with pinwheel-like structures. Theoretical studies debating whether phylogeny or universal principles determine development of pinwheels point to V1 size as a critical constraint. Thus, we set out to study maps of agouti, a big diurnal rodent with a V1 size comparable to cats'. In electrophysiology, we detected interspersed orientation and direction-selective neurons with a bias for horizontal contours, corroborated by homogeneous activation in optical imaging. Compatible with spatial clustering at short distance, nearby neurons tended to exhibit similar orientation preference. Our results argue against V1 size as a key parameter in determining the presence of periodic orientation maps. They are consistent with a phylogenetic influence on the map layout and development, potentially reflecting distinct retinal traits or interspecies differences in cortical circuitry.

Keywords: Biological Sciences; Cellular Neuroscience; Developmental Neuroscience; Neuroscience; Sensory Neuroscience.

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Conflict of interest statement

The authors declare no competing interests.

Figures

None
Graphical abstract
Figure 1
Figure 1
Receptive field size in agoutis and cats (A) Sketch of the electrophysiologically sampled area in agouti V1. (B) aCRF mapping examples from agouti V1 at three different eccentricities (E) along the visual streak (elevation less than 5°) and two fields from cat area 18. Scale bars represent 2°. (C) Receptive field size as a function of elevation. Data from 5 cats and 11 agoutis: 125 multi-units for cat A18, 82 for cat A17, and 401 for agouti V1. (D) Receptive field size as a function of eccentricity. More lateral part of the visual streak in agouti (light violet shade in A, 30–120 deg). Agouti aCRFs do not increase at large eccentricities (≥90 deg). (E) Receptive field size as a function of eccentricity. Zoom into the central visual field <25 deg (dark violet shade in A). (F) Cumulative distributions of aCRF size for agouti V1, cat area 17, and 18. Note that agouti V1 neurons tend to have aCRFs of similar size as cat area 17. SL, lateral sulcus; HM, horizontal meridian; VM, vertical meridian. Cortical coordinates: M, medial; L, lateral; A anterior; P, posterior; adapted from Picanço-Diniz et al. (1991).
Figure 2
Figure 2
Orientation selectivity in primary visual cortex of agouti and cat (A and B) Examples of isolated units for agouti (A) and for cat area 18 (B) stimulated at 0.08 cpd. Dashed lines indicate double Gaussian fits to the mean firing rates. Light gray lines indicate pre-stimulus firing rate. Error bars, standard deviation. Note that here agouti and cat units prefer the horizontal direction of movement and have thus vertical orientation preference. (C) Distributions of orientation selectivity indices (OSIs) in both species. Agouti selectivity indices (n = 349) are significantly lower than indices for cat area 18 (n = 97, Mann-Whitney U, p < 0.0001) and cat area 17 (n = 22, Mann-Whitney U, p < 0.0001). (D) Distributions of direction selectivity indices (DSIs) in both species. For (C and D), cat distributions of OSI and DSI are divided into Brodmann areas 17 (gray) and 18 (black). Only indices of neurons that passed both the spike-dependent threshold and a static threshold of 0.1 are depicted. Error bars are SEM (standard error of the mean).
Figure 3
Figure 3
Agouti V1 neurons are selective for spatial frequency (A) Population mean firing rate of all orientation-selective agouti single units evoked at different spatial frequencies (black line) and during the pre-stimulus period (gray line). (B) Counts of neurons that evoked maximum mean firing rate at that SF. (C) Spatial frequency tuning curve example. Mean maximum firing rate obtained with an optimal grating at each SF. Error bars, standard deviation. (D) Polar plot of the example agouti single unit (upper) and of a cat area 17 single unit (lower) at five different SFs. (E) Orientation selectivity index of the two neurons of D at different SFs. Note that the agouti neuron fires most at 0.08 and exhibits highest orientation selectivity at 0.16 cpd. For comparison, the cat area 17 neuron remains selective at high SFs. (F) Spatial frequency selectivity of the mean orientation selectivity indices for agouti, cat A17, and cat A18 in the same scale. (G) Same as (F) zooming in on the agouti curve. Note that agoutis show small orientation selectivity indices, with optimal OSI tuning at 0.32 cpd in the visual area investigated. Only indices of neurons that passed both the OSI spike-dependent threshold and a static threshold of 0.1 were included (n = 349). Error bars are SEM (standard error of the mean), except for (C)
Figure 4
Figure 4
Sharpness of orientation and direction tuning curves in agoutis and cats (A–C) (A) Examples of Gaussian fits of orientation tuning curves elicited at 0.32 cpd for one agouti and one cat single unit. Mean population half-width at half-height (HWHH) of orientation (B) and direction (C) selectivity tuning curves. Firing rates for each stimulation orientation/direction were normalized for every neuron with a selectivity index >0.2. A single peak Gaussian function was fitted to each of the normalized firing rates for orientation/direction, for each spatial frequency. Note that tuning curves of cat area 18 neurons have much lower HWHH values than agouti, especially for direction selectivity. Data from 2 cats and 9 agoutis. Error bars: SEM. Stars indicate significant differences between agoutis and cats (Wilcoxon rank-sum test; p < 0.001; n = agouti units, cat units)
Figure 5
Figure 5
Spatial layout: tuning difference between cell pairs as a function of distance Mean pairwise angle difference (A) and pairwise Pearson correlation of firing rates to stimulation angle (B) as a function of horizontal cortical distance for cat A18 and agouti V1. For each cell, only the orientation preference at the spatial frequency, which elicited the highest OSI, was considered. Gray dotted lines represent the calculation for the shuffled data. Asterisks depict significant differences between the correlations obtained for recorded and shuffled data. Significance criterion: Mann-Whitney p < 0.001 (Bonferroni correction for 10 multiple comparisons) for the pairwise comparison of the data points and the shuffled data. Data from 2 cats and 5 agoutis. For raw p values, see Tables S1 and S2, for number of data points, see Table S3. Note that agouti neuron similarity is only different than chance for neurons that lie close to each other. Error bars: SEM.
Figure 6
Figure 6
Orientation preference distribution across vertical and horizontal dimensions (A) Polar plots of example single units recorded from a vertical double shank probe at 0.08 cpd. Waveforms from separated units are color coded. Note that orientation preference in agoutis is relatively stable along the vertical axis. Representatively, units on both shanks prefer orientations varying around the horizontal axis. (B) Angle differences are higher across (gray filled circle, n = 121) than along shanks (empty circle, n = 145; Mann-Whitney-U, p < 0.005) and between units separated from the same site (black filled circle, n = 24; Mann-Whitney-U, p < 0.0001). Pairwise differences (C) Pairwise comparisons of orientation preference across all electrodes of each device. Median and interquartile ranges are depicted by circles and lines, respectively. Empty and filled circles depict pairwise comparisons between single units from Neuronexus probes or electrode arrays, respectively. Probe electrode sample from a vertical cylinder (A, orthogonal to cortical surface). Array sample from horizontal planes (parallel to cortical surface). Angle difference (top) and tuning similarity (bottom). Both measures indicate a greater similarity between neurons arranged vertically. ∗ depicts p < 0.0001 (Mann-Whitney U test, for raw p values see Tables S4 and S5). Probe electrode data from 3 agoutis. Array electrode data from 5 agoutis. (D) Percentage of agouti single units with different orientation preferences above selectivity threshold categorized in 12 groups of ±7.5 deg at 0.16 cpd and 2 Hz (n = 85 neurons). Strikingly, in the overall sample, the horizontal orientation preference predominates.
Figure 7
Figure 7
Neuronal (in)stability of preferred angles across different spatial frequencies (A) Orientation preference and selectivity index at different SFs for three example units from agouti (red, blue, gray squares) and one from cat area 17 (green circles). Note that agouti orientation preference varies much more than the cat's. (B) Overall cumulative distribution of angle range (top) and circular variance (bottom) for all cells. (C) Mean of the pairwise within-cell comparisons. For each pair of orientation selective responses (to different spatial frequencies) crossing the selectivity threshold, the difference of preferred angle was computed. The octaves denote the difference in spatial frequencies of the responses being compared (e.g. comparisons between 0.04-0.08 cpd and 0.32–0.64 cpd are both one octave apart). (D) Zoom into the agouti curve shown in (C). Note that orientation difference increases with SF difference. Error bars: SEM.
Figure 8
Figure 8
Intrinsic signal maps of retinotopy Left, upper image: color overlay on the vessel image of position specific activation with bars of 5 deg width spanning the whole monitor in horizontal (A, 6 positions) or vertical (B, 8 positions, indicated by checker sketches on top) orientation. Lower image: sketch depicting iso-elevation (A) or iso-azimuth lines. Right: single condition maps. (A) The activation starts with 15 deg in the upper visual field activating the lateral-posterior part of the craniotomy migrating to the anterior part. The visual streak extends from red to yellow. (B) A vertical bar positioned at the visual field's midline evokes activity at anterior-lateral part moving to medial. HM, horizontal meridian; VM, vertical meridian. Cortical coordinates: M, medial; L, lateral; A, anterior; P, posterior.
Figure 9
Figure 9
Orientation maps obtained by grating stimulation in agouti primary visual cortex (A) Unfiltered averaged single condition maps after first frame correction. (B) Left, polar (saturation of the color codes for vector strength) map according to the color bar below; blue outline, stimROI; red outline, shiftROI. right: vessel image of the recorded area. Scale bar, 1 mm; cortical coordinates as in Figure 8. (C) Relative count of pixels preferring one of the four angle categories as indicated below in two ROIs, a medial and a more temporal one. Note that preferences for either horizontal or right oblique (recording the left hemisphere) dominate in all animals and ROIs. (D) Mean spatial correlation coefficients between all frames within the stimulated ROI (blue), an ROI shifted in an area not stimulated by that monitor position (red) and on a rubber brain illuminated with red light (green) for C50. Error bars: SEM.
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