Mixed functional microarchitectures for orientation selectivity in the mouse primary visual cortex

Kondo, Satoru; Yoshida, Takashi; Ohki, Kenichi

doi:10.1038/ncomms13210

Cited by 56 publications

(66 citation statements)

References 64 publications

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“…In contrast, we observed pronounced local clustering on the <30 µm scale within each column, in which nearby neurons were more likely to share whisker tuning than predicted by chance, or than expected from the subcolumnar tuning gradient. Thus S1 appears similar to rodent V1, which contains microcolumn-like structures of co-tuned neurons on the 5-40 µm scale (Kondo et al, 2016;Ringach et al, 2016). Such clusters have not yet been found in auditory cortex (Bandyopadhyay et al, 2010;Issa et al, 2014;Panniello et al, 2018).…”

Section: Discussionmentioning

confidence: 88%

“…To determine if local clusters of similarly tuned neurons exist within the salt-andpepper map, as in V1 (Kondo et al, 2016;Ringach et al, 2016), we examined pairwise signal correlations (tuning similarity) for co-columnar neuron pairs. Signal correlation fell off with distance between paired neurons ( Figure 3A, red).…”

Section: L2/3 Pyr Neurons Show Heterogeneous Locally Clustered Tuningmentioning

confidence: 99%

“…This represents high local scatter overlaid on the gradual, average somatotopic gradient across L2/3 of S1 (Clancy et al, 2015;Margolis et al, 2012;Sato et al, 2007). Intermixing has been suggested to be locally random in S1 (Peron et al, 2015;Sato et al, 2007), unlike L2/3 of visual cortex (V1), which contains fine-scale clusters (5-40 µm) of similarly tuned neurons, which may represent columnar primitives (Kondo et al, 2016;Ringach et al, 2016;Rothschild et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

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Whisker map organization in somatosensory cortex of awake, behaving mice

Wang

LeMessurier

Feldman

2019

Preprint

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The whisker map in rodent somatosensory cortex is well characterized under anesthesia, but its organization during awake sensation, when cortical coding can differ strongly, is unknown. Using a novel behavioral task, we measured whisker receptive fields and maps in awake mice with 2-photon calcium imaging in vivo. During a whisker-attentive task, layer 2/3 pyramidal neurons were sharply tuned, with cells tuned to different whiskers intermixed in each column. This salt-and-pepper organization consisted of small clusters of similarly-tuned neurons superimposed on a mean subcolumnar map. Parvalbumin interneurons had broader tuning, and were more homogeneously tuned to the columnar whisker. During a sound-attentive task, whisker tuning of pyramidal cells was less heterogeneous in each column, and firing correlations increased. Thus, behavioral demands modulate fine-scale map structure, and decorrelate the whisker map during whisker-attentive behavior.

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Section: Discussionmentioning

confidence: 88%

Section: L2/3 Pyr Neurons Show Heterogeneous Locally Clustered Tuningmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Whisker map organization in somatosensory cortex of awake, behaving mice

Wang

LeMessurier

Feldman

2019

Preprint

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“…Over the past decade the mouse has become an increasingly popular model system to study vision (1)(2)(3)(4)(5). Many defining characteristics of the murine cortical visual system are analogous to primates (6): They have retinotopically-organized, spatially-restricted receptive fields (4,7,8), a primary visual cortex that is the primary recipient of retinal input via the lateral geniculate nucleus in the thalamus (9), and multiple interconnected higher visual areas (2,10,11).…”

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confidence: 99%

A global map of orientation tuning in mouse visual cortex

Fahey

Muhammad

et al. 2019

Preprint

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In primates and most carnivores, neurons in primary visual cortex are spatially organized by their functional properties. For example, neurons with similar orientation preferences are grouped together in iso-orientation domains that smoothly vary over the cortical sheet. In rodents, on the other hand, neurons with different orientation preferences are thought to be spatially intermingled, a feature which has been termed "salt-and-pepper" organization. The apparent absence of any systematic structure in orientation tuning has been considered a defining feature of the rodent visual system for more than a decade, with broad implications for brain development, visual processing, and comparative neurophysiology. Here, we revisited this question using new techniques for wide-field two-photon calcium imaging that enabled us to collect nearly complete population tuning preferences in layers 2-4 across a large fraction of the mouse visual hierarchy. Examining the orientation tuning of these hundreds of thousands of neurons, we found a global map spanning multiple visual cortical areas in which orientation bias was organized around a single pinwheel centered in V1. This pattern was consistent across animals and cortical depth. The existence of this global organization in rodents has implications for our understanding of visual processing and the principles governing the ontogeny and phylogeny of the visual cortex of mammals. visual cortex | orientation tuning orientation tuning | cortical maps | mouse | V1 | cardinal bias | orientation bias Correspondence: astolias@bcm.edu, reimer@bcm.edu lateromedial (LM)). Scale bar = 250 µm. Fahey et al. | bioRχiv |

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“…The challenge has been greatest in rodents because of the long-held view that cortex lacks columnar organization (Ohki et al, 2005;. However, recent studies in mouse primary visual cortex (V1) have found that subcortically and intracortically projecting PNs are spatially clustered and are vertically aligned to mini-and microcolumns of cell bodies and dendrites with distinct tuning preferences (Kondo et al, 2016;Marukoda et al, 2017;Znamenskiy et al 2018).…”

Section: Introductionmentioning

confidence: 99%

Spatial clustering of inhibition in mouse primary visual cortex

Bista¹,

D’Souza²,

Meier³

et al. 2019

Preprint

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Whether mouse visual cortex contains orderly feature maps is debated. The overlapping pattern of geniculocortical (dLGN) inputs with M2 muscarinic acetylcholine receptor-rich patches in layer 1 (L1) suggests a non-random architecture. Here, we found that L1 inputs from the lateral posterior thalamus (LP) avoid patches and target interpatches. Channelrhodopsin-assisted mapping of EPSCs in L2/3 shows that the relative excitation of parvalbumin-expressing interneurons (PVs) and pyramidal neurons (PNs) by dLGN, LP and cortical feedback are distinct and depend on whether the neurons reside in clusters aligned with patches or interpatches.Paired recordings from PVs and PNs shows that unitary IPSCs are larger in interpatches than patches. The spatial clustering of inhibition is matched by dense clustering of PV-terminals in interpatches. The results show that the excitation/inhibition balance across V1 is organized into patch and interpatch subnetworks which receive distinct long-range inputs and are specialized for the processing of distinct spatiotemporal features. S1), and measured EGFP intensity in patches (top 3 rd ) and interpatches (bottom 3 rd ). We then normalized the pixel values in interpatches to the mean intensity in patches and plotted the counts in different intensity bins. We found that the fluorescence intensity in patches was 2.1 ± 0.024fold (p = 8x10 -18 , Komolgorov-Smirnov test [KS]) higher in patches than interpatches ( Figure 1D). Similar to our previous findings, patches and interpatches in L1 were 60-80 µm wide and their centroids were 120-140 µm apart. dLGN projections to L4, and 5/6 appeared uniform (data not shown). Inputs to L1 from the LP thalamus exhibited a strikingly different pattern, showing 1.6 ± 0.14-fold (p = 1.33x10 -4 , KS) stronger projections to M2-interpatches ( Figure 1E-H).Simultaneous tracing of dLGN and LP inputs with AAV2/1hSyn.tdTomato.WPRE.bGH and AAV2/1.hSyn.EGFP, respectively, confirmed the interdigitating pattern of projections from primary and higher order thalamic nuclei, showing denser LP input to interpatches (p = 7.95 x 10 -4 , KS) ( Figure 1I-M). Clustering of intracortical inputs to L1 of V1We next compared feedback projections from the higher visual cortical ventral stream lateromedial area, LM, to V1 with inputs from the dLGN. Double viral tracings from the dLGN (AAV2/1.hSyn.EGFP) and LM (AAV2/1hSyn.tdTomato.WPRE.bGH) showed that inputs from both sources overlapped in presumtive M2+ patches of L1 ( Figure 1A-C; 2A). Quantitative analysis showed that LM inputs to patches were 1.7 ± 0.05-fold denser than to interpatches (p = 1.45x10 4 , KS) ( Figure 2B). We have shown previously that inputs from the dorsal stream anterolateral area, AL, terminate in M2+ patches (Ji et al., 2015), raising the question whether M2+ patches are the preferred targets of cortical feedback. To address this, we traced the connections to V1 from the posteromedial area, PM, another member of the dorsal stream (Wang et al. 2012). We found that inputs from PM were non-uniform, overlapped i...

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Mixed functional microarchitectures for orientation selectivity in the mouse primary visual cortex

Cited by 56 publications

References 64 publications

Whisker map organization in somatosensory cortex of awake, behaving mice

Whisker map organization in somatosensory cortex of awake, behaving mice

A global map of orientation tuning in mouse visual cortex

Spatial clustering of inhibition in mouse primary visual cortex

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