Local Diversity and Fine-Scale Organization of Receptive Fields in Mouse Visual Cortex

Abstract

Many thousands of cortical neurons are activated by any single sensory stimulus, but the organization of these populations is poorly understood. For example, are neurons in mouse visual cortex-whose preferred orientations are arranged randomly-organized with respect to other response properties? Using high-speed in vivo two-photon calcium imaging, we characterized the receptive fields of up to 100 excitatory and inhibitory neurons in a 200 m imaged plane. Inhibitory neurons had nonlinearly summating, complex-like receptive fields and were weakly tuned for orientation. Excitatory neurons had linear, simple receptive fields that can be studied with noise stimuli and system identification methods. We developed a wavelet stimulus that evoked rich population responses and yielded the detailed spatial receptive fields of most excitatory neurons in a plane. Receptive fields and visual responses were locally highly diverse, with nearby neurons having largely dissimilar receptive fields and response time courses. Receptive-field diversity was consistent with a nearly random sampling of orientation, spatial phase, and retinotopic position. Retinotopic positions varied locally on average by approximately half the receptive-field size. Nonetheless, the retinotopic progression across the cortex could be demonstrated at the scale of 100 m, with a magnification of ϳ10 m/°. Receptive-field and response similarity were in register, decreasing by 50% over a distance of 200 m. Together, the results indicate considerable randomness in local populations of mouse visual cortical neurons, with retinotopy as the principal source of organization at the scale of hundreds of micrometers.

Cortical neural populations can guide behavior by integrating inputs linearly, independent of synchrony

“…1C and Figs. S1 and S2), comparable to the number of neurons affected by the smallest possible visual stimulus because of the size and scatter of V1 receptive fields (22). Animals readily detected ChR2 stimulation, and we obtained precise psychometric thresholds for direct cortical stimulation, as in sensory tasks (23), by changing the intensity of the stimulus ( Fig.…”

Functional organization of excitatory synaptic strength in primary visual cortex

“…Please note that we applied no randomization or blinded assignment of animals to groups and no animals were excluded from any analyses. The number of experimental preparations used in the analysis was chosen according to previous studies 10,13 . Mice were initially anaesthetized with a mixture of fentanyl (0.05 mg per kg), midazolam (5.0 mg per kg), and medetomidine (0.5 mg per kg).…”

“…After in vivo imaging experiments, whole-cell recordings in vitro were performed using an approach as described previously 10,13 . After two-photon calcium imaging in vivo, red fluorescent microspheres (Lumafluor) were injected into the imaged region to facilitate identification of the same region in sliced tissue.…”

“…Using this procedure, 42% of neurons, 1,969/4,743, had fraction of explained variance >10% (range: 22-59%, 17 experiments), comparable to previous reports (48%, 222/463, in ref. 13), where fraction of explained variance is defined as 100 (R 2 ), where R is the Pearson's product-moment correlation coefficient between the actual and predicted responses.…”

“…The linear RF describes the relative position of ON (response to light increments) and OFF (response to light decrements) subfields in visual space, and thus provides information about visual features to which a neuron is most sensitive, including their orientation, phase, spatial frequency and size. RFs of nearby cortical neurons were highly diverse within each imaged population in L2/3 [12][13][14][15] (example region in Fig. 2b).…”