Abstract

Cortical maps, consisting of orderly arrangements of functional columns, are a hallmark of the organization of the cerebral cortex. However, the microorganization of cortical maps at the level of single neurons is not known, mainly because of the limitations of available mapping techniques. Here, we used bulk loading of Ca(2+) indicators combined with two-photon microscopy to image the activity of multiple single neurons in layer (L) 2/3 of the mouse barrel cortex in vivo. We developed methods that reliably detect single action potentials in approximately half of the imaged neurons in L2/3. This allowed us to measure the spiking probability following whisker deflection and thus map the whisker selectivity for multiple neurons with known spatial relationships. At the level of neuronal populations, the whisker map varied smoothly across the surface of the cortex, within and between the barrels. However, the whisker selectivity of individual neurons recorded simultaneously differed greatly, even for nearest neighbors. Trial-to-trial correlations between pairs of neurons were high over distances spanning multiple cortical columns. Our data suggest that the response properties of individual neurons are shaped by highly specific subcolumnar circuits and the momentary intrinsic state of the neocortex.

Highlights

  • In sensory cortical areas, neurons that respond to similar stimuli are clustered together in vertical cortical columns [1,2,3,4,5]

  • In many areas of the cerebral cortex, the action potential (AP) rates are low, and sensory information is encoded by the presence or absence, or the timing, of individual APs [12,32,61]

  • AP-evoked fluorescence changes have been characterized in the rat barrel cortex loaded with Oregon Green BAPTA-1 AM, in which single APs could be detected with more than 95% fidelity

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Summary

Introduction

Neurons that respond to similar stimuli are clustered together in vertical cortical columns [1,2,3,4,5]. Cortical columns are typically arranged in maps, so that columns with similar response properties are close to each other along the cortical surface [2,6,7,8,9]. Most of our knowledge about cortical maps comes from measurements with limited spatial resolution. Single-unit measurements sample neurons over distances of 100 lm or more [10,11]. Blind extracellular recordings are biased towards neurons with strong responses [10,12,13,14]. We know little about the organization of cortical maps with single-cell resolution. Bulkloading of Ca2þ indicators, in combination with two-photon microscopy [19,20,21,22], has been used to analyze the microstructure of visual cortical maps at the level of individual neurons [23,24]

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