Milliseconds of Sensory Input Abruptly Modulate the Dynamics of Cortical States for Seconds

Abstract

Spontaneous internal activity plays a major role in higher brain functions. The question of how it modulates sensory evoked activity and behavior has been explored in anesthetized rodents, cats, monkeys and in behaving human subjects. However, the complementary question of how a brief sensory input modulates the internally generated activity in vivo remains unresolved, and high-resolution mapping of these bidirectional interactions was never performed. Integrating complementary methodologies, at population and single cells levels, we explored this question. Voltage-sensitive dye imaging of population activity in anesthetized rats' somatosensory cortex revealed that spontaneous up-states were largely diminished for ~2 s, even after a single weak whisker deflection. This effect was maximal at the stimulated barrel but spread across several cortical areas. A higher velocity whisker deflection evoked activity at ~15Hz. Two-photon calcium imaging activity and cell-attached recordings confirmed the VSD results and revealed that for several seconds most single cells decreased their firing, but a small number increased firing. Comparing single deflection with long train stimulation, we found a dominant effect of the first population spike. We suggest that, at the onset of a sensory input, some internal messages are silenced to prevent overloading of the processing of relevant incoming sensory information.

Keywords: barrel cortex; calcium imaging; cortical states; internal activity; spontaneous activity; two-photon microscopy; voltage-sensitive dye imaging.