Voltage-Sensitive Dye Imaging Reveals Dynamic Spatiotemporal Properties of Cortical Activity after Spontaneous Muscle Twitches in the Newborn Rat

Spontaneous activity in the developing brain contributes to its maturation, but how this activity is coordinated between distinct cortical regions and whether it might reflect developing sensory circuits is not well understood. Here, we address this question by imaging the spread and synchronization of cortical activity using voltage-sensitive dyes (VSDs) in the developing rat in vivo. In postnatal day 4-6 rats (n = 10), we collected spontaneous changes in VSD signal that reflect underlying membrane potential changes over a large craniotomy (50 mm(2)) that encompassed both the sensory and motor cortices of both hemispheres. Bursts of depolarization that occurred approximately once every 12 s were preceded by spontaneous twitches of the hindlimbs and/or tail. The close association with peripheral movements suggests that these bursts may represent a slow component of spindle bursts, a prominent form of activity in the developing somatosensory cortex. Twitch-associated cortical activity was synchronized between subregions of somatosensory cortex, which reflected the synchronized twitching of the limbs and tail. This activity also spread asymmetrically, toward the midline of the brain. We found that the spatial and temporal structure of such spontaneous cortical bursts closely matched that of sensory-evoked activity elicited via direct stimulation of the periphery. These data suggest that spontaneous cortical activity provides a recurring template of functional cortical circuits within the developing cortex and could contribute to the maturation of integrative connections between sensory and motor cortices.