Oscillations of extracellular voltage, reflecting synchronous rhythmic activity in large populations of neurons, are a ubiquitous feature in the mammalian brain and are thought to subserve critical, if not fully understood cognitive functions. Oscillations at different frequency bands are hallmarks of specific brain or behavioral states. At the higher end of the scale, ultrafast (400-600 Hz) oscillations in the somatosensory cortex, in response to peripheral stimulation, were previously observed in human and a handful of animal studies; however, their synaptic basis and functional significance remain largely unexplored. Here we report that brief optogenetic activation of thalamocortical axons, in brain slices from mouse somatosensory (barrel) cortex, elicited in the thalamorecipient layer local field potential (LFP) oscillations (“ripplets”) consisting of a sequence of precisely reproducible negative transients at ~400 Hz. Fast-spiking (FS) inhibitory interneurons fired ~400 Hz spike bursts entrained but in antiphase to the LFP oscillation, while regular-spiking (RS) excitatory neurons fired only 1-2 spikes per ripplet and nearly 180 degrees out of phase with FS spikes.  During a ripplet, RS cells received synchronous, precisely repeating sequences of alternating excitatory and inhibitory postsynaptic currents phase-locked to the LFP oscillation, suggesting that ripplets were generated by a chain of excitatory spike volleys synchronized by volleys of IPSPs.  We suggest that ripplets are a ubiquitous cortical response to a brief, highly synchronous and exceptionally salient sensory stimulus, and could provide increased bandwidth for encoding and transmitting sensory information.