Cell-type-specific coupling of single-unit spikes and cortical ripples in macaque and human V1

Abstract

Cortical ripples are brief high-frequency (80-150 Hz) oscillatory bursts in the extracellular potential, typically associated with sleep, memory, and attention processes. So far it is unclear whether cortical ripples are specific to a given function or brain state and what types of neurons engage in synchronous rhythmic firing during the oscillation. First, we report the presence of cortical ripples in V1 of macaque monkeys at rest. These bursts arise both with eyes closed and open, and exhibit distinct spatio-temporal organization, with ripple-band power increases consistently accompanied by elevated spiking. Exploiting unique massively parallel recordings in macaque monkeys, spike sorting combined with waveform classification revealed six single-unit classes: two matching canonical Layer 4 waveforms, one broadly distributed type, and three types with features consistent with deep layers. These classes are differentially modulated with respect to ripple-band activity, differing in firing-rate modulation, strength of phase locking, and preferred ripple-band phase. In particular, putative deep-layer neurons show non-sinusoidal phase locking, which we explain using a simple thresholding mechanism implemented in a computational model. Beyond the resting state, we show that this ripple-associated spiking organization is also present during natural-image viewing, with preserved preferred phases and firing-rate modulation. Finally, we confirm the translatability of these findings by identifying analogous spiking organization in V1 of a blind human. Together, these results suggest that ripple oscillations during both rest and visual stimulation may arise from a shared underlying circuit that is conserved across species and largely independent of behavioral state or sensory drive.