Evidence for common spike-based temporal coding of overt and covert speech in pars triangularis of human Broca's area

Brocas area has long been described as a central region of cortical speech networks. Yet, its detailed role during speech production remains largely unknown and even sometimes debated. Recordings at the individual neuron level could help understand whether and how speech is encoded in this region but such data remain very scarce. Here we use direct intracortical recording in pars triangularis of human Brocas area to show that the encoding of speech in this region relies not only on spike rates but also on the precise timing of action potentials within individual spike trains. First, we found that the overall spike rate of the whole population remained unchanged between periods of rest, overt and covert speech, but that individual firing rates of a few neurons fluctuated across these conditions. These fluctuations resulted in different overall population dynamics across conditions. Next, we also observed that the temporal arrangement of spikes within individual spike trains was not purely random but also signed which sentence was produced. By matching ensemble spike trains based on inter-spike intervals, it was possible to decode which sentence had been pronounced well above chance and with a comparable accuracy than when using spike counts. Moreover, the temporal code characterizing the overt production of individual sentences was found to be largely conserved when the same sentences were covertly imagined and enabled to decode cover sentences with an accuracy 75% higher than when considering spike counts. Altogether, these results suggest the existence of 2 modes of speech encoding in Brocas area, one based on the modulation of individual firing rates and the other based on the precise temporal structure of individual spike trains, and that the latter type of encoding remains more largely conserved between overt and covert speech production.