Precise spike-timing information in the brainstem is well aligned with the needs of communication and the perception of environmental sounds

The dynamic fluctuations in the amplitude of sound, known as sound envelopes, are ubiquitous in natural sounds and convey information critical for the recognition of speech, and of sounds generally. We are perceptually most sensitive to slow modulations which are most common. However, previous studies of envelope coding in the brainstem found an under-representation of these slow, low-frequency, modulations. Specifically, the synchronization of spike times to the envelope was enhanced in some neuron types, forming channels specialized for envelope processing but tuned to a restricted range of fast, high-frequency, envelopes (200–500 Hz). Here, we show using a historical dataset from cats that previous analyses, which made strong assumptions about the neural code, underestimated the encoding of low-frequency envelopes. While some neurons encode envelope better than others, most encode a wide range of envelope frequencies, and represent slower envelope fluctuations most accurately in their precise patterns of spike times. Identification of envelope frequency from spike-timing was linked to reliability, and to the way that dynamics of spiking interacted with the time-varying envelope. In some of the best-performing neurons, temporally complex “mode-locked” spike patterns served to enhance envelope coding. A second long-standing contradiction was that neural envelope coding is degraded at high sound levels, whilst the perception of envelope is robust at a wide range of sound levels. We find that spike-time encoding of envelope shape becomes level-robust for small populations of neurons. These findings argue against feature-specific coding of envelopes in the brainstem, and for a distributed population spike-time code for which synchrony to the envelope is an incomplete description. This code is accurate for slow fluctuations and robust across sound level. Thus, precise spike-timing information in the brainstem is after-all aligned with the needs of communication and the perception of environmental sounds.Classical studies suggested that slow amplitude fluctuations in sounds critical for speech recognition are poorly represented in the brainstem. This paper shows that overlooked intricacies of spike timing represent these fluctuations, reconciling low-level neural processing with perception.