Fast frequency modulation is encoded according to the listener expectations in the human subcortical auditory pathway

Abstract

Expectations aid and bias our perception. In speech, expected words are easier to recognise than unexpected words, particularly in noisy environments, and incorrect expectations can make us misunderstand our conversational partner. Expectations are combined with the output from the sensory pathways to form representations of speech in the cerebral cortex. However, it is unclear whether expectations are propagated further down to subcortical structures to aid the encoding of the basic dynamic constituent of speech: fast frequency-modulation (FM). Fast FM-sweeps are the basic invariant constituent of consonants, and their correct encoding is fundamental for speech recognition. Here we tested the hypothesis that subjective expectations drive the encoding of fast FM-sweeps characteristic of speech in the human subcortical auditory pathway. We used fMRI to measure neural responses in the human auditory midbrain (inferior colliculus) and thalamus (medial geniculate body). Participants listened to sequences of FM-sweeps for which they held different expectations based on the task instructions. We found robust evidence that the responses in auditory midbrain and thalamus encode the difference between the acoustic input and the subjective expectations of the listener. The results indicate that FM-sweeps are already encoded at the level of the human auditory midbrain and that encoding is mainly driven by subjective expectations. We conclude that the subcortical auditory pathway is integrated in the cortical network of predictive speech processing and that expectations are used to optimise the encoding of even the most basic acoustic constituents of speech.

Frequency and frequency modulation share the same predictive encoding mechanisms in human auditory cortex

“…We analyzed fMRI-data from two previous studies that focused on subcortical auditory prediction error encoding of pure tones [23] and FM-sweeps [59]. Both experiments used the same auditory oddball paradigm with different stimulus types.…”

“…All participants were neurotypical normal-hearing German native speakers (see [23] and [59] for further details on inclusion criteria). Nineteen participants (12 female) between the ages of 24 and 34 (average 26.6) participated in the pure tone study; eighteen participants (12 female) between the age of 19 and 31 (average 24.6) participated in the FM-sweep study.…”

“…Each of the sequences was consequently characterized by one of three possible absolute frequency span differences characterizing the distance between standards and deviants (∆ = |∆f dev − ∆f std |). See Figure 1B for an exemplary illustration of the FM-sweep stimuli and sequences [59].…”

“…However, if the deviant was not in position 4, since deviants occur once in each sequence, the probability of hearing a deviant in position five after hearing four standards is 1/2. If the deviant was neither in position 4 nor 5, the probability of a deviant in position six after hearing five standards is 1 [23,59].…”

“…However, E/MEG studies lack the spatial resolution to precisely locate neural populations generating these responses. The only fMRI study that has investigated prediction error to FM focused on subcortical areas [59]. It is still unclear whether FM is encoded as prediction error in the AC and, if so, whether the same neural populations encode prediction error to pure tones and FM-sweeps.…”