New article clarifies the predictive nature of auditory responses in brainstem and cortex.
Another great collaboration with Emily Coffey (Concordia U) and the Zatorre lab (McGill), demonstrating the unique ability of MEG to reveal subtle neurophysiological mechanisms in local and large-scale brain circuits. The findings were published in The Journal of Neuroscience.
The challenge here consisted in elucidating the nature of the signals induced by repeated auditory presentations known to entrain a so-called frequency-following response (FFR) in brain circuits along the auditory pathway (from cochlea to cortex). The FFR is a tool that is extensively used in audiology, for instance to test the integrity of brain auditory responses. We had found in previous studies that FFR has several neural generators, from small and deep brainstem nuclei, to cortex. These results have had substantial impact in the field.
The present study addressed a form of controversy in neuroscience concerning the actual nature of “neural entrainment”, whereby neural circuits may be driven in an oscillatory fashion by repeating, oscillatory inputs. The core of the controversy resided in the question whether neural oscillations are mere passive responses driven by the physical properties of stimulus inputs, or whether there is a form of resonance in neural activity that is the product of active neurophysiological processes.
This question may sound über specialized but is actually important because entrainment, especially in the typical FFR frequency range, is relevant to speech and music processing by the brain. If we understand better these basic mechanisms, we may also understand better both the nature of auditory cognition and how these mechanisms are affected in e.g., hearing loss and other syndromes that challenge perception, such as in autism and schizophrenia.
One of the main findings of Emily’s present study is that there is indeed clear, active oscillatory entrainment in auditory cortex and brainstem pathways, that persists after FFR auditory stimulation. Below is an illustration of the effect in the auditory cortex (AC).
Another very cool result is that neural instantaneous frequency in the auditory cortex and as deep as the cochlear nucleus of the brainstem evolves over a very short period of time: neural oscillations start around 80Hz at the onset of the auditory presentation, and increase over 100 ms to catch up with the frequency of the physical auditory input (100Hz). They then go back to their baseline frequency after stimulus offset, but it takes another “good 50ms” for this to happen. Both the frequency adaption and ringing of neural oscillations indicate there are active processes at play, and that they are not just passive responses to external responses. This effect is shown in the right auditory cortex in the figure below.
In a second experiment, Emily tested how transitions between stimulus frequencies affected the FFR. This question is important because perception depends on context, in the sense that the brain constantly tries to predict the next inputs from our senses for us to respond as adequately as possible: in other words, we love being offered presents but we tend to dislike being taken by surprise ;)
Emily found indeed that the FFR was affected by the frequency of the preceding tone for up to 40 ms at subcortical levels, and even longer durations at cortical levels. This is illustrated below.
Activity in the right auditory cortex in response to pairs of tones, aligned at the transition point between tone dyads (dashed lines). In the transition to the same stimulus (top), the cortical response to tone B appears to differ, whereas after transition from tone B (bottom), both traces resemble one another despite a 50 Hz difference in stimulus frequency.
There are many other interesting results in the paper, so please dive in if interested. The original manuscript is accessible in open access via ResearchGate. Please contact us directly if you do not have access to the Journal of Neuroscience version.
From the article: “There is much debate about the existence and function of neural oscillatory mechanisms in the auditory system. The frequency-following response (FFR) is an index of neural periodicity encoding that can provide a vehicle to study entrainment in frequency ranges relevant to speech and music processing. Criteria for entrainment include the presence of post-stimulus oscillations and phase alignment between stimulus and endogenous activity. To test the hypothesis of entrainment, in experiment 1 we collected FFR data to a repeated syllable using magneto- and electroencephalography in 20 male and female human adults. We observed significant oscillatory activity after stimulus offset in auditory cortex and subcortical auditory nuclei, consistent with entrainment. In these structures the FFR fundamental frequency converged from a lower value over 100 ms to the stimulus frequency, consistent with phase alignment, and diverged to a lower value after offset, consistent with relaxation to a preferred frequency. In experiment 2, we tested how transitions between stimulus frequencies affected the MEG-FFR to a train of tone pairs in 30 people. We found that the FFR was affected by the frequency of the preceding tone for up to 40 ms at subcortical levels, and even longer durations at cortical levels. Our results suggest that oscillatory entrainment may be an integral part of periodic sound representation throughout the auditory neuraxis. The functional role of this mechanism is unknown, but it could serve as a fine-scale temporal predictor for frequency information, enhancing stability and reducing susceptibility to degradation that could be useful in real-life noisy environments.”
Significance statement: “Neural oscillations are proposed to be a ubiquitous aspect of neural function, but their contribution to auditory encoding is not clear, particularly at higher frequencies associated with pitch encoding. In a magnetoencephalography experiment, we found converging evidence that the frequency-following response has an oscillatory component according to established criteria: post-stimulus resonance, progressive entrainment of the neural frequency to the stimulus frequency, and relaxation toward the original state upon stimulus offset. In a second experiment, we found that the frequency and amplitude of the frequency-following response to tones are affected by preceding stimuli. These findings support the contribution of intrinsic oscillations to the encoding of sound, and raise new questions about their functional roles, possibly including stabilization and low-level predictive coding.”