Entracking as a Brain Stem Code for Pitch: The Butte Hypothesis

Abstract

The basic nature of pitch is much debated. A robust code for pitch exists in the auditory nerve in the form of an across-fiber pooled interspike interval (ISI) distribution, which resembles the stimulus autocorrelation. An unsolved question is how this representation can be "read out" by the brain. A new view is proposed in which a known brain-stem property plays a key role in the coding of periodicity, which I refer to as "entracking", a contraction of "entrained phase-locking". It is proposed that a scalar rather than vector code of periodicity exists by virtue of coincidence detectors that code the dominant ISI directly into spike rate through entracking. Perfect entracking means that a neuron fires one spike per stimulus-waveform repetition period, so that firing rate equals the repetition frequency. Key properties are invariance with SPL and generalization across stimuli. The main limitation in this code is the upper limit of firing (~ 500 Hz). It is proposed that entracking provides a periodicity tag which is superimposed on a tonotopic analysis: at low SPLs and fundamental frequencies > 500 Hz, a spectral or place mechanism codes for pitch. With increasing SPL the place code degrades but entracking improves and first occurs in neurons with low thresholds for the spectral components present. The prediction is that populations of entracking neurons, extended across characteristic frequency, form plateaus ("buttes") of firing rate tied to periodicity.

Inhibition in the auditory brainstem enhances signal representation and regulates gain in complex acoustic environments

“…Hence, our results show that acoustically evoked inhibition plays a major role in shaping the SBC response. Most models of pitch perception are based on or related to an autocorrelation of neuronal activity and rely on temporal precision and reproducibility (Licklider, 1951; Meddis and Hewitt, 1991; Cariani and Delgutte, 1996; Yost, 1996; de Cheveigné, 1998; Denham, 2005; Joris, 2016). The improvement of both characteristics at the ANF-SBC synapse might support the neuronal processing of pitch, but experimental evidence is lacking.…”

A Neuronal Network Model for Pitch Selectivity and Representation

“…Although the frequency range is restricted compared to human pitch perception (up to 4 kHz), pitch range of complex tones, such as the MF and amplitude-modulated tones, are generally restricted to low frequencies as well, up to a few hundred hertz (Plack and Oxenham, 2005 , Section 3.5.1). Besides, physiological recordings of brain stem neurons also generally show a decrease of entrainment for frequency higher than 500 Hz (Recio-Spinoso, 2012 ; Joris, 2016 ). The pitch of a pure tone of higher frequency can be encoded by its spectral content.…”

“…In this case, the pitch frequency estimate is a monotonic function of firing rate and the range of pitch frequency representation depends on the phase-locking capability of the neuron. Joris ( 2016 ) also propose that entrained phase-locking of neurons in the brain stem can serve as a representation of pitch, as an alternative to the autocorrelations of AN spike times.…”

Modeling Pitch Perception With an Active Auditory Model Extended by Octopus Cells

“…It is a pure place code by indexing the innervated auditory nerve fiber (ANF) along the tonotopically ordered axis. In the second case pitch is derived from inter-spike interval histograms of consecutively firing CFs relying on phase locking of the auditory nerve spike firings to quasi-stationary tonal signals (Stolzenburg, 2015 ; Joris, 2016 ). Neuro-physiologically parameterized auditory models mimic the dynamics of the basilar membrane, the mechano-electrical coupling of inner hair cells, and the membrane voltage regulated vesicle rate-kinetics (Voutsas et al, 2005 ; Balaguer-Ballester et al, 2009 ).…”