An Integrative Tinnitus Model Based on Sensory Precision

Abstract

Tinnitus is a common disorder that often complicates hearing loss. Its mechanisms are incompletely understood. Current theories proposing pathophysiology from the ear to the cortex cannot individually - or collectively - explain the range of experimental evidence available. We propose a new framework, based on predictive coding, in which spontaneous activity in the subcortical auditory pathway constitutes a 'tinnitus precursor' which is normally ignored as imprecise evidence against the prevailing percept of 'silence'. Extant models feature as contributory mechanisms acting to increase either the intensity of the precursor or its precision. If precision (i.e., postsynaptic gain) rises sufficiently then tinnitus is perceived. Perpetuation arises through focused attention, which further increases the precision of the precursor, and resetting of the default prediction to expect tinnitus.

Keywords: auditory cortex; precision; predictive coding; tinnitus.

Figure 1

Conceptual Overview of the Model. The core of the model is the process of perceptual inference, driven by a descending auditory prediction (yellow arrow; initially of silence) and by spontaneous activity in the auditory pathway that constitutes a sensory prediction error (red arrow) and, in effect, a ‘tinnitus precursor’. The precision of ascending prediction errors and descending predictions is denoted by arrow width, where the tinnitus precursor has an inherently low precision and therefore makes little or no contribution to perception or posterior beliefs. Various factors (blue boxes) – alone or in combination – can increase the precision of the tinnitus precursor which, if it becomes sufficiently high, results in the perception of tinnitus (orange). Even if this increase in precision is reversed, tinnitus can be perpetuated by two mechanisms (orange arrows): learning to expect tinnitus, and reinforcement via attention.

Figure 2

Key Figure: Putative Neurobiological Architecture of the Model The proposed neurobiological basis of tinnitus is summarised here, focusing on auditory cortex, which receives a tinnitus precursor signal (originating peripherally or subcortically). This precursor acts as a spontaneous prediction error in a process of perceptual inference involving predictions from regions encoding prior expectations, particularly auditory memory representations from parahippocampal cortex. Key contributory processes are numbered (primary in black, contributory in grey). Most of these processes promote tinnitus by increasing the effective precision of the tinnitus precursor in auditory cortex via the following mechanisms: increasing ascending input to auditory cortex (2, 3, 5, 10); increasing the gain on cortical superficial pyramidal cells that encode prediction errors (5, 7, 11); increasing synchrony of gamma oscillations encoding prediction errors (6, 7); increasing the long-range synchrony of gamma oscillation bursts via low-frequency oscillations (4). Abbreviations: BF, basal forebrain; dACC, dorsal anterior cingulate cortex; DCN, dorsal cochlear nucleus; GPNs, global perceptual networks; HG, Heschl's gyrus (incorporating A1, the primary auditory cortex); IC, inferior colliculus; IPC, inferior parietal cortex; NS, non-specific auditory thalamus; OFM, orofacial movements (cross-modal inputs); PHC, parahippocampal cortex; Prec., precuneus; S, specific (lemniscal) auditory thalamus; SG/G/IG, supragranular/granular/infragranular neuronal layers; STG, superior temporal gyrus (incorporating non-primary auditory cortex); TRN, thalamic reticular nucleus; vl/vmPFC, ventrolateral/ventromedial prefrontal cortex. Oscillation frequencies: δ, delta (∼1–4 Hz); θ, theta (∼4–8 Hz); α, alpha (∼8–12 Hz); β, beta (∼12–30 Hz); γ, gamma (>∼30 Hz).

Figure 3

Perceptual Inference Processes Underlying Tinnitus Initiation, Perpetuation, and Modulation. The inset box annotates perceptual inference in terms of the prior (prediction), likelihood (tinnitus precursor) and posterior (tinnitus percept) represented by Gaussian distributions over a perceptual dimension of intensity or loudness, with their widths indicating precision. Loudness may be encoded by neuronal firing rate or be represented more abstractly. In each plot, the perceived loudness of tinnitus is indicated by the position of the posterior distribution on the horizontal axis. (A) In hearing loss alone, the tinnitus precursor has insufficient precision to override the default prediction of silence. (B) With increased precision the precursor influences perception, leading to a revised posterior percept of tinnitus. Potentially there is a window of reversibility at this stage. (C) If the default prediction is revised to expect tinnitus (generally less intense than the precursor), then the condition becomes chronic (through experience-dependent plasticity). (D) Reduction of the precision of the precursor to its pre-tinnitus level results in habituation, but not cessation of tinnitus – on account of plastic changes to prior predictions. (E) Theoretically, patients with functional overlay may have a prediction of louder tinnitus than encoded by the precursor, and therefore tinnitus intensity would have no empirical bound. (F) Residual inhibition (RI) can be understood as attenuating the precision and/or intensity of the precursor through forward masking, thus reducing the precision-weighted prediction error (PWPE) and therefore gamma oscillations. An alternative mechanism is the temporary resetting of descending predictions to ‘silence’, increasing prediction error per se (hence gamma) but reducing the posterior percept. (G) In residual excitation (RE), temporary modification of the tinnitus prediction (increasing its loudness and/or reducing its precision) by a perceptually similar and precise stimulus leads to reduced prediction error (hence gamma), and increased tinnitus loudness more in line with that encoded by the precursor. (H) In functional overlay patients, acoustic forward masking, and the consequent fall in gamma oscillations, bias inference towards higher tinnitus intensity than encoded by the precursor (leading to RE).

Figure I

Schematic of Altered Inter-Areal Inputs in Existing Models of Tinnitus Generation.