Tinnitus-like "hallucinations" elicited by sensory deprivation in an entropy maximization recurrent neural network

PLoS Comput Biol. 2021 Dec 8;17(12):e1008664. doi: 10.1371/journal.pcbi.1008664. eCollection 2021 Dec.

Abstract

Sensory deprivation has long been known to cause hallucinations or "phantom" sensations, the most common of which is tinnitus induced by hearing loss, affecting 10-20% of the population. An observable hearing loss, causing auditory sensory deprivation over a band of frequencies, is present in over 90% of people with tinnitus. Existing plasticity-based computational models for tinnitus are usually driven by homeostatic mechanisms, modeled to fit phenomenological findings. Here, we use an objective-driven learning algorithm to model an early auditory processing neuronal network, e.g., in the dorsal cochlear nucleus. The learning algorithm maximizes the network's output entropy by learning the feed-forward and recurrent interactions in the model. We show that the connectivity patterns and responses learned by the model display several hallmarks of early auditory neuronal networks. We further demonstrate that attenuation of peripheral inputs drives the recurrent network towards its critical point and transition into a tinnitus-like state. In this state, the network activity resembles responses to genuine inputs even in the absence of external stimulation, namely, it "hallucinates" auditory responses. These findings demonstrate how objective-driven plasticity mechanisms that normally act to optimize the network's input representation can also elicit pathologies such as tinnitus as a result of sensory deprivation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Algorithms
  • Auditory Perception / physiology
  • Cochlear Nucleus / physiology
  • Computer Simulation*
  • Entropy
  • Hallucinations / physiopathology*
  • Humans
  • Information Theory
  • Neural Networks, Computer*
  • Neuronal Plasticity / physiology
  • Sensory Deprivation / physiology*
  • Tinnitus / physiopathology*

Grant support

OS received financial support from the Israel Science Foundation (https://www.isf.org.il; Grant No. 504/17). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.