Amplification through local critical behavior in the mammalian cochlea

Significance Uniquely among our sensory organs, the ear expends energy to amplify the very stimuli that it detects. This “active process” endows the cochlea with exceptional sensitivity, sharp frequency tuning, and broad dynamical range—yet its workings remain elusive. To date, the cochlea’s fragility and inaccessibility have confined studies in vivo, where global phenomena confound local dynamics. Bridging the gap between cellular and whole-organ behavior, we introduce a preparation that preserves the active process ex vivo in a cochlear segment and thus overcome a long-lasting experimental barrier. We show that the active process operates locally and that the sensory epithelium operates near criticality at a Hopf bifurcation. This result reveals a unified biophysical principle that underlies hearing across insects, nonmammalian vertebrates, and mammals alike.

• Publication year

  2025

• Venue

  Proceedings of the National Academy of Sciences of the United States of America

• Publication date

  2025-07-14

• Fields of study

  Medicine, Physics

• Identifiers
  DOI 10.1073/pnas.2503389122PMID 40658842PMCID 12304976
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Toward an ex vivo preparation for studies of the cochlear active process in mammals.

  2025cited by this paper
• Amplification through local critical behavior in the mammalian cochlea

  2025cited by this paper
• Tuning and Timing of Organ of Corti Vibrations at the Apex of the Intact Chinchilla Cochlea

  2024cited by this paper
• Asymmetric vibrations in the organ of Corti by outer hair cells measured from excised gerbil cochlea

  2024cited by this paper
• The Critical Thing about the Ear's Sensory Hair Cells

  2024cited by this paper
• A bifurcation integrates information from many noisy ion channels and allows for milli-Kelvin thermal sensitivity in the snake pit organ

  2023cited by this paper
• Rectifying and sluggish: Outer hair cells as regulators rather than amplifiers.

  2021cited by this paper
• Salicylate-induced changes in organ of Corti vibrations.

  2021cited by this paper
• Light sheet microscopy of the gerbil cochlea

  2020cited by this paper
• The frequency limit of outer hair cell motility measured in vivo

  2019cited by this paper
• The Frequency Response of Outer Hair Cell Voltage-Dependent Motility Is Limited by Kinetics of Prestin

  2018cited by this paper
• Vibration hotspots reveal longitudinal funneling of sound-evoked motion in the mammalian cochlea

  2018cited by this paper
• Simulating the Chan-Hudspeth experiment on an active excised cochlear segment.

  2017cited by this paper
• Identification of Bifurcations from Observations of Noisy Biological Oscillators

  2016cited by this paper
• State-dependent intrinsic predictability of cortical network dynamics

  2015cited by this paper
• Energy Flux in the Cochlea: Evidence Against Power Amplification of the Traveling Wave

  2015cited by this paper
• Control of a hair bundle’s mechanosensory function by its mechanical load

  2015cited by this paper
• The physics of hearing: fluid mechanics and the active process of the inner ear

  2014cited by this paper
• Integrating the active process of hair cells with cochlear function

  2014cited by this paper
• Detection of cochlear amplification and its activation.

  2013cited by this paper
• Auditory distortions: origins and functions.

  2013cited by this paper
• The diverse effects of mechanical loading on active hair bundles

  2012cited by this paper
• The spatial pattern of cochlear amplification.

  2012cited by this paper
• Phantom tones and suppressive masking by active nonlinear oscillation of the hair-cell bundle

  2012cited by this paper
• Discrimination of Low-Frequency Tones Employs Temporal Fine Structure

  2012cited by this paper
• The interplay between active hair bundle motility and electromotility in the cochlea.

  2010cited by this paper
• A critique of the critical cochlea: Hopf--a bifurcation--is better than none.

  2010cited by this paper
• Ossicular motion related to middle ear transmission delay in gerbil.

  2010cited by this paper
• Spontaneous movements and linear response of a noisy oscillator

  2009cited by this paper
• Cochlear amplification, outer hair cells and prestin.

  2008cited by this paper
• Making an effort to listen: mechanical amplification in the ear.

  2008cited by this paper
• Longitudinally propagating traveling waves of the mammalian tectorial membrane

  2007cited by this paper
• Basilar membrane mechanics in the 6-9 kHz region of sensitive chinchilla cochleae.

  2007cited by this paper
• Panoramic Measurements of the Apex of the Cochlea

  2006cited by this paper
• A generalization of the van-der-Pol oscillator underlies active signal amplification in Drosophila hearing

  2006cited by this paper
• Mechanical responses of the organ of corti to acoustic and electrical stimulation in vitro.

  2005influential reference
• Ca2+ current–driven nonlinear amplification by the mammalian cochlea in vitro

  2005cited by this paper
• Active traveling wave in the cochlea.

  2003cited by this paper
• Cochlear Phase and Amplitude Retrieved from the Auditory Nerve at Arbitrary Frequencies

  2003cited by this paper
• Spontaneous Oscillation by Hair Bundles of the Bullfrog's Sacculus

  2003cited by this paper
• A wave traveling over a Hopf instability shapes the cochlear tuning curve.

  2001cited by this paper
• Auditory nerve fibers in young and quiet-aged gerbils: morphometric correlations with endocochlear potential.

  2001cited by this paper
• Compressive nonlinearity in the hair bundle's active response to mechanical stimulation

  2001cited by this paper
• Evidence for an active process and a cochlear amplifier in nonmammals.

  2001cited by this paper
• Mechanics of the mammalian cochlea.

  2001cited by this paper
• Comparison of a hair bundle's spontaneous oscillations with its response to mechanical stimulation reveals the underlying active process

  2001cited by this paper
• Cochlear mechanisms from a phylogenetic viewpoint.

  2000cited by this paper
• Deformations of the isolated mouse tectorial membrane produced by oscillatory forces.

  2000cited by this paper
• Essential nonlinearities in hearing.

  2000cited by this paper
• Negative hair-bundle stiffness betrays a mechanism for mechanical amplification by the hair cell.

  2000cited by this paper
• Auditory sensitivity provided by self-tuned critical oscillations of hair cells.

  2000cited by this paper
• Mechanical bases of frequency tuning and neural excitation at the base of the cochlea: comparison of basilar-membrane vibrations and auditory-nerve-fiber responses in chinchilla.

  2000cited by this paper
• Active hair-bundle movements can amplify a hair cell's response to oscillatory mechanical stimuli.

  1999cited by this paper
• A model for amplification of hair-bundle motion by cyclical binding of Ca2+ to mechanoelectrical-transduction channels.

  1998cited by this paper
• A new method for the automated detection of spontaneous otoacoustic emissions embedded in noisy data.

  1998cited by this paper
• Two-tone distortion on the basilar membrane of the chinchilla cochlea.

  1997cited by this paper
• The cochlear place-frequency map of the adult and developing Mongolian gerbil.

  1996cited by this paper
• Effects of aging on potassium homeostasis and the endocochlear potential in the gerbil cochlea.

  1996cited by this paper
• Auditory illusions and the single hair cell

  1993cited by this paper
• The active cochlea

  1992cited by this paper
• Two-tone distortion in the basilar membrane of the cochlea

  1991cited by this paper
• A fast motile response in guinea‐pig outer hair cells: the cellular basis of the cochlear amplifier.

  1987cited by this paper
• The Ca2+ activity of cochlear endolymph of the guinea pig and the effect of inhibitors.

  1987cited by this paper
• Analysis of the microphonic potential of the bullfrog's sacculus

  1983cited by this paper
• Temperature Regulation and Bioenergetics of the Mongolian Gerbil Meriones unguiculatus

  1972cited by this paper

• Auditory frequency analysis as an active dissipative process

  2026cites this paper
• Remembering A. James Hudspeth, hair cell explorer

  2025cites this paper
• Sound Masking Strategies for Interference with Mosquito Hearing

  2025cites this paper
• Amplification through local critical behavior in the mammalian cochlea

  2025cites this paper
• Marrying critical oscillators with traveling waves shapes nonlinear sound processing in the cochlea

  2025cites this paper
• Electrical Control of the Transduction Channels’ Gating Force in Mechanosensory Hair Cells

  2025cites this paper
• Efferent control of hair cells mechanically coupled by artificial membranes

  2025cites this paper