Developmental Deprivation-induced Perceptual and Cortical Processing Deficits in Awake-behaving Animals

Overview

Journal Elife

Specialty Biology

Date 2018 Jun 7

PMID 29873632

Citations 24

Authors

Justin D Yao

Dan H Sanes

Affiliations

Soon will be listed here.

Abstract

Sensory deprivation during development induces lifelong changes to central nervous system function that are associated with perceptual impairments. However, the relationship between neural and behavioral deficits is uncertain due to a lack of simultaneous measurements during task performance. Therefore, we telemetrically recorded from auditory cortex neurons in gerbils reared with developmental conductive hearing loss as they performed an auditory task in which rapid fluctuations in amplitude are detected. These data were compared to a measure of auditory brainstem temporal processing from each animal. We found that developmental HL diminished behavioral performance, but did not alter brainstem temporal processing. However, the simultaneous assessment of neural and behavioral processing revealed that perceptual deficits were associated with a degraded cortical population code that could be explained by greater trial-to-trial response variability. Our findings suggest that the perceptual limitations that attend early hearing loss are best explained by an encoding deficit in auditory cortex.

Citing Articles

Developmental hearing loss-induced perceptual deficits are rescued by genetic restoration of cortical inhibition.

Masri S, Mowery T, Fair R, Sanes D Proc Natl Acad Sci U S A. 2024; 121(24):e2311570121.

PMID: 38830095 PMC: 11181144. DOI: 10.1073/pnas.2311570121.

Increased reliance on temporal coding when target sound is softer than the background.

Alamatsaz N, Rosen M, Ihlefeld A Sci Rep. 2024; 14(1):4457.

PMID: 38396044 PMC: 10891139. DOI: 10.1038/s41598-024-54865-5.

Superior semicircular canal dehiscence and subsequent closure induces reversible impaired decision-making.

Mowery T, Wackym P, Nacipucha J, Dangcil E, Stadler R, Tucker A Front Neurol. 2023; 14:1259030.

PMID: 37905188 PMC: 10613502. DOI: 10.3389/fneur.2023.1259030.

Sensory cortex plasticity supports auditory social learning.

Paraouty N, Yao J, Varnet L, Chou C, Chung S, Sanes D Nat Commun. 2023; 14(1):5828.

PMID: 37730696 PMC: 10511464. DOI: 10.1038/s41467-023-41641-8.

Increased Central Auditory Gain and Decreased Parvalbumin-Positive Cortical Interneuron Density in the Mouse Model of Schizophrenia Correlate With Hearing Impairment.

Zinnamon F, Harrison F, Wenas S, Liu Q, Wang K, Linden J Biol Psychiatry Glob Open Sci. 2023; 3(3):386-397.

PMID: 37519460 PMC: 10382707. DOI: 10.1016/j.bpsgos.2022.03.007.

References

Muller-Preuss P, Flachskamm C, Bieser A . Neural encoding of amplitude modulation within the auditory midbrain of squirrel monkeys. Hear Res. 1994; 80(2):197-208. DOI: 10.1016/0378-5955(94)90111-2. View

Sadagopan S, Wang X . Contribution of inhibition to stimulus selectivity in primary auditory cortex of awake primates. J Neurosci. 2010; 30(21):7314-25. PMC: 3842484. DOI: 10.1523/JNEUROSCI.5072-09.2010. View

Ponton C, Eggermont J . Of kittens and kids: altered cortical maturation following profound deafness and cochlear implant use. Audiol Neurootol. 2002; 6(6):363-80. DOI: 10.1159/000046846. View

Mowery T, Kotak V, Sanes D . The onset of visual experience gates auditory cortex critical periods. Nat Commun. 2016; 7:10416. PMC: 4736048. DOI: 10.1038/ncomms10416. View

Mowery T, Penikis K, Young S, Ferrer C, Kotak V, Sanes D . The Sensory Striatum Is Permanently Impaired by Transient Developmental Deprivation. Cell Rep. 2017; 19(12):2462-2468. PMC: 5577933. DOI: 10.1016/j.celrep.2017.05.083. View

Carandini M, Ferster D . Membrane potential and firing rate in cat primary visual cortex. J Neurosci. 2000; 20(1):470-84. PMC: 6774139. View

McAdams C, Maunsell J . Effects of attention on the reliability of individual neurons in monkey visual cortex. Neuron. 1999; 23(4):765-73. DOI: 10.1016/s0896-6273(01)80034-9. View

BUCHWALD J, Huang C . Far-field acoustic response: origins in the cat. Science. 1975; 189(4200):382-4. DOI: 10.1126/science.1145206. View

von Trapp G, Aloni I, Young S, Semple M, Sanes D . Developmental hearing loss impedes auditory task learning and performance in gerbils. Hear Res. 2016; 347:3-10. PMC: 5391307. DOI: 10.1016/j.heares.2016.07.020. View

10.

Xu L, Furukawa S, Middlebrooks J . Sensitivity to sound-source elevation in nontonotopic auditory cortex. J Neurophysiol. 1998; 80(2):882-94. DOI: 10.1152/jn.1998.80.2.882. View

11.

Boettcher F, Poth E, Mills J, Dubno J . The amplitude-modulation following response in young and aged human subjects. Hear Res. 2001; 153(1-2):32-42. DOI: 10.1016/s0378-5955(00)00255-0. View

12.

Billimoria C, Kraus B, Narayan R, Maddox R, Sen K . Invariance and sensitivity to intensity in neural discrimination of natural sounds. J Neurosci. 2008; 28(25):6304-8. PMC: 2730838. DOI: 10.1523/JNEUROSCI.0961-08.2008. View

13.

Kiorpes L . Visual processing in amblyopia: animal studies. Strabismus. 2006; 14(1):3-10. DOI: 10.1080/09273970500536193. View

14.

Otazu G, Tai L, Yang Y, Zador A . Engaging in an auditory task suppresses responses in auditory cortex. Nat Neurosci. 2009; 12(5):646-54. PMC: 4084972. DOI: 10.1038/nn.2306. View

15.

Grant K, Summers V, Leek M . Modulation rate detection and discrimination by normal-hearing and hearing-impaired listeners. J Acoust Soc Am. 1998; 104(2 Pt 1):1051-60. DOI: 10.1121/1.423323. View

16.

Viemeister N . Temporal modulation transfer functions based upon modulation thresholds. J Acoust Soc Am. 1979; 66(5):1364-80. DOI: 10.1121/1.383531. View

17.

Krishna B, Semple M . Auditory temporal processing: responses to sinusoidally amplitude-modulated tones in the inferior colliculus. J Neurophysiol. 2000; 84(1):255-73. DOI: 10.1152/jn.2000.84.1.255. View

18.

Takesian A, Kotak V, Sanes D . Age-dependent effect of hearing loss on cortical inhibitory synapse function. J Neurophysiol. 2011; 107(3):937-47. PMC: 3289466. DOI: 10.1152/jn.00515.2011. View

19.

Safaai H, von Heimendahl M, Sorando J, Diamond M, Maravall M . Coordinated population activity underlying texture discrimination in rat barrel cortex. J Neurosci. 2013; 33(13):5843-55. PMC: 6705064. DOI: 10.1523/JNEUROSCI.3486-12.2013. View

20.

Popescu M, Polley D . Monaural deprivation disrupts development of binaural selectivity in auditory midbrain and cortex. Neuron. 2010; 65(5):718-31. PMC: 2849994. DOI: 10.1016/j.neuron.2010.02.019. View