Dynamic Encoding of Phonetic Categories in Zebra Finch Auditory Forebrain

Overview

Journal Sci Rep

Specialty Science

Date 2023 Jul 10

PMID 37430030

Authors

Wanyi Liu

David S Vicario

Affiliations

Soon will be listed here.

Abstract

Vocal communication requires the formation of acoustic categories to enable invariant representations of sounds despite superficial variations. Humans form acoustic categories for speech phonemes, enabling the listener to recognize words independent of speakers; animals can also discriminate speech phonemes. We investigated the neural mechanisms of this process using electrophysiological recordings from the zebra finch secondary auditory area, caudomedial nidopallium (NCM), during passive exposure to human speech stimuli consisting of two naturally spoken words produced by multiple speakers. Analysis of neural distance and decoding accuracy showed improvements in neural discrimination between word categories over the course of exposure, and this improved representation transferred to the same words by novel speakers. We conclude that NCM neurons formed generalized representations of word categories independent of speaker-specific variations that became more refined over the course of passive exposure. The discovery of this dynamic encoding process in NCM suggests a general processing mechanism for forming categorical representations of complex acoustic signals that humans share with other animals.

References

DiCarlo J, Cox D . Untangling invariant object recognition. Trends Cogn Sci. 2007; 11(8):333-41. DOI: 10.1016/j.tics.2007.06.010. View

Sharpee T, Atencio C, Schreiner C . Hierarchical representations in the auditory cortex. Curr Opin Neurobiol. 2011; 21(5):761-7. PMC: 3223290. DOI: 10.1016/j.conb.2011.05.027. View

Friederici A . The brain basis of language processing: from structure to function. Physiol Rev. 2011; 91(4):1357-92. DOI: 10.1152/physrev.00006.2011. View

Bizley J, Cohen Y . The what, where and how of auditory-object perception. Nat Rev Neurosci. 2013; 14(10):693-707. PMC: 4082027. DOI: 10.1038/nrn3565. View

Burdick C, Miller J . Speech perception by the chinchilla: discrimination of sustained /a/ and /i/. J Acoust Soc Am. 1975; 58(2):415-27. DOI: 10.1121/1.380686. View

Dooling R, Brown S . Speech perception by budgerigars (Melopsittacus undulatus): spoken vowels. Percept Psychophys. 1990; 47(6):568-74. DOI: 10.3758/bf03203109. View

Hienz R, Brady J . The acquisition of vowel discriminations by nonhuman primates. J Acoust Soc Am. 1988; 84(1):186-94. DOI: 10.1121/1.396963. View

Kluender K, Diehl R, Killeen P . Japanese quail can learn phonetic categories. Science. 1987; 237(4819):1195-7. DOI: 10.1126/science.3629235. View

Kuhl P, Miller J . Speech perception by the chinchilla: voiced-voiceless distinction in alveolar plosive consonants. Science. 1975; 190(4209):69-72. DOI: 10.1126/science.1166301. View

10.

Ohms V, Gill A, van Heijningen C, Beckers G, Ten Cate C . Zebra finches exhibit speaker-independent phonetic perception of human speech. Proc Biol Sci. 2009; 277(1684):1003-9. PMC: 2842761. DOI: 10.1098/rspb.2009.1788. View

11.

Carruthers I, Laplagne D, Jaegle A, Briguglio J, Mwilambwe-Tshilobo L, Natan R . Emergence of invariant representation of vocalizations in the auditory cortex. J Neurophysiol. 2015; 114(5):2726-40. PMC: 4644228. DOI: 10.1152/jn.00095.2015. View

12.

Elie J, Theunissen F . Meaning in the avian auditory cortex: neural representation of communication calls. Eur J Neurosci. 2015; 41(5):546-67. PMC: 4347984. DOI: 10.1111/ejn.12812. View

13.

Moore R, Lee T, Theunissen F . Noise-invariant neurons in the avian auditory cortex: hearing the song in noise. PLoS Comput Biol. 2013; 9(3):e1002942. PMC: 3591274. DOI: 10.1371/journal.pcbi.1002942. View

14.

Schneider D, Woolley S . Sparse and background-invariant coding of vocalizations in auditory scenes. Neuron. 2013; 79(1):141-52. PMC: 3713513. DOI: 10.1016/j.neuron.2013.04.038. View

15.

Chew S, Mello C, Nottebohm F, Jarvis E, Vicario D . Decrements in auditory responses to a repeated conspecific song are long-lasting and require two periods of protein synthesis in the songbird forebrain. Proc Natl Acad Sci U S A. 1995; 92(8):3406-10. PMC: 42175. DOI: 10.1073/pnas.92.8.3406. View

16.

Phan M, Pytte C, Vicario D . Early auditory experience generates long-lasting memories that may subserve vocal learning in songbirds. Proc Natl Acad Sci U S A. 2006; 103(4):1088-93. PMC: 1327730. DOI: 10.1073/pnas.0510136103. View

17.

Soyman E, Vicario D . Rapid and long-lasting improvements in neural discrimination of acoustic signals with passive familiarization. PLoS One. 2019; 14(8):e0221819. PMC: 6715244. DOI: 10.1371/journal.pone.0221819. View

18.

Kobak D, Brendel W, Constantinidis C, Feierstein C, Kepecs A, Mainen Z . Demixed principal component analysis of neural population data. Elife. 2016; 5. PMC: 4887222. DOI: 10.7554/eLife.10989. View

19.

Trautmann E, Stavisky S, Lahiri S, Ames K, Kaufman M, OShea D . Accurate Estimation of Neural Population Dynamics without Spike Sorting. Neuron. 2019; 103(2):292-308.e4. PMC: 7002296. DOI: 10.1016/j.neuron.2019.05.003. View

20.

Kriengwatana B, Escudero P, Kerkhoven A, Ten Cate C . A general auditory bias for handling speaker variability in speech? Evidence in humans and songbirds. Front Psychol. 2015; 6:1243. PMC: 4548094. DOI: 10.3389/fpsyg.2015.01243. View