Time scale of adaptation at the tonal sequence processing in the awake mice auditory cortex neurons

Мұқаба

Дәйексөз келтіру

Толық мәтін

Ашық рұқсат Ашық рұқсат
Рұқсат жабық Рұқсат берілді
Рұқсат жабық Тек жазылушылар үшін

Аннотация

The study was firstly carried out on stimulus-specific adaptation of neurons in the primary and anterior fields of the awake house mice auditory cortex to sound sequences of four 100-ms tonal signals, with frequency of tones corresponding to the neuronal characteristic frequency, and also with the inter-tone interval constant for one sequence and varying from 0 to 2000 ms in different sequences. The analysis of the data obtained showed the adaptation effect in the responses of all studied primary auditory cortex neurons, which was observed as the absence or significant decrease in activity evoked by the components of a series of tones following the 1st, at inter-stimulus intervals of 0–500 ms. A quantitative assessment of the adaptation effects as a function of inter-stimulus intervals within the tonal sequence, performed over whole population of studied neurons, showed that the individual time scales of adaptation of neurons varied significantly, which may be crucial for the formation of optimal time windows for the processing of grouping and separation of sound events, which are important both for perception of animal vocalizations and human speech.

Толық мәтін

Рұқсат жабық

Авторлар туралы

М. Egorova

Sechenov Institute of Evolutionary Physiology and Biochemistry of the Russian Academy of Sciences

Хат алмасуға жауапты Автор.
Email: ema6913@yandex.ru
Ресей, Saint Petersburg

А. Akimov

Sechenov Institute of Evolutionary Physiology and Biochemistry of the Russian Academy of Sciences

Email: ema6913@yandex.ru
Ресей, Saint Petersburg

G. Khorunzhii

Sechenov Institute of Evolutionary Physiology and Biochemistry of the Russian Academy of Sciences

Email: ema6913@yandex.ru
Ресей, Saint Petersburg

Әдебиет тізімі

  1. Adrian ED (1928) The basis of sensation. New York. W.W. Norton.
  2. Бибиков НГ (2010) Нейрофизиологические механизмы слуховой адаптации. II. Эффекты последействия. Успехи физиол. наук 41(4): 77–92. [Bibikov NG (2010) Neurophysiological mechanisms of auditory adaptation. II. Aftereffects. Advanc Physiol Sci 41(4): 77–92. (In Russ)].
  3. Ulanovsky N, Las L, Farkas D, Nelken I (2004) Multiple time scales of adaptation in auditory cortex neurons. J Neurosci 24(46): 10440–10453. https://doi.org/10.1523/JNEUROSCI.1905-04.2004
  4. Malmierca MS, Sanchez-Vives MV, Escera C, Bendixen A (2014) Neuronal adaptation, novelty detection and regularity encoding in audition. Front Syst Neurosci 8: 111. https://doi.org/10.3389/fnsys.2014.00111
  5. Valdés-Baizabal C, Carbajal GV, Pérez-González D, Malmierca MS (2020) Dopamine modulates subcortical responses to surprising sounds. PLoS Biol 18(10): e3000744. https://doi.org/10.1371/journal.pbio.3000984
  6. Bregman AS (1990) Auditory scene analysis. The Perceptual Organization of Sound. Cambridge. MA. MIT Press.
  7. MacDougall-Shackleton SA, Hulse SH, Gentner TQ, White W (1998) Auditory scene analysis by European starlings (Sturnus vulgaris): Perceptual segregation of tone sequences. J Acoust Soc Am 103(6): 3581–3587. https://doi.org/10.1121/1.423063
  8. Kanwal JS, Medvedev AV, Micheyl C (2003) Neurodynamics for auditory stream segregation: tracking sounds in the mustached bat’s natural environment. Network 14(3): 413–435. https://doi.org/10.1088/0954-898X_14_3_303
  9. Gaub S, Ehret G (2005) Grouping in auditory temporal perception and vocal production is mutually adapted: the case of wriggling calls of mice. J Comp Physiol A 191: 1131–1135. https://doi.org/10.1007/s00359-005-0036-y
  10. Pérez-González D, Malmierca MS, Covey E (2005) Novelty detector neurons in the mammalian auditory midbrain. Europ J Neurosci 22(11): 2879–2885. https://doi.org/10.1111/j.1460-9568.2005.04472.x
  11. Pérez-González D, Hernández O, Covey E, Malmierca MS (2012) GABAA-mediated inhibition modulates stimulus-specific adaptation in the inferior colliculus. PLoS One 7(3): e34297. https://doi.org/10.1371/journal.pone.0034297
  12. Anderson LA, Malmierca MS (2012) The effect of auditory cortex deactivation on stimulus-specific adaptation in the inferior colliculus of the rat. Eur J Neurosci 37(1): 52–62. https://doi.org/10.1111/ejn.12018
  13. Malmierca MS, Cristaudo S, Pérez-González D, Covey E (2009) Stimulus-specific adaptation in the inferior colliculus of the anesthetized rat. J Neurosci 29(17): 5483–5493. https://doi.org/10.1523/JNEUROSCI.4153-08.2009
  14. Valdés-Baizabal C, Casado-Román L, Bartlett EL, Malmierca MS (2021) In vivo whole-cell recordings of stimulus-specific adaptation in the inferior colliculus. Hear Res 399: 107978. https://doi.org/10.1016/j.heares.2020.107978
  15. Anderson LA, Christianson GB, Linden JF (2009) Stimulus-specific adaptation occurs in the auditory thalamus. J Neurosci 29(22): 7359–7363. https://doi.org/10.1523/JNEUROSCI.0793-09.2009
  16. Antunes FM, Malmierca MS (2011) Effect of auditory cortex deactivation on stimulus-specific adaptation in the medial geniculate body. J Neurosci 31(47): 17306–17316. https://doi.org/10.1523/JNEUROSCI.1915-11.2011
  17. Malinina ES, Egorova MA, Khorunzhii GD, Akimov AG (2016) The time scale of adaptation in tonal sequence processing by the mouse auditory midbrain neurons. Dokl Biol Sci 470: 209–213. https://doi.org/10.1134/S001249661605001X
  18. Egorova MA, Malinina ES, Akimov AG, Khorunzhii GD (2018) Adaptation of different types of neurons in the midbrain auditory center to sound pulse sequences. J Evol Biochem Physiol 54(6): 482–486. https://doi.org/10.1134/S002209301806008X
  19. Egorova MA, Akimov AG (2020) Specialization of neurons with different response patterns in the mouse Mus musculus auditory midbrain and primary auditory cortex during communication call processing. J Evol Biochem Physiol 56: 406–414. https://doi.org/10.1134/S0022093020050038
  20. Egorova MA, Khorunzhii GD, Akimov AG (2019) The timescale of adaptation in tonal sequence processing by mouse primary auditory cortical neurons. J Evol Biochem Physiol 55: 497–501. https://doi.org/10.1134/S0022093019060085
  21. Joachimsthaler B, Uhlmann M, Miller F, Ehret G, Kurt S (2014) Quantitative analysis of neuronal response properties in primary and higher-order auditory cortical fields of awake house mice (Mus musculus). Eur J Neurosci 39(6): 904–918. https://doi.org/10.1111/ejn.12478
  22. Joachimsthaler B, Brugger D, Skodras A, Schwarz C (2015) Spine loss in primary somatosensory cortex during trace eyeblink conditioning. J Neurosci 35(9): 3772–3781. https://doi.org/10.1523/JNEUROSCI.2043-14.2015
  23. Egorova MA (2005) Frequency selectivity of neurons of the primary auditory field (A1) and anterior auditory field (AAF) in the auditory cortex of the house mouse (Mus musculus). J Evol Biochem Physiol 41: 476–480. https://doi.org/10.1007/s10893-005-0085-4
  24. Ehret G, Riecke S (2002) Mice and humans perceive multiharmonic communication sounds in the same way. Proc Natnl Acad Sci U S A 99(1): 479–482. https://doi.org/10.1073/pnas.012361999
  25. Stiebler I, Neulist R, Fichtel I, Ehret G (1997) The auditory cortex of the house mouse: left-right differences, tonotopic organization and quantitative analysis of frequency representation. J Comp Physiol A 181: 559–571. https://doi.org/10.1007/s003590050140
  26. Duque D, Malmierca MS (2015) Stimulus-specific adaptation in the inferior colliculus of the mouse: anesthesia and spontaneous activity effects. Brain Struct Funct 220: 3385–3398. https://doi.org/10.1007/s00429-014-0862-1
  27. Nieto-Diego J, Malmierca MS (2016) Topographic distribution of stimulus-specific adaptation across auditory cortical fields in the anesthetized rat. PLoS Biol 14(3): e1002397. https://doi.org/10.1371/journal.pbio.1002397
  28. Von der Behrens W, Bäuerle P, Kössl M, Gaese BH (2009) Correlating stimulus-specific adaptation of cortical neurons and local field potentials in the awake rat. J Neurosci 29(44): 13837–13849. https://doi.org/10.1523/JNEUROSCI.3475-09.2009
  29. Farley BJ, Quirk MC, Doherty JJ, Christian EP (2010) Stimulus-specific adaptation in auditory cortex is an NMDA-independent process distinct from the sensory novelty encoded by the mismatch negativity. J Neurosci 30(49): 16475–16484. https://doi.org/10.1523/JNEUROSCI.2793-10.2010
  30. Вартанян ИА (1978) Слуховой анализ сложных звуков. Л. Наука. [Vartanyan IA (1978) Auditory analysis of complex sounds. L. Nauka. (In Russ)].
  31. Бобошко МЮ (2012) Речевая аудиометрия: учебное пособие. СПб: Изд-во СПбГМУ. [Boboshko MJ (2012) Speech audiometry: textbook. St. Petersburg: Publ House of St. Petersburg State Med Univer. (In Russ)].

Қосымша файлдар

Қосымша файлдар
Әрекет
1. JATS XML
2. Fig. 1. Examples of the activity of two neurons in the auditory cortex of an awake mouse with different temporal dynamics of adaptation (a, b). In the upper part of the figure are peristimulus histograms of neuronal responses evoked by series of tones with different interstimulus intervals. The value of the interstimulus interval for each series is indicated by numbers on the diagram. The number of signal repetitions is 20. The bin size is 2 ms. Abscissa – time, ms. The ordinate is the number of spikes, N. Under each histogram there is a mark of the stimulus, which is a series of 4 tones with a duration of 100 ms each. In the lower part of the figure is the dependence of the magnitude of the response of the same neurons to the 2nd, 3rd and 4th signals of the series on the interpulse interval (response recovery curves). The magnitude of the neuron’s response to the 2–4th signal of the series (the number of spikes) is normalized relative to its response to the 1st signal, i.e., it is equal to the ratio of the number of spikes in the neuron’s response to the corresponding signal to the number of spikes in the response to the 1st signal.

Жүктеу (389KB)
3. Fig. 2. Normalized functions of restoration of responses to the 2nd, 3rd and 4th signals of the series, averaged over 39 neurons. The standard deviations of the average responses of neurons to the corresponding tones of the series are indicated. Other designations are as in Fig. 1.

Жүктеу (114KB)
4. Fig. 3. Temporal dynamics of adaptation to series of near-threshold signals. (a) Peristimulus histograms of responses of a single neuron evoked by series of tones with different interstimulus intervals. The value of the interstimulus interval for each series is indicated by numbers on the diagram. The number of signal repetitions is 20. The bin size is 2 ms. The time window for data analysis is 6.4 s. Abscissa – time, c. Ordinate – number of spikes, N. Below each histogram is a stimulus mark, which is a series of 4 tones each lasting 100 ms. (b) – Dependence of the number of spikes in the response of a single neuron to the 1st, 2nd, 3rd and 4th signals of the series on the interstimulus interval. Abscissa – time, ms. Ordinate – number of spikes, N. (c) – Normalized functions for reconstructing the responses of a single neuron to the 2nd, 3rd and 4th signals of the series; (d) – Normalized reconstruction functions of responses to the 2nd, 3rd and 4th signals of the series, averaged over 8 neurons. The standard deviations of the average responses of neurons to the corresponding tones of the series are indicated. Other designations are as in Fig. 1.

Жүктеу (430KB)

© Russian Academy of Sciences, 2024