Sensory SystemsSensory SystemsСенсорные системы0235-00923034-5936The Russian Academy of Sciences67578010.31857/S0235009224020017DDVFSNОБЗОРЫReview ArticleThe characteristic features of the auditory neurons responses in terrestrial vertebrates to species-specific communication calls (analytical review)К вопросу о специфике реакции нейронов слуховой системы наземных позвоночных на видовые коммуникационные стимулы (аналитический обзор)BibikovN. G.БибиковН. Г.
Russian Federation
nbibikov1@yandex.ruN.N. Andreev Acoustic InstituteАкустический институт им. акад. Н. Н. АндрееваA. A. Kharkevich Institute of Information Transmission Problems of the Russian Academy of SciencesИнститут проблем передачи информации им. А. А. Харкевича РАН0108202438232728022025Copyright ©; 2024, Russian Academy of SciencesCopyright ©; 2024, Российская академия наук2024Russian Academy of SciencesРоссийская академия наукhttps://journals.eco-vector.com/0235-0092/article/view/675780

One of the main functions of sensory systems is the implementation of intraspecific communication, which often occurs through the exchange of communication calls. It is quite natural that the hypothesis arises that the radiation and reception of these signals should be coordinated. There is usually a certain similarity in the characteristics of specific communication sounds and the receiving devices of an auditory analyzer. However, the degree of such correspondence in the neural structures of the brain remains a subject of debate. The review examines studies aimed at solving the issue of specialized encoding of such signals in the brains of various terrestrial vertebrates, ranging from tailless amphibians to primates. For decades, researchers have been searching for neurons in the direct auditory pathway that could serve as detectors of communication signals. However, an analysis of the extensive literature does not reveal the existence of any clearly defined area of the direct auditory pathway that would be specialized for analyzing this category of sounds. It seems that the functional significance of the neurons of this pathway consists of highlighting many features of the temporal flow within the entire perceived spectral composition of sound. This process is carried out on the trained synaptic connections in the process of permanent evolution, determined by the sensory environment. Dynamically organized ensembles of neurons can be formed in the central parts of the direct auditory pathway, synchronously reacting to the action of a certain sound. It is precisely such ensembles that can be considered as output structures of an auditory analyzer, which can determine the perception and the corresponding motor reactions.

Одной из основных функций сенсорных систем является осуществление внутривидового общения, которое часто проходит путем обмена коммуникационными звуковыми сигналами. Естественно возникает гипотеза о том, что излучение и прием этих сигналов должны быть согласованы. В самом деле, обычно наблюдается сходство характеристик звуков видового общения и приемных устройств слухового анализатора. Однако степень такого соответствия в нейронных структурах головного мозга остается предметом оживленных дискуссий. В обзоре рассматриваются исследования, направленные на решение вопроса о специализированном кодировании видовых сигналов у разных наземных позвоночных. В течение многих десятилетий исследователи стремились найти нейроны, служащие детекторами сигналов внутривидового общения. Однако анализ литературы не выявляет существования областей прямого слухового пути, специализированных для выделения только этой категории звуков. Представляется, что функция нейронов, составляющих его ядра, состоит в выделении особенностей временного течения звуков, воспринятых слуховым нервом. Этот процесс осуществляется на обучаемых синаптических связях в процессе перманентной эволюции, определяемой сенсорным окружением. В центральных отделах могут формироваться динамически организуемые ансамбли нейронов, синхронно реагирующих при действии определенного звука. Такие ансамбли могут рассматриваться в качестве выходных структур слухового анализатора, определяющих восприятие сигнала и моторные реакции организма.

communication callsdirect auditory pathwayneuronal detectorsevolutionкорковый нейронвидовой коммуникационный звукпрямой слуховой путьсинхронизированный нейронный ансамбльAkimov A.G. Kodirovaniye modeley krika diskomforta myshat populyatsiyey neyronov tsentral’nogo yadra zadnego kholma srednego mozga myshi (Mus musculus) [Encoding of pups’ wriggling call models by neuronal population of midbrain inferior colliculus central nucleus in house mouse (Mus musculus)] Zhurnal evolyutsionnoy biokhimii i fiziologii [Journal of Evolutionary Biochemistry and Physiology]. 2013. V. 49. № 3. P. 233–236 (in Russian). https://doi.org/10.1134/S0022093013030122Акимов А.Г. Кодирование моделей крика дискомфорта мышат популяцией нейронов центрального ядра заднего холма среднего мозга мыши (Mus musculus). Журн. эвол. биохим. и физиол. 2013. Т. 49. № 3. С. 233–236.Bibikov N.G. Impul’snaya aktivnost’ neyronov torus semicircularis travyanoy lyagushki (Rana temporaria) [Impulse activity of neurons of the torus semicircularis grass frog (Rana temporaria)] Zhurnal evolyutsionnoy biokhimii i fiziologii [Journal of Evolutionary Biochemistry and Physiology].1974. V. 10. № 1. P. 40–47 (in Russian).Бибиков Н.Г. Импульсная активность нейронов torus semicircularis травяной лягушки (Rana temporaria) Журн. эвол. биохим. и физиол. 1974. Т. 10. № 1. С. 40–47.Bibikov N.G. Reaktsiya neyronov polukruzhnogo torusa ozernoy lyagushki (Rana ridibunda) na nekotoryye kommunikatsionnyye signaly amfibiy. [Reaction of neurons of the semicircular torus of the lake frog (Rana ridibunda) to some communication signals of amphibians]. Zoologicheskiy zhurnal [Zoolog. Journal] 1987. V. 66. № 8. P. 1214–1223 (in Russian).Бибиков Н.Г. Реакция нейронов полукружного торуса озерной лягушки (Rana r. ridibunda) на некоторые коммуникационные сигналы амфибий. Зоолог. журн. 1987. Т. 66. № 8. С. 1214–1223.Bibikov N.G. Aktivnost’ slukhovykh neyronov istmal’noy zony ozernoy lyagushki. [Activity of auditory neurons in the isthmal zone of the lake frog]. Sensornye sistemy [Sensory systems]. 2002. V. 16. № 1. P. 23–34 (in Russian).Бибиков Н.Г. Активность слуховых нейронов истмальной зоны озерной лягушки. Сенсорные системы. 2002. Т. 16. № 1. С. 23–34.Bibikov N.G. Metody otsenki slukhovykh sposobnostey beskhvostykh amfibiy [Methods for assessing the hearing abilities of tailless amphibians]. Zoologicheskiy zhurnal [Zoolog. Journal]. 2019. V. 98. № 3. P. 285–301. https://doi.org/10.1134/S0044513419030048Бибиков Н.Г. Методы оценки слуховых способностей бесхвостых амфибий. Зоолог. журн. 2019. Т. 98. № 3. С. 285–301. https://doi.org/10.1134/S0044513419030048Adrian E.D., Craik K.J.W., Sturdy R.S. The electrical response of the auditory mechanism in cold-blooded vertebrates. Proceed. Royal Society London. 1938. V. 125. № 841. P. 435–455. https://doi.org/jstor.org/stable/i204892Akimov G., Egorova M.A., Ehret G. Spectral summation and facilitation in on- and off-responses for optimized representation of communication calls in mouse inferior colliculus. Eur. J.Neurosci. 2017. V. 46. № 3. P. 440–459. https://doi.org/10.1111/ejn.13488Akimov.G., Egorova M.A., Ehret G. Spectral summation and facilitation in on- and off-responses for optimized representation of communication calls in mouse inferior colliculus. Eur. J.Neurosci. 2017. V. 46. № 3. P. 440–459. https://doi.org/10.1111/ejn.13488.Aushana Y., Souffi S., Edeline J.-M., Lorenzi C., Huetz C. Robust neuronal discrimination in primary auditory cortex despite degradations of spectro-temporal acoustic details: comparison between guinea pigs with normal hearing and mild age-related hearing loss. J. Assoc. Res. Otolaryng. 2018. V. 19. № 2. P.163–180. https://doi.org/10.1007/s10162-017-0649-1Aushana Y., Souffi S., Edeline J.-M., Lorenzi C., Huetz C. Robust neuronal discrimination in primary auditory cortex despite degradations of spectro-temporal acoustic details: comparison between guinea pigs with normal hearing and mild age-related hearing loss. J. Assoc. Res. Otolaryng. 2018. V. 19. № 2. P. 163–180. https://doi.org/10.1007/s10162-017-0649-1.Betancourth-Cundar M., Lima A.P., Hӧdl W., Amézquita A. Decoupled evolution between senders and receivers in the Neotropical Allobates femoralis frog complex. Plos One. 2016. V. 11. Article E0155929. https://doi.org/10.1371/journ al.pone.0155929Betancourth-Cundar M., Lima A.P., Hӧdl W., Amézquita A. Decoupled evolution between senders and receivers in the Neotropical Allobates femoralis frog complex. Plos One. 2016. V. 11. P. E0155929. https://doi.org/10.1371/journ al.pone.0155929Bibikov N.G. Auditory units in the medulla of the marsh frog with unusual patterns of spontaneous activity. J. Comp. Physiol. A. 1993. V. 173. № 1. P. 123–131. https://doi.org/10.1007/bf00209624Bibikov N.G. Auditory units in the medulla of the marsh frog with unusual patterns of spontaneous activity. J. Comp. Physiol. A. 1993. V. 173. №. 1. P. 123–131. https://doi.org/10.1007/bf00209624Bibikov N.G., Elepfandt A. Auditory evoked potentials from medulla and midbrain in the clawed frog Xenopus laevis. Hear. Res. 2005. V. 204. P. 29–36. https://doi.org/10.1016/j.heares.2004.12.009Bibikov N.G. Nizamov S.V. Temporal coding of low-frequency amplitude modulation in the torus semicircularis of the grassfrog. Hear. Res. 1996. V. 101. № 1. P. 23–44. https://doi.org/10.1016/s0378-5955(96)00128-1Bibikov N.G. Nizamov S.V. Statistical characteristics of the spike activity of neurons in the midbrain auditory center in frogs on exposure to tones modulated by low-frequency noise. Neurosc. Behav. Physiol. 2018. V. 48. № 6. P. 764–773. https://doi.org/10.1007/s11055-018-0628-yBibikov N.G. Addition of noise enhanced neural synchrony to amplitude-modulated sounds in the frog’s midbrain. Hear. Res. 2002. V. 173. № 1. P. 21–28. https://doi.org/10.1016/s0378-5955(02)00456-2Bibikov N.G., Grubnik O.N. Responses to intensity increments and decrements in different types of midbrain auditory units of the frog. In: Acoustical signal processing in the central auditory system. New York. Plenum Press, 1997. P. 271–277. https://doi.org/10.1007/978-1-4419-8712Bibikov N.G., Grubnik O.N. Responses to intensity increments and decrements in different types of midbrain auditory units of the frog. Acoustical signal processing in the central auditory system. New York. Plenum Press.1997. P. 271–277. https://doi.org/10.1007/978-1-4419-8712.Bizley J.K., Walker K.M.M., King A.J., Schnupp J.W.H. Neural ensemble codes for stimulus periodicity in auditory cortex. J. Neurosc. 2010. V. 30. № 14. P. 5078–5091. https://doi.org/10.1523/jneurosci.5475-09.2010Bizley J.K., Walker K.M. M., King A.J., Schnupp J.W.H. Neural ensemble codes for stimulus periodicity in auditory cortex. J. Neurosc. 2010. V. 30. № 14. P. 5078–5091. https://doi.org/10.1523/jneurosci.5475-09.2010Brittan-Powell E.F., Christensen-Dalsgaard J., Tang Y.Z., Carr C., Dooling R.J. The auditory brainstem response in two lizard species. J. Acoust. Soc. Amer. 2010. V. 128. P. 787–794. https://doi.org/10.1121/1.3458813Brittan-Powell E.F., Christensen-Dalsgaard J., Tang Y.Z., Carr C., Dooling R.J. The auditory brainstem response in two lizard species. J. Acoust. Soc. Amer. 2010. V. 128. P.787–794. https://doi.org/10.1121/1.3458813Capranica R.R., Moffat A.J.M. Neurobehavioral correlates of sound communication in anurans. Advances in Vertebrate Neuroethology. Eds: Ewert J.-P., Capranica R.R., Ingle D.J. Springer US. Boston.1983. P. 701–730. https://doi.org/10.1007/978-1-4684- 4412-4_36Capranica R.R., Moffat A.J.M. Neurobehavioral correlates of sound communication in anurans. Advances in Vertebrate Neuroethology. Eds: Ewert J.P., Capranica R.R., Ingle D.J. Springer US. Boston.1983. P. 701–730. https://doi.org/10.1007/978-1-4684-4412-4_36Carruthers I.M., Laplagne D.A., Jaegle A., Briguglio J.J., Mwilambwe-Tshilobo L., Natan R.G., Geffen M.N. Emergence of invariant representation of vocalizations in the auditory cortex. J. Neurophysiol. 2015. V. 114. № 5. P.726–740. https://doi.org/10.1152/jn.00095.2015Carruthers I.M., Laplagne D.A., Jaegle A., Briguglio J.J., Mwilambwe-Tshilobo L., Natan R.G., Geffen M.N. Emergence of invariant representation of vocalizations in the auditory cortex. J. Neurophysiol. 2015. V. 114. № 5. P. 726–740. https://doi.org/10.1152/jn.00095.2015.Chen J., Jono T., Cui J., Yue X., Tang Y. The acoustic properties of low intensity vocalizations match hearing sensitivity in the webbed-toed gecko Gekko subpalmatus. Plos ONE. 2016. V. 11. Article E0146677. https://doi.org/10.1371/journal.pone.0146677Chen J., Jono T., Cui J., Yue X., Tang Y. The acoustic properties of low intensity vocalizations match hearing sensitivity in the webbed-toed gecko Gekko subpalmatus. Plos ONE. 2016. V. 11. P. E0146677. https://doi.org/10.1371/journal.pone.0146677Cobo-Cuan A., Narins P.M. Reciprocal matched filtering in the inner ear of the african clawed frog (Xenopus laevis). J. Ass. Res. Otolaryng. 2020. V. 21. P. 33–42. https://doi.org/10.1007/s1016 2-019-00740-4Cobo-Cuan.A., Narins P.M. Reciprocal matched filtering in the inner ear of the african clawed frog (Xenopus laevis). J. Ass. Res. Otolaryng. 2020. V. 21. P. 33–42. https://doi.org/10.1007/s1016 2-019-00740-4De Charms R.C., Merzenich M.M. Primary cortical representation of sounds by the coordination of action-potential timing. Nature.1996. V. 381. P. 610–613. https://doi.org/10.1038/381610a0De Cheveigne A. The auditory system as a “separation machine”. Physiological and psychophysical bases of auditory function. Eds: Breebart D.J., Houtsma A.J.M., Kohlrausch A., Prijs V.F., Schoonhoven R. Maastricht. 2001. P. 453–460.Egorova M., Akimov A. 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. 2020. V. 56. P. 406–414. https://doi.org/10.1134/S0022093020050038Egorova M., Akimov A. 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. 2020. V. 56. P. 406–414. https://doi.org/10.1134/S0022093020050038.Ehret G., Geissler D. Communication-call representation in the mouse auditory cortex: perception vs. recognition. Plasticity and Signal Representation in the Auditory System. 2005. P. 85–96. https://doi.org/10.1007/0-387-23181-1-8Ehret G., Geissler D. Communication-call representation in the mouse auditory cortex: perception vs. recognition // In the book “Plasticity and Signal Representation in the Auditory System”. 2005. P. 85–96. https://doi.org/10.1007/0-387-23181-1-8Eliades S.J., Tsunada J. Auditory cortical activity drives feedback-dependent vocal control in marmosets. Nature Comm. 2018. V. 9. № 1. P.1–13. https://doi.org/10.1038/s41467-018-04961-8Eliades S.J., Tsunada J. Auditory cortical activity drives feedback-dependent vocal control in marmosets. Nature Comm. 2018. V. 9. №.1. P.1–13. https://doi.org/10.1038/s41467-018-04961-8Eliades S.J., Wang X. Contributions of sensory tuning to auditory-vocal interactions in marmoset auditory cortex. Hear. Res. 2017. V. 348. P. 98–111. https://doi.org/10.1016/j.heares.2017.03.001Endler J.A. Some general comments on the evolution and design of animal communication systems. Philosoph. Transactions: Biol. Sciences.1993. V. 340. P. 215–225. https://doi.org/10.1098/rstb.1993.0060Endler J.A. Some general comments on the evolution and design of animal communication systems. Philosoph. Transactions: Biol.Sciences.1993. V. 340. P. 215–225. https://doi.org/10.1098/rstb.1993.0060Frishkopf L.S., Capranica R.R., Goldstein M.H.J. Neural coding in the bullfrog’s auditory system – a teleological approach. Proceedings IEEE.1968. V. 56. № 6. P. 969–980. https://doi.org/10.1109/proc.1968.6448Frishkopf L.S., Capranica R.R., Goldstein M.H.J. Neural coding in the bullfrog’s auditory system – a teleological approach. Proceedings IEEE. 1968. V. 56. № 6. P. 969–980. https://doi.org/10.1109/proc.1968.6448Fuzesseryz M., Feng A.S. Mating call selectivity in the thalamus and midbrain of the leopard frog (Rana p. Pipiens): Single and multiunit analyses. J. Comp. Physiol. 1983. V. 150. P. 333–344. https://doi.org/10.1007/BF00605023Gadziola M.A., Grimsley J.M.S, Shanbhag S.J., Wenstrup J.J. A novel coding mechanism for social vocalizations in the lateral amygdala. J. Neurophysiol. 2012. V. 107. P. 1047–1057. https://doi.org/10.1152/jn.00422.2011Gansel K.S. Neural synchrony in cortical networks: mechanisms and implications for neural information processing and coding. Front. Integr. Neurosci. 2022. V. 16. Article 900715. https://doi.org/10.3389/fnint.2022.900715Gansel K.S. Neural synchrony in cortical networks: mechanisms and implications for neural information processing and coding. Front. Integr. Neurosci. 2022. V. 16. P. 900715. https://doi.org/10.3389/fnint.2022.900715Gaucher Q., Huetz C., Gourévitch B., Edeline J.M. Cortical inhibition reduces information redundancy at presentation of communication sounds in the primary auditory cortex. J. Neurosci. 2013а. V. 33. № 26. P. 10713–10728. https://doi.org/10.1523/jneurosci.0079-13.2013Gaucher Q., Huetz C., Gourévitch B., Edeline J.M. Cortical inhibition reduces information redundancy at presentation of communication sounds in the primary auditory cortex. J. Neurosci. 2013а. V. 33. №. 26. P.10713–10728. https://doi.org/10.1523/jneurosci.0079-13.2013Gaucher Q., Huetz C., Gourévitch B., Laudanski J., Occelli F., Edeline J.M. How do auditory cortex neurons represent communication sounds? Hear Res. 2013b. V. 305. P.102–112. https://doi.org/10.1016/j.heares.2013.03.011Gaucher Q., Huetz C., Gourévitch B., Laudanski J., Occelli F., Edeline J.M. How do auditory cortex neurons represent communication sounds? Hear Res. 2013b. V. 305. P. 102–112. https://doi.org/10.1016/j.heares.2013.03.011Gehr D.D., Komiya H., Eggermont J.J. Neuronal responses in cat primary auditory cortex to natural and altered species-specific calls. Hear Res. 2000. V. 150. P. 27–42. https://doi.org/10.1016/s0378-5955(00)00170-2Gehr D.D., Komiya H., Eggermont J.J. Neuronal responses in cat primary auditory cortex to natural and altered species-specific calls. Hear Res. 2000.V. 150. P. 27–42. https://doi.org/10.1016/s0378-5955(00)00170-2Geissler D.B., Ehret. G. Time-critical integration of formants for perception of communications calls in mice. Proc. Natl. Acad. Sci. USA. 2002. V. 99. P. 9021–9025. https://doi.org/10.1073/pnas.122606499Glass I., Wollberg Z. Lability in the responses of cells in the auditory cortex of squirrel monkeys to species-specific vocalizations. Exp. Brain Res.1979. V. 34. P. 489–498. https://doi.org/10.1007/BF00239144Gourévitch B., Eggermont J.J. Spatial representation of neural responses to natural and altered conspecific vocalizations in cat auditory cortex. J. Neurophysiol. 2007. V. 97. № 1. P. 144–158. https://doi.org/10.1152/jn.00807.2006Gourévitch B., Eggermont J.J. Spatial representation of neural responses to natural and altered conspecific vocalizations in cat auditory cortex. J. Neurophysiol. 2007. V. 97. № 1. P. 144–158. https://doi.org/10.1152/jn.00807.2006.Goutte S., Mason M.J., Christensen-Dalsgaard J., Montealegre F., Chivers B., Sarria F.A., Antoniazzi M.M., Jared C., Satol A., Toledo L.F. Evidence of auditory insensitivity to vocalization frequencies in two frogs. Scientific Reports. 2017. V. 7. Article 12121. https://doi.org/10.1038/s4159 8-017-12145-5Goutte S., Mason M.J., Christensen-Dalsgaard J., Montealegre F., Chivers B., Sarria F.A., Antoniazzi M.M., Jared C., Toledo L.F. Evidence of auditory insensitivity to vocalization frequencies in two frogs. Scientific Reports .2017. V. 7. Article 12121. https://doi.org/10.1038/s4159 8-017-12145-5Grimsley J.M.S., Shanbhag S.J., Palmer A.R., Wallace M.N. Processing of communication calls in guinea pig auditory cortex. Plos ONE. 2012a. V. 7. Article e51646. https://doi.org/10.1371/journal.pone.0051646Grimsley J.M.S., Palmer A.R., Wallace M.N. Different representations of tooth chatter and purr call in guinea pig auditory cortex. Neuroreport. 2011b. V. 22. № 12. P. 613–616. https://doi.org/10.1097/WNR.0b013e3283495ae9Grimsley J.M.S., Palmer A.R., Wallace M.N. Age differences in the purr call distinguished by units in the adult guinea pig primary auditory cortex. Hear. Res. 2011a. V. 277. P. 134–142. https://doi.org/10.1016/j.heares.2011.01.018Gupta S., Alluri R.K., Rose G.J., Bee M.A. Neural basis of acoustic species recognition in a cryptic species complex. J. Exp. Biol. 2021. V. 224. № 23. Article Jeb243405. https://doi.org/10.1242/jeb.243405Hall J.C. Feng A.S. Evidence for parallel processing in the frog’s auditory thalamus. J. Comp. Neurol. 1987. V. 258. № 3. P. 407–419. https://doi.org/10.1002/cne.902580309. PMID: 3495555.Hall J.C., Feng A.S. Evidence for parallel processing in the frog’s auditory thalamus. J. Comp. Neurol. 1987. V. 258. № 3. P. 407–419. https://doi.org/10.1002/cne.902580309. PMID: 3495555.Huetz C., Philibert B., Edeline J.-M. A spike timing code for discriminating conspecific vocalizations in the thalamocortical system of anesthetized and awake guinea pigs. J. Neurosci. 2009. V. 29. P. 334–350. https://doi.org/10.1523/jneurosci.3269-08.2009Huetz C., Gourevitch B., Edeline J.-M. Neural codes in the thalamocortical auditory system: From artificial stimuli to communication sounds. Hear Res. 2011. V. 271. P. 147–158. https://doi.org/10.1016/j.heares.2010.01.010Jia G., Bai S., Lin Y., Wang X., Zhu L., Lyu C, Sun G., An K., Roe A.W., Li X., Gao L. Representation of conspecific vocalizations in amygdala of awake marmosets. Natl. Sci. Rev. 2023. V. 10. Article nwad194. https://doi.org/10.1093/nsr/nwad194Jia G., Bai S., Lin Y., Wang X., Zhu L., Lyu C., Sun G., An K., Roe A.W., Li X., Gao L. Representation of conspecific vocalizations in amygdala of awake marmosets. Natl. Sci. Rev. 2023. V. 10. Article nwad194. https://doi.org/10.1093/nsr/nwad194.Kar M., Pernia M., Williams K. et al. Vocalization categorization behavior explained by a feature-based auditory categorization model. Elife. 2022. V. 11. Article E78278. https://doi.org/10.7554/elife.78278Kar M., Pernia M., Williams K. et al. Vocalization categorization behavior explained by a feature-based auditory categorization model. Elife. 2022. V. 11. E78278. https://doi.org/10.7554/elife.78278Kanwal J.S., Rauschecker J.P. Auditory cortex of bats and primates: managing species-specific calls for social communication. Frontiers in Bioscience. 2007. V. 12. P. 4621–4640. https://doi.org/10.2741/2413Kusmierek P., Rauschecker J.P. Functional specialization of medial auditory belt cortex in the alert rhesus monkey. J. Neurophysiol. 2009. V. 102. P. 1606–1622. https://doi.org/10.1152/jn.00167.2009Labra A., Reyes-Olivares C., Moreno-Gómez F.N., Velásquez N.A., Penna M., Delano P.H., Narins P.M. Geographic variation in the matching between call characteristics and tympanic sensitivity in the Weeping lizard. Ecol. Evol. 2021. V. 11. № 24. P. 18633–18650. https://doi.org/10.1002/ece3.8469Lee N., Schrode K.M., Bee M.A. Nonlinear processing of a multicomponent communication signal by combination-sensitive neurons in the anuran inferior colliculus. J. Comp. Physiol. S.A. 2017. V. 203. № 9. P. 749–772. https://doi.org/10.1007/s00359-017-1195-3Lettvin J.Y., Maturana H.R., Mcculloch W.S., Pitts W. What the frog’s eye tells the frog’s brain. Proceedings of the IRE. 1959. V. 47. P. 1940–1951. https://doi.org/10.1109/jrproc.1959.287207Lu S., Steadman M, Ang G.W.Y., Kozlov A. Composite receptive fields in the mouse auditory cortex. J. Physiol. 2023. V. 601. №.18. P. 4091–4104. https://doi.org/10.1113/JP285003Lu S., Steadman M, Ang. G.W.Y., Kozlov A. Composite receptive fields in the mouse auditory cortex. J. Physiol. 2023. V. 601. № 18. P. 4091–4104. https://doi.org/10.1113/JP285003Ma H., Qin L., Dong C., Zhong R., Sato Y. Comparison of neural responses to cat meows and human vowels in the anterior and posterior auditory field of awake cats. Plos ONE. 2013. V. 8. P. E52942. https://doi.org/10.1371/journal.pone.0052942Ma H., Qin L., Dong C., Zhong R., Sato Y. Comparison of neural responses to cat meows and human vowels in the anterior and posterior auditory field of awake cats. Plos ONE. 2013. V. 8. Article E52942. https://doi.org/10.1371/journal.pone.0052942Manley G., Kraus J. Exceptional high-frequency hearing and matched vocalizations in Australian pygopod geckos. J. Exp. Biology. 2010. V. 213. P. 1876–1885. https://doi.org/10.1242/jeb.040196Manley G., Kraus J. Exceptional high-frequency hearing and matched vocalizations in Australian pygopod geckos. J. Exp.Biology. 2010. V. 213. P. 1876–1885. https://doi.org/10.1242/jeb.040196Manley J.A., Muller-Preuss P. Response variability of auditory cortex cells in the squirrel monkey to constant acoustic stimuli. Exp. Brain Res. 1978. V. 32. № 2. P. 171–180. https://doi.org/10.1007/bf00239725Mathevon N., Vergne A., Aubin T. Acoustic communication in crocodiles: How do juvenile calls code information? Proceed. Meetings. Acoust. 2013. V. 19. Article 010001. https://doi.org/10.1121/1.4799192Mathevon N., Vergne A., Aubin T. Acoustic communication in crocodiles: How do juvenile calls code information? Proceed. Meet. Acoust. 2013. V. 19. Article 010001. https://doi.org/10.1121/1.4799192Medvedev A.V., Kanwal J.S. Local field potentials and spiking activity in the primary auditory cortex in response to social calls. J. Neurophysiol. 2004. V. 92. № 1. P. 52–65. https://doi.org/10.1152/jn.01253.2003Metzen M.G., Jamali M., Carriot J., Ávila-Ǻkerberg O., Cullen K.E., Chacron M.J. Coding of envelopes by correlated but not single-neuron activity requires neural variability. Proceed. Nat. Acad. Sciences. 2015. V. 112. № 15. P. 4791–4796. https://doi.org/10.1073/pnas.1418224112Metzen M.G., Jamali M., Carriot J., Ávila-Ǻkerberg O., Cullen K.E., Chacron M.J. Coding of envelopes by correlated but not single-neuron activity requires neural variability. Proceed. Nat. Acad. Sciences. 2015. V. 112. № 15. 4791–4796. https://doi.org/10.1073/pnas.1418224112Miller C.T., Thomas A.W., Nummela S.U., de la Mothe L.A. Responses of primate frontal cortex neurons during natural vocal communication. J. Neurophysiol. 2015. V. 114. № 2. P. 1158–1171. https://doi.org/10.1152/jn.01003.2014Montes-Lourido P., Kar M., David S.V., Sadagopan S. Neuronal selectivity to complex vocalization features emerges in the superficial layers of primary auditory cortex. Plos Biol. 2021. V. 19. E3001299. https://doi.org/10.1371/journal.pbio.300129Montes-Lourido P., Kar M., David S.V., Sadagopan S. Neuronal selectivity to complex vocalization features emerges in the superficial layers of primary auditory cortex. Plos. Biol. 2021. V. 19. Article E3001299. https://doi.org/10.1371/journal.pbio.300129Montes-Lourido P., Kar M., Pernia M., Parida S., Sadagopan S. Updates to the guinea pig animal model for in-vivo auditory neuroscience in the low-frequency hearing range. Hear Res. 2022. V. 424. 108603. https://doi.org/10.1016/j.heares.2022.108603Montes-Lourido P., Kar M., Pernia M., Parida S., Sadagopan S. Updates to the guinea pig animal model for in-vivo auditory neuroscience in the low-frequency hearing range. Hear Res. 2022. V. 424. Article 108603. https://doi.org/10.1016/j.heares.2022.108603Mudry K.M., Capranica R.R. Correlation between auditory evoked responses in the thalamus and species-specific call characteristics. J. Comp. Physiol. 1987. V. 160. P. 477–489. https://doi.org/10.1007/BF00615081Nelken I.A., Fishbach L., Las L., Ulanovsky N., Farkas D. Primary auditory cortex of cats: feature detection or something else? Biol. Cyber. 2003. V. 89. P. 397–406. https://doi.org/10.1007/s00422-003-0445-3Newman J.D., Wollberg Z. Responses of single neurons in the auditory cortex of squirrel monkeys to variants of a single call type. Exp. Neurol. 1973a. V. 40. P. 821–824. https://doi.org/10.1016/0014-4886(73)90116-7Newman J.D., Wollberg Z. Multiple coding of species-specific vocalizations in the auditory cortex of squirrel monkeys. Brain Res. 1973b. V. 54. P. 287–304. https://doi.org/10.1016/0006-8993(73)90050-4Penna M., Velásquez N.A., Bosc J. Dissimilarities in auditory tuning in midwife toads of the genus Alytes (Amphibia: Anura). Biol. J. Linnean Society. 2015. V. 116. P. 41–51. https://doi.org/10.1111/bij.12563Petkov C.I., Kayser C., Steudel T., Whittingstall K., Augath M., Logothetis N.K. A voice region in the monkey brain. Nat Neurosci. 2008. V. 1. P. 367–374. https://doi.org/10.1038/nn2043Petkov C.I., Kayser C., Steudel T., Whittingstall K., Augath M., Logothetis N.K. A voice region in the monkey brain. Nat. Neurosci. 2008. V. 1. P. 367–374. https://doi.org/10.1038/nn2043Philibert B., Laudanski J., Edeline J.-M. Auditory thalamus responses to guinea pig vocalizations: a comparison between rat and guinea pig. Hear Res. 2005. V. 209. P. 97–103. https://doi.org/10.1016/j.heares.2005.07.004Peterson D.C., Wenstrup J.J. Selectivity and persistent firing responses to social vocalizations in the basolateral amygdala. Neuroscience. 2012. V. 17. P. 154–171. https://doi.org/10.1016/j.neuroscience.2012. 04.069Plakke B., Diltz M.D., Romanski L.M. Coding of vocalizations by single neurons in ventrolateral prefrontal cortex. Hear. Res. 2013. V. 305. P. 135–143. https://doi.org/10.1016/j.heares.2013.07.011Poremba A., Bigelow J., Rossi B. Processing of communication sounds: contributions of learning, memory, and experience. Hear. Res. 2013. V. 305. P. 31–34. https://doi.org/10.1016/j.heares.2013.06.005Portfors C.V., Roberts P.D., Jonson K. Over-representation of species-specific vocalizations in the awake mouse inferior colliculus. Neuroscience 2009. V. 162. P. 486–500. https://doi.org/10.1016/j.neuroscience.2009.04.056Portfors C.V., Roberts P. D, Jonson K. Over-representation of species-specific vocalizations in the awake mouse inferior colliculus. Neuroscience 2009. V. 162. P. 486–500. https://doi.org/10.1016/j.neuroscience.2009.04.056Potter H.D. Patterns of acoustically evoked discharges of neurons in the mesencephalon of the bullfrog. J. Neurophysiol. 1965. V. 28. № 6. P. 1155–1184. https://doi.org/10.1152/jn.1965.28.6.1155Qin L., Wang J.Y., Sato Y. Representations of cat meows and human vowels in the primary auditory cortex of awake cats. J. Neurophysiol. 2008. V. 99. P. 2305–2319. https://doi.org/10.1152/jn.01125.2007Rauschecker J.P. Parallel processing in the auditory cortex of primates. Audiol. Neurotol. 1998. V. 3. № 2-3. P. 86–103. https://doi.org/10.1159/000013784Recanzone G.H. Representation of conspecific vocalizations in the core and belt areas of the auditory cortex in the alert macaque monkey. J. Neurosci. 2008. V. 28. P. 13184–13193. https://doi.org/10.1523/JNEUROSCI.3619-08.2008Remedios R., Logothetis N.K. Kayser C. An auditory region in the primate insular cortex responding preferentially to vocal communication sounds. J. Neurosci. 2009. V. 29. P. 1034–1045. https://doi.org/10.1523/JNEUROSCI.4089-08.2009Roberts P.D., Portfors C.V. Responses to social vocalizations in the dorsal cochlear nucleus of mice. Front. Syst. Neurosci. 2015. V. 9. P. 172–175. https://doi.org/10.3389/fnsys.2015.00172Roberts P.D., Portfors C.V. Responses to social vocalizations in the dorsal cochlear nucleus of mice. Front. Syst. Neurosci. 2015. V. 9. Р.172–177. https://doi.org/10.3389/fnsys.2015.00172Romanski L.M., Averbeck B.B. The primate cortical auditory system and neural representation of conspecific vocalizations. Ann. Rev. Neurosci. 2009. V. 32. P. 315–346. https://doi.org/10.1146/annurev.neuro.051508.135431Romanski L.M., Averbeck B.B., Diltz M. Neural representation of vocalizations in the primate ventrolateral prefrontal cortex J. Neurophysiol. 2005. V. 93. P. 734–747. https://doi.org/10.1152/jn.00675.2004Roy S., Zhao L., Wang X. Distinct neural activities in premotor cortex during natural vocal behaviors in a New World primate. The common marmoset (Callithrix jacchus). J. Neurosci. 2016. V. 36. P. 12168–12179. https://doi.org/10.1523/JNEUROSCI.1646-16.2016Royer J., Huetz C., Occelli F., Cancela J.M., Edeline J.M. Enhanced discriminative abilities of auditory cortex neurons for pup calls despite reduced evoked responses in c57bl/6 mother mice. Neuroscience. 2021. V. 453. P. 1–16. https://doi.org/10.1016/j.neuroscience.2020.11.031Royer J., Huetz C., Occelli F., Cancela J.M., Edeline J.M. Enhanced discriminative abilities of auditory cortex neurons for pup calls despite reduced evoked responses in c57bl/6 mother mice. Neuroscience. 2021. V. 453. P. 1–16. https://doi.org/10.1016/j.neuroscience.2020.11.031.Sangiamo D.T., Warren M.R., Neunuebel J.P. Ultrasonic signals associated with different types of social behavior of mice. Nature Neurosci. 2020. V. 23. P. 411–422. https://doi.org/10.1038/s41593-020-0584-zSadagopan S., Wang X. Nonlinear spectrotemporal interactions underlying selectivity for complex sounds in auditory cortex. J. Neurosci. 2009. V. 29. № 36. P. 11192–11202. https://doi.org/10.1038/s41593-020-0584-zSchnupp. J.W.H., Hall T.M. et al. Plasticity of temporal pattern codes for vocalization stimuli in primary auditory cortex. J. Neurosci. 2006. V. 26. № 18. P. 4785–4795. https://doi.org/10.1523/jneurosci.4330-05.2006Schnupp. J.W H., Hall T.M. et al. Plasticity of temporal pattern codes for vocalization stimuli in primary auditory cortex. J. Neurosci. 2006. V. 26. № 18. P. 4785–4795. https://doi.org/10.1523/jneurosci.4330-05.2006Souffi S., Lorenzi C., Varnet L., Huetz C., Edeline J.M. Noise-sensitive but more precise subcortical representations coexist with robust cortical encoding of natural vocalizations. J. Neurosci. 2020. V. 40. № 27. P. 5228–5246. https://doi.org/10.1523/JNEUROSCI.2731-19.2020Sovijarvi A.R.A. Detection of natural complex sounds by cells in the primary auditory cortex of the cat. Acta Physiol. Scand. 1975. V. 93. P. 318–335. https://doi.org/10.1111/j.1748-1716.1975.tb05821.xSteinschneider M., Nourski K.V., Fishman Y.I. Representation of speech in human auditory cortex: is it special? Hear Res. 2013. V. 305. P. 57–73. https://doi.org/10.1016/j.heares.2013.05.013Suta J., Kvasiniak E., Popelar J., Syka J. Representation of species-specific vocalizations in the inferior colliculus of the guinea pig. J. Neurophysiol. 2003. V. 90. P. 3794–3808. https://doi.org/10.1152/JN.01175.2002Suta D., Popelar J., Kvasniak E., Syka J. Representation of species-specific vocalizations in the medial geniculate body of the guinea pig. Exp. Brain Res. 2007. V. 183. P. 377–388. https://doi.org/10.1007/s00221-007-1056-3Syka J., Suta D., Popelar J. Responses to species-specific vocalizations in the auditory cortex of awake and anesthetized guinea pigs. Hear. Res. 2005. V. 206. P. 177–184. https://doi.org/10.1016/j.heares.2005.01.013Tanaka H., Taniguchi I. Responses of medial geniculate neurons to species-specific vocalized sounds in the guinea pig. Jap. J. Physio. 1991. V. 41. № 6. P. 817–829. https://doi.org/10.2170/jjphysiol.41.817Tanaka H., Taniguchi I. Responses of medial geniculate neurons to species-specific vocalized sounds in the guinea pig. Jap. J. Physio. 1991. V. 41. № 6. P. 817–829. https://doi.org/10.2170/jjphysiol.41.817.Tian B., Reser D., Durham A., Kustov A., Rauschecker J.P. Functional specialization in rhesus monkey auditory cortex. Science. 2001. V. 292. P. 290–293. https://doi.org/10.2307/3082738Tonini J.F.R., Provete D.B., Maciel N.M., Morais A.R., Goutte S., Toledo L.F., Pyron R.A. Allometric escape from acoustic constraints is rare for frog calls. Ecology Evol. 2020. V. 10. P. 3686–3695. https://doi.org/10.1002/ece3.6155Velásquez N.A., Valdes J.L., Vasquez R.A., Penna M. Lack of phonotactic preferences of female frogs and its consequences for signal evolution. Behav. Process. 2015. V. 118. P. 76–84. https://doi.org/10.1016/j.beproc.2015.06.001Velásquez N.A., Moreno-Gómez F.N., Brunett E., Penna M. The acoustic adaptation hypothesis in a widely distributed South American frog: Southernmost signals propagate better. Scientific Reports. 2018. V. 8. Article 6990. https://doi.org/10.1038/s41598-018-25359-yVelásquez N.A., Moreno-Gómez F.N., Brunett E., Penna M. The acoustic adaptation hypothesis in a widely distributed South American frog: Southernmost signals propagate better. Scientific Reports.2018. V. 8. P. 6990. https://doi.org/10.1038/s41598-018-25359-yVergne A.L., Thierry A., Martin S., Mathevon N. Acoustic communication in crocodilians: Information encoding and species specificity of juvenile calls. Animal Cognition. 2012. V. 15. P. 1095–1109. https://doi.org/10.1007/s1007 1-012-0533-7Wallace M.N., Palmer A.R. Functional subdivisions in low-frequency primary auditory cortex (A1). Exp. Brain Res. 2009. V. 194. P. 395–408. https://doi.org/10.1007/s00221-009-1714-8Wallace M.N., Shackleton T.M., Anderson L.A., Palmer A.R. Representation of the purr call in the guinea pig primary auditory cortex. Hear Res. 2005. V. 204. P. 115–126. https://doi.org/10.1016/j.heares.2005.01.007Wang X., Wang D., Wu X., Wang C., Wang R., Xia T. Response specificity to advertisement vocalization in the Chinese alligator (Alligator sinensis). Ethology. 2009. V. 115. P. 832–839. https://doi.org/10.1111/j.1439-0310.2009.01671.xWilczynski W., Ryan M.J. The behavioral neuroscience of anuran social signal processing. Curr. Opin. Neurobiol. 2010. V. 20. № 6. P. 754–763. https://doi.org/10.1016/j.conb.2010.08.021Wilczynski W., Keddy-Hector A.C., Ryan M.J. Call patterns and basilar papilla tuning in cricket frogs. 1. Differences among populations and between sexes. Brain Behavior. Evol. 1992. V. 39. № 4. P. 229–237. https://doi.org/10.1159/000114120Winter P., Funkenstein H.H. The effect of species-specific vocalization on the discharge of auditory cortical cells in the awake squirrel monkey (Saimiri sciureus). Exp. Brain Res. 1973. V. 18. P. 489–504. https://doi.org/10.1007/BF00234133Winter P., Funkenstein H.H. The effect of species-specific vocalization on the discharge of auditory cortical cells in the awake squirrel monkey (Saimiri sciureus). Exp. Brain Res. 1973. V. 18. P. 489–504. https://doi.org/10.1007/BF00234133.Wollberg Z., Newman J.D. Auditory cortex of squirrel monkey: response patterns of single cells to species-specific vocalizations. Science. 1972. V. 175. P. 212–214. https://doi.org/10.2307/1733054Zhao L., Wang J., Yang Y., Zhu B., Brauth S.E., Tang Y., Cui J. An exception to the matched filter hypothesis: A mismatch of male call frequency and female best hearing frequency in a torrent frog. Ecol. Evol. 2016. V. 7. P. 419–428. https://doi.org/10.1002/ece3.2621Ziegler L., Arim M., Narins P. Linking amphibian call structure to the environment: The interplay between phenotypic flexibility and individual attributes. Behav. Ecol. 2011. V. 22. P. 520–526. https://doi.org/10.1093/beheco/arr011