兽类学报 ›› 2025, Vol. 45 ›› Issue (6): 743-752.DOI: 10.16829/j.slxb.2015-1084
收稿日期:2025-04-08
接受日期:2025-05-26
出版日期:2025-11-30
发布日期:2025-12-03
通讯作者:
叶欢,罗金红
作者简介:周诗雨 (2002- ),女,硕士研究生,主要从事神经行为学研究基金资助:
Shiyu ZHOU, Di ZHANG, Huan YE(
), Jinhong LUO(
)
Received:2025-04-08
Accepted:2025-05-26
Online:2025-11-30
Published:2025-12-03
Contact:
Huan YE, Jinhong LUO
摘要:
蝙蝠作为唯一具有动力飞行能力的哺乳动物,通过回声定位和飞行行为的相互协同,占据了重要的夜空生态位,成为了生态分布最丰富的哺乳动物之一。多年来,基于电生理技术的神经机理研究,揭示了蝙蝠回声定位能力潜在的神经基础。本文以蝙蝠电生理研究的不同行为范式为主线,首先比较了不同行为范式下神经电生理研究的优缺点:(1) 麻醉状态:适用于特定脑区神经元功能的解析,但受限于麻醉药物对神经活动的干扰;(2) 头部固定清醒状态:能在清醒状态下快速高效记录高信噪比的神经信号,但蝙蝠的行为自由受限;(3) 自由活动状态:结合电极植入手段,能最真实地反映自由行为中的神经活动,但技术存在挑战。此外,本文系统地梳理了3种主要行为范式下取得的关键研究发现,其中发声蝙蝠神经元活动的记录揭示了回声定位高度依赖听觉通路和发声控制通路的协调整合。近年来,光遗传、化学遗传和双光子钙成像等新技术的应用,开拓了蝙蝠回声定位神经机制研究的新思路;未来的研究需要结合新兴技术,更全面系统地揭示蝙蝠回声定位的神经基础。
中图分类号:
周诗雨, 张迪, 叶欢, 罗金红. 蝙蝠回声定位听觉基础的电生理研究范式及其进展[J]. 兽类学报, 2025, 45(6): 743-752.
Shiyu ZHOU, Di ZHANG, Huan YE, Jinhong LUO. Electrophysiological recording paradigms and advances in the study of auditory basis of echolocation in bats[J]. ACTA THERIOLOGICA SINICA, 2025, 45(6): 743-752.
图1 蝙蝠捕食过程中回声定位声波示意图. 上图:典型调频蝙蝠——大棕蝠 (A) 和典型恒频-调频蝙蝠——马铁菊头蝠 (B) 在捕食声境下的回声定位示意图,及植被反射的杂波;下图:叫声和回声声谱示意图,包括搜索阶段和靠近阶段
Fig. 1 Schematic representations of echolocation calls and the acoustic environment of bats. Upper pannels: echolocation processes of typical frequency-modulated bats - big brown bat (A) and the constant frequency-frequency modulation bats - greater horseshoe bat (B) during foraging. Bottom panels: diagrams of spectrograms for calls and echoes, including search phase and approach phase respectively
图2 基于不同电生理记录范式下取得的蝙蝠回声定位听觉机制的代表性成果. A:蝙蝠电生理记录状态的行为范式示意图;B:蝙蝠电生理记录状态的行为范式的部分文献时间线及重要结论总结
Fig. 2 Representative findings of the auditory mechanisms for bat echolocation revealed by different electrophysiological recording methods. A: Schematic diagram of behavioral paradigms of auditory electrophysiological recording in bat echolocation; B: Timeline of some studies and summary of key findings for auditory electrophysiological recording in bat echolocation
| Andoni S, Li N, Pollak G D. 2007. Spectrotemporal receptive fields in the inferior colliculus revealing selectivity for spectral motion in conspecific vocalizations [J]. Journal of Neuroscience, 27 (18): 4882-4893. | |
| Bartenstein S K, Gerstenberg N, Vanderelst D, Peremans H, Firzlaff U. 2014. Echo‑acoustic flow dynamically modifies the cortical map of target range in bats [J]. Natature Communications, 5 (1): 4668. DOI: 10.1038/ncomms5668 . | |
| Beetz M J, Hechavarría J C. 2022. Neural processing of naturalistic echolocation signals in bats [J]. Frontiers in Neural Circuits, 16: 899370.DOI: 10.3389/fncir.2022.899370 . | |
| Beetz M J, Hechavarría J C, Kössl M. 2016a. Temporal tuning in the bat auditory cortex is sharper when studied with natural echolocation sequences [J]. Scientific Reports, 6 (1): 29102.DOI: 10.1038/srep29102 . | |
| Beetz M J, Hechavarría J C, Kössl M. 2016b. Cortical neurons of bats respond best to echoes from nearest targets when listening to natural biosonar multi‑echo streams [J]. Scientific Reports, 6 (1): 35991. DOI: 10.1038/srep35991 . | |
| Beetz M J, Kordes S, García‑Rosales F, Kössl M, Hechavarría J C. 2017. Processing of natural echolocation sequences in the inferior colliculus of Seba’s fruit eating bat, Carollia perspicillata [J]. ENEURO, 4 (6): 0314-17.2017. DOI: 10.1523/ENEURO.0314-17.2017 . | |
| Bharioke A. 2022. General anesthesia globally synchronizes activity selectively in layer 5 cortical pyramidal neurons [J]. Neuron, 110 (12): 2024-2040. | |
| Casseday J, Ehrlich D, Covey E. 1994. Neural tuning for sound duration: role of inhibitory mechanisms in the inferior colliculus [J]. Science, 264 (5160): 847-849. | |
| Church M W, Gritzke R. 1987. Effects of ketamine anesthesia on the rat brain‑stem auditory evoked potential as a function of dose and stimulus intensity [J]. Electroencephalography and Clinical Neurophysiology, 67 (6): 570-583. | |
| Covey E. 2005. Neurobiological specializations in echolocating bats [J]. The Anatomical Record Part A: Discoveries in Molecular, Cellular, and Evolutionary Biology: An Official Publication of the American Association of Anatomists, 287 (1): 1103-1116. | |
| Covey E, Casseday J H. 1999. Timing in the auditory system of the bat [J]. Annual Review of Physiology, 61 (1): 457-476. | |
| Cui J, Zhu B, Fang G, Smith E, Brauth S E, Tang Y. 2017. Effect of the level of anesthesia on the auditory brainstem response in the Emei Music Frog (Babina daunchina) [J]. PLoS ONE, 12 (1): e0169449. DOI: 10.1371/journal.pone.0169449 . | |
| Cui Z, Yu C, Wang X, Yin K, Luo J. 2024. Prevalent harmonic interaction in the bat inferior colliculus [J]. Journal of Neuroscience, 44 (49): e0916242024. DOI: 10.1523/JNEUROSCI.0916-24.2024 . | |
| Dalland J I. 1965. Hearing sensitivity in bats [J]. Science, 150 (3700): 1185-1186. | |
| Diebold C A, Lawlor J, Allen K, Capshaw G, Humphrey M G, Leon D C D, Kuchibhotla K V, Moss C F. 2024. Rapid sensorimotor adaptation to auditory midbrain silencing in free‑flying bats [J]. Current Biology, 34 (23): 5507-5517. | |
| Ehrlich D, Casseday J H, Covey E. 1997. Neural tuning to sound duration in the inferior colliculus of the big brown bat, Eptesicus fuscus [J]. Journal of Neurophysiology, 77 (5): 2360-2372. | |
| Eliav T, Maimon S R, Aljadeff J, Tsodyks M, Ginosar G, Las L, Ulanovsky N. 2021. Multiscale representation of very large environments in the hippocampus of flying bats [J]. Science, 372 (6545): eabg4020. DOI: 10.1126/science.abg4020 . | |
| Feng A S, Simmons J A, Kick S A. 1978. Echo detection and target ranging neurons in the auditory system of the bat Eptesicus fuscus [J]. Science, 202 (4368): 645-648. | |
| Fenzl T, Schuller G. 2005. Echolocation calls and communication calls are controlled differentially in the brainstem of the bat Phyllostomus discolor [J]. BMC BGiology, 3: 1-12. | |
| Fuzessery Z, Razak K, Williams A. 2011. Multiple mechanisms shape selectivity for FM sweep rate and direction in the pallid bat inferior colliculus and auditory cortex [J]. Journal of Comparative Physiology A, 197: 615-623. | |
| Fuzessery Z M. 1994. Response selectivity for multiple dimensions of frequency sweeps in the pallid bat inferior colliculus [J]. Journal of Neurophysiology, 72 (3): 1061-1079. | |
| Fuzessery Z M, Pollak G D. 1984. Neural mechanisms of sound localization in an echolocating bat [J]. Science, 225 (4663): 725-728. | |
| Galambos R. 1942. Cochlear potentials elicited from bats by supersonic sounds [J]. The Journal of the Acoustical Society of America, 14 (1): 41-49. | |
| Galambos R. 1941. Cochlear potentials from the bat [J]. Science, 93 (2409): 215.DOI: 10.1126/science.93.2409.215 . | |
| García‑Rosales F, López‑Jury L, González‑Palomares E, Wetekam J, Cabral‑Calderín Y, Kiai A, Kössl M, Hechavarría J C. 2022. Echolocation‑related reversal of information flow in a cortical vocalization network [J]. Nature Communications, 13 (1): 3642. DOI: 10.1038/s41467-022-31230-6 . | |
| Geipel I, Lattenkamp E Z, Dixon M M, Wiegrebe L, Page R A. 2021. Hearing sensitivity: an underlying mechanism for niche differentiation in gleaning bats [J]. Proceedings of the National Academy of Sciences, 118 (36): e2024943118. DOI: 10.1073/pnas.2024943118 . | |
| Gosselin E, Bagur S, Bathellier B. 2024. Massive perturbation of sound representations by anesthesia in the auditory brainstem [J]. Science Advances, 10 (42): eado2291. DOI: 10.1126/sciadv.ado2291 . | |
| Gould E. 1970. Echolocation and communication in bats [J]. Fondren Science Series, 1 (11): 9. | |
| Griffin D R. 1944. Echolocation by blind men, bats, and radar [J]. Science, 100 (2609): 589-590. | |
| Griffin D R, Galambos R. 1941. The sensory basis of obstacle avoidance by flying bats [J]. Journal of Experimental Zoology, 86: 481-506. | |
| Grinnell A D. 1963. The neurophysiology of audition in bats: intensity and frequency parameters [J]. The Journal of Physiology, 167 (1): 38. DOI: 10.1113/jphysiol.1963.sp007132 . | |
| Hariharan S, Palomares E G, Babl S S, López‑Jury L, Hechavarria J C. 2024. Cerebellar activity predicts vocalization in fruit bats [J]. Current Biology, 34 (21): 5112-5119. | |
| Henson O W, Pollak G D. 1972. A technique for chronic implantation of electrodes in the cochleae of bats [J]. Physiology & Behavior, 8 (6): 1185-1187. | |
| Henson O W, Pollak G D, Kobler J B, Henson M M, Goldman L J. 1982. Cochlear microphonic potentials elicited by biosonar signals in flying bats, Pteronotus p. parnellii [J]. Hearing Research, 7 (2): 127-147. | |
| Henson O W, Schuller G, Vater M. 1985. A comparative study of the physiological properties of the inner ear in Doppler shift compensating bats (Rhinolophus rouxi and Pteronotus parnellii) [J]. Journal of Comparative Physiology A, 157: 587-597. | |
| Herkt K M B, Barnikel G, Skidmore A K, Fahr J. 2016. A high‑resolution model of bat diversity and endemism for continental Africa [J]. Ecological Modelling, 320: 9-28. | |
| Jacobs D S, Bastian A. 2016. Predator-Prey Interactions: Co-evolution Between Bats and Their Prey [M]. Cham: Springer, 13-30. | |
| Kothari N B, Wohlgemuth M J, Moss C F. 2018. Dynamic representation of 3D auditory space in the midbrain of the free‑flying echolocating bat [J]. Elife, 7: e29053. DOI: 10.7554/eLife.29053 . | |
| Kurz A. 2001. Effects of anaesthesia on thermoregulation [J]. Current Anaesthesia & Critical Care, 12 (2): 72-78. | |
| Lattenkamp E Z, Nagy M, Drexl M, Vernes S C, Wiegrebe L, Knörnschild M. 2021. Hearing sensitivity and amplitude coding in bats are differentially shaped by echolocation calls and social calls [J]. Proceedings of the Royal Society B, 288 (1942): 20202600. DOI: 10.1098/rspb.2020.2600 . | |
| Lawlor J, Wohlgemuth M J, Moss C F, Kuchibhotla K V. 2025. Spatially clustered neurons in the bat midbrain encode vocalization categories. Nature Neuroscience, 28: 1038-1047. | |
| Leroy S A, Wenstrup J J. 2000. Spectral integration in the inferior colliculus of the mustached bat [J]. Journal of Neuroscience, 20 (22): 8533-8541. | |
| Liu M L, Wang C L, Huo L F, Cao J, Mao X G, He Z Q, Hu C X, Sun H J, Deng W J, He W Y, Chen Y F, Gu M F, Liao J Y, Guo N, He X Y, Wu Q, Chen J K, Zhang L B, Wang X Q, Shang C P, Dong J. 2024. Complexin‑1 enhances ultrasound neurotransmission in the mammalian auditory pathway [J]. Nature Genetics, 56 (7): 1503-1515. | |
| Long G R, Schnitzler H U. 1975. Behavioural audiograms from the bat, Rhinolophus ferrumequinum [J]. Journal of Comparative Physiology, 100 (3): 211-219. | |
| Luo J, Macias S, Ness T V, Einevoll G T, Zhang K, Moss C F. 2018. Neural timing of stimulus events with microsecond precision [J]. PLoS Biology, 16 (10): e2006422. DOI: 10.1371/journal.pbio.2006422 . | |
| Luo J, Simmons A M, Beck Q M, Macías S, Moss C F, Simmons J A. 2019. Frequency‑modulated up‑chirps produce larger evoked responses than down‑chirps in the big brown bat auditory brainstem [J]. The Journal of the Acoustical Society of America, 146 (3): 1671-1684. | |
| Macias S, Bakshi K, Troyer T, Smotherman M. 2022. The prefrontal cortex of the Mexican free‑tailed bat is more selective to communication calls than primary auditory cortex [J]. Journal of Neurophysiology, 128 (3): 634-648. | |
| Macias S, Luo J, Moss C F. 2018. Natural echolocation sequences evoke echo‑delay selectivity in the auditory midbrain of the FM bat, Eptesicus fuscus [J]. Journal of Neurophysiology, 120 (3): 1323-1339. | |
| Metzner W. 1989. A possible neuronal basis for doppler‑shift compensation in echo‑locating horseshoe bats [J]. Nature, 341 (6242): 529-532. | |
| Mittmann D H, Wenstrup J J. 1995. Combination‑sensitive neurons in the inferior colliculus [J]. Hearing Research, 90 (1-2): 185-191. | |
| Moss C F, Bohn K, Gilkenson H, Surlykke A. 2006. Active listening for spatial orientation in a complex auditory scene [J]. PLoS Biology, 4 (4): 615-626. | |
| Moss C F, Sinha S R. 2003. Neurobiology of echolocation in bats. Current Opinion in Neurobiology, 13 (6): 751-758. | |
| Nelson M E, MacIver M A. 2006. Sensory acquisition in active sensing systems [J]. Journal of Comparative Physiology A, 192: 573-586. | |
| Neuweiler G, Schuller G, Schnitzler H U. 1971. On‑ and off‑responses in the inferior colliculus of the Greater Horseshoe bat to pure tones [J]. Zeitschrift für Vergleichende Physiologie, 74: 57-63. | |
| Neuweiler G, Singh S, Sripathi K. 1984. Audiograms of a South Indian bat community [J]. Journal of Comparative Physiology A, 154: 133-142. | |
| Pollak G, Marsh D, Bodenhamer R, Souther A. 1977. Echo detecting characteristics of neurons in inferior colliculus of unanesthetized bats [J]. Science, 196 (4290): 675-678. | |
| Portfors C V, Wenstrup J J. 1999. Delay‑tuned neurons in the inferior colliculus of the mustached bat: Implications for analyses of target distance [J]. Journal of Neurophysiology, 82 (3): 1326-1338. | |
| Razak K A, Fuzessery Z M. 2008. Facilitatory mechanisms underlying selectivity for the direction and rate of frequency modulated sweeps in the auditory cortex [J]. Journal of Neuroscience, 28 (39): 9806-9816. | |
| Salles A, Loscalzo E, Montoya J, Mendoza R, Boergens K M, Moss C F. 2024. Auditory processing of communication calls in interacting bats [J]. Iscience, 27 (6): 109872. DOI: 10.1016/j.isci.2024.109872 . | |
| Schuller G. 1979. Vocalization influences auditory processing in collicular neurons of the CF‑FM‑bat,Rhinolophus ferrumequinum [J]. Journal of Comparative Physiology, 132: 39-46. | |
| Schuller G, Fischer S, Schweizer H. 1997. Significance of the paralemniscal tegmental area for audio‑motor control in the moustached bat, Pteronotus p. parnellii: the afferent and efferent connections of the paralemniscal area [J]. European Journal of Neuroscience, 9 (2): 342-355. | |
| Schuller G, Pollak G. 1979. Disproportionate frequency representation in the inferior colliculus of doppler‑compensating greater horseshoe bats: evidence for an acoustic fovea [J]. Journal of Comparative Physiology, 132: 47-54. | |
| Schuller G, Radtke‑S‑chuller S. 1990. Neural control of vocalization in bats: mapping of brainstem areas with electrical microstimulation eliciting species‑specific echolocation calls in the rufous horseshoe bat [J]. Experimental Brain Research, 79: 192-206. | |
| Sinha S R, Moss C F. 2007. Vocal premotor activity in the superior colliculus [J]. Journal of Neuroscience, 27 (1): 98-110. | |
| Suga N. 2018. Specialization of the auditory system for the processing of bio‑sonar information in the frequency domain: mustached bats [J]. Hearing Research, 361: 1-22. DOI: 10.1016/j.heares.2018.01.012 . | |
| Suga N. 2015. Neural processing of auditory signals in the time domain: Delay‑tuned coincidence detectors in the mustached bat [J]. Hearing Research, 324: 19-36. | |
| Suga N. 1969. Classification of inferior collicular neurones of bats in terms of responses to pure tones, frequency‑modulated sounds and noise bursts [J]. The Journal of Physiology, 200 (2): 555-574. | |
| Suga N. 1964. Single unit activity in cochlear nucleus and inferior colliculus of echo‑locating bats [J]. The Journal of Physiology, 172 (3): 449-474. | |
| Suga N, O’Neill W, Manabe T. 1978. Cortical neurons sensitive to combinations of information‑bearing elements of biosonar signals in the mustache bat [J]. Science, 200: 778-781. | |
| Suga N, O’Neill W E, Manabe T. 1979. Harmonic‑sensitive neurons in the auditory cortex of the mustache bat [J]. Science, 203 (4377): 270-274. | |
| Suga N, Schlegel P. 1972. Neural attenuation of responses to emitted sounds in echolocating bats [J]. Science, 177 (4043): 82-84. | |
| Suga N, Shimozawa T. 1974. Site of neural attenuation of responses to self vocalized sounds in echolocating bats [J]. Science, 183 (4130): 1211-1213. | |
| Ulanovsky N, Moss C F. 2008. What the bat’s voice tells the bat’s brain [J]. Proceedings of the National Academy of Sciences, 105 (25): 8491-8498. | |
| Valentine D E, Moss C F. 1997. Spatially selective auditory responses in the superior colliculus of the echolocating bat [J]. The Journal of Neuroscience, 17 (5): 1720-1733. | |
| Van Looij M A J, Liem S S, Van Der Burg H, Van Der Wees J, De Zeeuw C I, Van Zanten B G A. 2004. Impact of conventional anesthesia on auditory brainstem responses in mice [J]. Hearing Research, 193 (1-2): 75-82. | |
| Weineck K, García‑Rosales F, Hechavarría J C. 2020. Neural oscillations in the fronto‑striatal network predict vocal output in bats [J]. PLoS Biology, 18 (3): e3000658. DOI: 10.1371/journal.pbio.3000658 . | |
| Wenstrup J J, Nataraj K, Sanchez J T. 2012. Mechanisms of spectral and temporal integration in the mustached bat inferior colliculus [J]. Frontiers in Neural Circuits, 6: 75.DOI: 10.3389/fncir.2012.00075 . | |
| Wenstrup J J, Portfors C V. 2011. Neural processing of target distance by echolocating bats: Functional roles of the auditory midbrain [J]. Neuroscience & Biobehavioral Reviews, 35 (10): 2073-2083. | |
| Wirthlin M E, Schmid T A, Elie J E, Zhang X, Kowalczyk A, Redlich R, Shvareva V A, Rakuljic A, Ji M B, Bhat N S, Kaplow I M. 2024. Vocal learning‑associated convergent evolution in mammalian proteins and regulatory elements [J]. Science, 383 (6690): eabn3263. DOI: 10.1126/science.abn3263 . | |
| Wohlgemuth M J, Luo J, Moss C F. 2016. Three‑dimensional auditory localization in the echolocating bat [J]. Current Opinion in Neurobiology, 41: 78-86. | |
| Wohlgemuth M J, Moss C F. 2016. Midbrain auditory selectivity to natural sounds [J]. Proceedings of the National Academy of Sciences, 113 (9): 2508-2513. | |
| Wohlgemuth M J, Kothari N B, Moss C F. 2018a. Functional organization and dynamic activity in the superior colliculus of the echolocating bat, Eptesicus fuscus [J]. The Journal of Neuroscience, 38 (1): 245-256. | |
| Wohlgemuth M J, Yu C, Moss C F. 2018b. 3D hippocampal place field dynamics in free‑flying echolocating bats [J]. Frontiers in Cellular Neuroscience, 12: 270. DOI: 10.3389/fncel.2018.00270 . | |
| Ye H, Cui Z, Liu Z, Qin X, Huang X, Bai Y, Luo J. 2025. Neural identification of self‑emitted vocalizations in the auditory midbrain of behaving bats [J]. Science China Life Sciences. (Accepted). | |
| 付子英, 唐佳, 陈其才. 2022. 综述与专论: 蝙蝠, 听觉和回声定位研究的模型动物 [J]. 生物化学与生物物理进展, 49: 883-896. | |
| 林洪军, 王磊, 冯江. 2014. 蝙蝠回声定位声波的可塑性及其生态适应 [J]. 兽类学报, 34 (3): 307-312. |
| No related articles found! |
| 阅读次数 | ||||||
|
全文 |
|
|||||
|
摘要 |
|
|||||
青公网安备 63010402000199号 青ICP备05000010号-2