声刺激时程和模式影响大蹄蝠下丘神经元的恢复周期

本文旨在探讨声刺激时程及模式参量对恒频-调频(constant frequency-frequency modulation,CF-FM)蝙蝠下丘(inferior colliculus,IC)神经元恢复周期的影响。实验选用5只听力正常的大蹄蝠为实验动物,采用不同时程或不同模式的双声刺激,记录IC神经元的反应和恢复周期。结果共记录到169个IC声敏感神经元。依据神经元恢复率达到50%时的双声刺激间隔(interpulse interval,IPI)将神经元恢复周期分为三种类型:快速恢复型(fast,F),50%IPI为0～15ms;短时恢复型(short,S),50%IPI为15.1～30ms;长时恢复型(long,L),50%IPI30ms。在2、5和7ms时程的CF声刺激下,神经元50%IPI平均值随声刺激时程的增加,分别为(30.2±27.6)、(39.9±29.1)和(49.4±34.7)ms,F和S型神经元比例逐渐下降,而L型神经元比例逐渐上升。当声刺激模式由2msCF声转变为2msFM声时,F、S和L三种类型神经元比例分别由32.3%、41.5%、26.2%转变为47.7%、24.6%、27.7%,平均恢复周期缩短,由(30.2±27.6)减至(23.9±19.0)ms(P0.05,n=65)。与7msCF声刺激相比,5+2msCF-FM声刺激使F型神经元比例上升(18.2%→29.1%),S型神经元(29.1%→27.3%)和L型神经元(52.7%→43.6%)比例下降,平均恢复周期缩短,由(49.4±34.7)减至(36.3±29.4)ms(P0.05,n=55)。结果提示,CF-FM蝙蝠回声定位信号中的CF和FM成分在蝙蝠导航和捕食过程中分别扮演不同的角色,其中终末相中的FM成分主要使F型神经元数量增多,平均恢复周期缩短。FM成分在蝙蝠靠近靶物的过程中发挥重要作用以快速处理高脉冲重复率回声信息,它有利于准确计算目标距离和识别目标表面质地。     

CF-FM蝙蝠听中枢神经元处理行为相关声信号的神经机制

蝙蝠具有高度发达的回声定位系统,能够准确地处理和整合不断变化环境中的声学参数,以保持最佳的生理和行为状态。这种行为的神经生理机制已经得到了广泛的研究。本文主要探究了CF-FM蝙蝠听觉中枢处理种属特异性声信号、共变参数、多普勒频移补偿信号及多谐波声信号的神经机制,可有助于了解回声定位蝙蝠处理行为相关声信号的神经策略。同时本文也提出将来可以CF-FM蝙蝠作为模式动物进行更深入的胞内研究。     

普氏蹄蝠下丘CF-CF联合敏感神经元的声反应

为了研究普氏蹄蝠(Hipposideros pratti)下丘(IC)中恒频-恒频(CF-CF)联合敏感神经元声反应特性,以及易化型和抑制型CF-CF联合敏感神经元在IC高频表征区神经元中所占的比例,实验记录了普氏蹄蝠IC神经元在不同频率和声强下的单声反应以及在不同延迟下的双声反应。本实验采用在体细胞内电生理技术从7只听力正常的蝙蝠上共获得77个IC声敏感神经元。所获得的数据经过处理并应用Sigma Plot 10.0软件作图。研究结果显示,77个神经元中37(48.1%)个为CF-CF联合敏感神经元,且多数为抑制型(24/37),少数为(13/37)易化型。实验结果说明普氏蹄蝠IC中既存在易化型也存在抑制型CF-CF联合敏感神经元,其中抑制型CF-CF联合敏感神经元比易化型所占比例更高。这些CF-CF联合敏感神经元有助于蝙蝠在巡航过程中处理回声信息时进行频谱和时相的整合。     

普氏蹄蝠下丘谐波内外神经元处理多普勒频移补偿信息的差异

为了探讨普氏蹄蝠下丘神经元在处理多普勒频移补偿后回声定位信号中的作用,实验采用双声刺激模式模拟蝙蝠不同飞行状态下产生多普勒频移补偿后的脉冲-回声对,即发声频率改变,回声频率维持恒定的情况下,研究下丘神经元对不同补偿值下的回声反应恢复率.结果发现:根据神经元在某一补偿值下对回声信号反应的恢复率是否超过70%,可将其分为具有选择性(S)和无选择性(NS)的两类神经元.且谐波内S神经元所占比例(68%)远超过非谐波内S神经元(39%).分析神经元的发放模式发现谐波内S神经元中相位型发放模式比例(44.3%)明显高于其他三种类型神经元.另外,虽然S和NS神经元的强度-潜伏期函数类型均以饱和型为主,但谐波内S神经元强度-潜伏期函数的最佳强度(best amplitude,BA)(95.3±14.0)dB SPL低于NS神经元的BA(104.1±10.2)d B SPL(P0.01),同时也低于非谐波内S神经元的BA(109.7±7.9)dB SPL(P0.01).以上实验结果表明,在下丘水平,神经元就已对多普勒频移补偿后回声定位信号的处理有了分工,集中在谐波内的S神经元通过提高对某一补偿值下回声信号反应的恢复率实现,对回声信息的精确编码,避免其他杂波干扰信息.同时,谐波内S神经元的发放模式和强度-潜伏期函数特点也满足其在复杂环境中精确声学成像的需求.     

大蹄蝠回声定位信号特征与下丘神经元频率调谐

采用超声监测仪录制超声信号和细胞外电生理记录下丘神经元的频率调谐曲线(frequency tuningcurqes,FTCs)的方法,探讨了大蹄蝠(Hipposideros armiger)回声定位信号与下丘(inferior colliculus,IC)神经元频率调谐之间的相关性.结果发现,大蹄蝠回声定位叫声为恒频-调频(consrant frequency-frequenevmodulated,CF-FM)信号,一般含有2-3个谐波,第二谐波为其主频,cF成分频率(Mean±SD,n=18)依次为:(33.3 4±0.2)、(66.5±0.3)、(99.4 4±0.5)kHz;电生理实验共获得72个神经元的频率调谐曲线,Q10-dB值的范围是0.5-95.4(9.2±14.6,rg=72),最佳频率(best frequency,BF)在回声定位主频附近的神经元具有尖锐的频率调谐特性.结果表明,大蹄蝠回声定位信号与下丘神经元频率调谐存在相关性,表现为最佳频率在回声定位信号主频附近的神经元频率调谐曲线的Q10-dB值较大,具有很强的频率分析能力.     

普氏蹄蝠下丘对回声定位信号恒频成分的群体加工

利用听觉诱发电位和计算机叠加平均技术研究了普氏蹄蝠下丘(Inferior colliculus,IC)500-4 000 μm 记录深度间,神经元群对3 个谐波恒频(Constant frequency,CF) 声刺激(CF1 -CF3 )的反应。结果显示,在蝙蝠回声定位信号CF 成分刺激下,其IC 的诱发电位包括2 -4 个波,在1 000 μm 以下的记录区域,3 种刺激均能诱发on-off 反应,on-反应的幅度均在3 000 μm 达最大之后减小(P < 0.001),而潜伏期则逐渐缩短(P < 0.001);CF2 能诱发大幅度的off-反应,而CF1 、CF3 诱发的off-反应幅度较小,随着记录深度的增加,CF2 (P <0. 001)的off-反应潜伏期逐渐缩短,而CF1 (P > 0. 05)和CF3 (P >0. 05)的潜伏期则无此单调性。结果表明神经元群体加工CF1 - CF3 的on-反应存在一致性变化,提示其对行为相关的声信号加工可能存在频率层间复杂的相互作用;对CF 信号加工的off-反应对主频附近声较敏感,提示其可能在恒频-调频蝙蝠的多普勒频移、捕获振翅昆虫信息或种间交流中起着某种作用。     

恒频-调频蝙蝠下丘神经元的恢复周期决定声脉冲跟随率

为探究恒频-调频蝙蝠下丘神经元恢复周期特点及其对声脉冲跟随率的影响,实验采用模拟的大蹄蝠(Hipposideros armiger)自然状态下的恒频-调频发声信号为声刺激,在5只听力正常的大蹄蝠上记录了下丘神经元的声反应和恢复周期(n = 93)．结果发现,根据神经元恢复率达50%时的双声刺激间隔(inter pulse interval,IPI),可将其分为长时恢复型(long recovery,LR;47.4%)、中等时间恢复型(moderate recovery,MR;35.1%)和短时恢复型(short recovery,SR;17.5%)．每种类型依据其恢复率随IPI增加而呈现的不同变化又可进一步分为单IPI反应区神经元,多IPI反应区神经元,以及单调IPI反应神经元．LR,MR和SR型神经元恢复率达50%时的平均IPI分别为(64.0 ± 24.8),(19.6 ± 5.8)和(7.1 ± 2.4) ms (P < 0.001),相对应的平均理论每秒声脉冲数分别为(18.2 ± 7.0),(55.4 ± 15.7)和(171.3 ± 102.9) Hz (P < 0.001)．结果提示,单IPI和多IPI反应区神经元具有特殊IPI反应特性,能对蝙蝠捕食和巡航期间所处的时相做出准确判断,而单调IPI反应神经元对IPI变化的敏感性较强,但时相判断性较差．另外LR,MR和SR型神经元恢复周期和理论脉冲跟随率的平均结果均能与这种蝙蝠回声定位期间3个时相的发声行为相匹配,且神经元恢复周期参与决定声脉冲跟随率,满足了蝙蝠巡航、捕食的行为学需要．     

综述与专论: 蝙蝠，听觉和回声定位研究的模型动物

科学家以蝙蝠为模式动物,从听觉、回声定位和生态适应与演化等方面开展了研究,取得了令人瞩目的成果。为适应回声定位,蝙蝠听觉系统的结构和功能产生了明显的特化。从外周到中枢形成了对声频率极为有序的表征,甚至在恒频-调频（constant frequency-frequency modulation,CF-FM）蝙蝠耳蜗形成了所谓的听觉凹,以及听皮质功能组构也模块化,成为了具有代表性的特化象征。神经元反应的潜伏期对蝙蝠不仅是基本特性,也是回声定位行为调控的一部分;研究发现,有较长潜伏期的神经元具有较尖锐的回声-延迟调谐特性,而较短潜伏期的神经元则有较宽的回声-延迟调谐特性。蝙蝠听神经元对频率调谐的精准度亦远胜于人类和其他非回声定位动物;而且,源于耳蜗听觉凹的传入在各级听中枢均显示出对回声定位信号第二谐波CF成分的过度表征,以满足对靶物回声多普勒频移探测的需要。时程是回声定位蝙蝠发声信号主动改变的参数之一,而时程调谐神经元则提供了一种编码声音时相特征的重要神经机制,匹配了对回声定位信号时相信息加工的需要。在多种回声定位蝙蝠的听中枢还发现,有回声-延迟调谐神经元,它们不仅能对靶物距离进行调谐,而且...     

普氏蹄蝠下丘谐波主频神经元的时程选择性

为探讨下丘(Inferior colliculus,IC)回声定位信号主频范围内的神经元的时程选择性,在自由声场刺激条件下,我们在4 只普氏蹄蝠的IC 采用不同时程的声刺激,研究了神经元的时程选择性。通过在体细胞外记录,共获得56 个声敏感下丘神经元,其记录深度、最佳频率和最小阈值的范围分别为1547 - 3967 (2878. 9 ±629.1)μm,20 -68 (49.0 ± 11. 1)kHz 和36.5 -95. 5 (59. 8 ±13. 0)dB SPL。根据所记录到的下丘神经元对不同时程的声刺激的反应,即对不同时程的选择性(Duration selectivity),将其分为6 种类型:短通型(Short-pass,SP,n = 11/56)、带通型(Band-pass,BP,n = 1/56)、长通型(Long-pass,LP,n = 5 /56)、反带通型(Band-reject,BR,n = 3 /56)、多峰型(Multi-peak,MP,n =6 /56)和全通型(All-pass,AP,n =30 /56)或非时程选择型(Nonduration-selective,NDS)。通过比较普氏蹄蝠下丘谐波主频内和主频外神经元的时程选择性,我们发现处于回声定位信号主频范围内神经元(n =32)比主频外神经元(n = 24)具有更短的最佳时程和更高的时程选择性。结果提示,在普氏蹄蝠回声定位过程中谐波主频内神经元较谐波主频外神经元发挥了更为重要的作用。     

高度杂波空间中 CF-FM 蝙蝠下丘回声定位的神经机制

蝙蝠是回声定位的专家。对于在高度杂波空间中捕食的CF-FM蝙蝠,面临着如何从发声和众多由背景环境物体反射的杂波回声中分辨和判断来自靶物的回声所携带信息的问题。已有研究表明,CF-FM蝙蝠可通过发出复杂成分的声脉冲,并通过听中枢的时相和频率整合来处理杂波环境下发声-回声对中包含的靶物距离和相对移动速度的信息。就以上方面在听中脑下丘的神经机制进行概述,以促进人们对听中枢在复杂听环境下对回声定位信号加工原理的认识。     

Sound duration and sound pattern affect the recovery cycles of inferior collicular neurons in leaf-nosed bat, Hipposideros armiger

The effects of sound duration and sound pattern on the recovery cycles of inferior collicular (IC) neurons in constant frequency-frequency modulation (CF-FM) bats were explored in this study. Five leaf-nosed bats, Hipposideros armiger (4 males, 1 female, 43-50 g body weight), were used as subjects. The extracellular responses of IC neurons to paired sound stimuli with different duration and patterns were recorded, and the recovery was counted as the ratio of the second response to the first response. Totally, 169 sound-sensitive IC neurons were recorded in the experiment. According to the interpulse interval (IPI) of paired sounds when neurons reached 50% recovery (50% IPI), the recovery cycles of these IC neurons were classified into 3 types: fast recovery (F, the 50% IPI was less than 15 ms), short recovery (S, the 50% IPI was between 15.1 and 30 ms) and long recovery (L, the 50% IPI was more than 30 ms). When paired CF stimuli with 2 ms duration was used, the ratio of F neurons was 32.3%, and it decreased to 18.1% and 18.2% respectively when 5 and 7 ms CF stimuli were used. The ratios of S and L neurons were 41.5%, 33.7%, 29.1% and 26.2%, 48.2%, 52.7% respectively when 2, 5 and 7 ms CF stimuli were used. The average 50% IPI determined after stimulation with paired 2 ms, 5 ms and 7 ms CF sounds were (30.2 ± 27.6), (39.9 ± 29.1) and (49.4 ± 34.7) ms, respectively, and the difference among them was significant (P< 0.01). When the stimuli of paired 2 ms CF sounds were shifted to paired 2 ms FM sounds, the proportion of F, S and L neurons changed from 32.3%, 41.5%, 26.2% to 47.7%, 24.6%, 27.7%, respectively, and the average 50% IPI decreased from (30.2 ± 27.6) to (23.9 ± 19.0) ms (P< 0.05, n = 65). When paired 5+2 ms CF-FM pulses were used instead of 7 ms CF sounds, the proportion of F, S and L neurons changed from 18.2%, 29.1%, 52.7% to 29.1%, 27.3%, 43.6%, respectively, and the average 50% IPI decreased from (49.4 ± 34.7) to (36.3 ± 29.4) ms (P< 0.05, n = 55). All these results suggest that the CF and FM components in echolocation signal of CF-FM bats play different roles during bats' hunting and preying on. The FM component of CF-FM signal presenting in the terminal phase can increase the number of F type neurons and decrease the recovery cycles of IC neurons for processing high repetition echo information, which ensures the bat to analyze the target range and surface texture more accurately.     

The role of prey-generated sounds,vision, and echolocation in prey localization by the African batCardioderma cor (Megadermatidae)

Summary Cardioderma cor responded with head movements and flight toward speakers broadcasting calls of frogs and crickets which contained only sonic frequencies. Unlike the frog-eating bat,Trachops cirrhosus, they did not make contact with the speakers. Prey movements that generated sonic and ultrasonic sounds were both sufficient and necessary for the bats to localize and capture prey. Prey dragged across a glass sheet with a thin layer of water did not generate sounds and bats did not attempt to capture these prey, even with the availability of visual and echolocation cues. There was no evidence for the use of visual cues while hunting; bats did not localize prey more readily in light than darkness. Prey were presented such that their movements initially generated sounds, but then the prey moved onto the water layer of the glass sheet and sounds were eliminated. The bats emitted echolocation signals while hunting in this situation; however, the information from these signals was not utilized. The bats landed at the site that prey last made sound. These results demonstrate the importance of passive hearing for prey localization in this bat, and further suggest that when preygenerated sounds and echolocation signals offer conflicting information the bat's behavior is guided by the former.     

Duration selectivity of bat inferior collicular neurons improves with increasing pulse repetition rate

Insectivorous big brown bats, Eptesicus fuscus, progressively increase the pulse repetition rate (PRR) throughout the course of hunting. While increasing PRR conceivably facilitates bats to extract information about the targets, it also inevitably affects sensitivity of their auditory neurons to pulse parameters. The present study examined the effect of increasing PRR on duration selectivity of this bat's inferior collicular (IC) neurons by comparing their impulse-duration functions determined at different PRRs. Impulse-duration functions plotted with the number of impulses in response to single pulses against pulse duration at different PRRs were described as short-pass, band-pass, long-pass, and all-pass. Short- or long-pass neurons discharged maximally to a range of short or long pulse durations. Band-pass neurons discharged maximally to one pulse duration. These three types of IC neurons were called duration tuned neurons. All-pass neurons were not duration tuned because they did not discharge maximally to any pulse duration. Increasing PRR improved duration selectivity of IC neurons by (1) increasing the number of duration tuned neurons; (2) decreasing the critical duration concomitant with increasing slope of the impulse-duration function; and (3) decreasing the 50% duration range of the impulse-duration function. This improved duration selectivity with PRR may potentially facilitate prey capture by bats.     

GABA-mediated echo duration selectivity of inferior collicular neurons of Eptesicus fuscus, determined with single pulses and pulse–echo pairs

When insectivorous bats such as Eptesicus fuscus emit ultrasonic signals and analyze the returning echoes to hunt insects, duration selectivity of auditory neurons plays an important role in echo recognition. The success of prey capture indicates that they can effectively encode progressively shortened echo duration throughout the hunting process. The present study examines the echo duration selectivity of neurons in the central nucleus of the bat inferior colliculus (IC) under stimulation conditions of single pulses and pulse–echo (P–E) pairs. This study also examines the role of gamma-aminobutyric acid (GABA)ergic inhibition in shaping echo duration selectivity of IC neurons. The data obtained show that the echo duration selectivity of IC neurons is sharper when determined with P–E pairs than with single pulses. Echo duration selectivity also sharpens with shortening of pulse duration and P–E gap. Bicuculline application decreases and GABA application increases echo duration selectivity of IC neurons. The degree of change in echo duration selectivity progressively increases with shortening of pulse duration and P–E gap during bicuculline application while the opposite is observed during the GABA application. These data indicate that the GABAergic inhibition contributes to sharpening of echo duration selectivity of IC neurons and facilitates echo recognition by bats throughout different phases of hunting.     

Neural mechanisms of target ranging in FM bats: physiological evidence from bats and frogs

Echolocating bats assess target range by the delay in echo relative to the emitted sonar pulse. Earlier studies in FM bats showed that a population of neurons in auditory centers above the inferior colliculus (IC) is tuned to echo delay, with different neurons tuned to different echo delays. A building block for delay-tuned responses is paradoxical latency shift (PLS), featuring longer response latencies to more intense sounds. PLS is first created in the IC, where neurons exhibit unit-specific quantum increase in response latency with increasing sound level. Other IC neurons display oscillatory discharges whose period is unit-specific and level tolerant, indicating that this is attributable to cell’s intrinsic properties. High-threshold inhibition of oscillatory discharge produces PLS, indicating that oscillatory discharge is a building block for PLS. To investigate the cellular basis of oscillatory discharges, we performed whole-cell patch-clamp recordings from IC neurons in leopard frogs (which also exhibit oscillatory discharges and PLS). These recordings show that IC neurons are heterogeneous displaying diverse biophysical phenotypes; each phenotype (and cell) has its own membrane time constant, input resistance, and strengths of I _h, I _kir, I _kv—these intrinsic properties give rise to cell-specific resonance which can be observed through current and afferent stimulations.     

Recovery cycle of neurons in the inferior colliculus of the FM bat determined with varied pulse-echo duration and amplitude

The recovery cycle of auditory neurons is an important neuronal property which underlies a bat's ability in analyzing returning echoes and to determine target distance (i.e., echo ranging). In the same token, duration selectivity of auditory neurons plays an important role in pulse recognition in bat echolocation. Because insectivorous bats progressively vary the pulse parameters (repetition rate, duration, and amplitude) during hunting, the recovery cycle of auditory neurons is inevitably affected by their selectivity to other co-varying echo parameters. This study examines the effect of pulse duration and amplitude on recovery cycle of neurons in the central nucleus of the inferior colliculus (IC) of the FM bat, Pipistrellus abramus, using biologically relevant pulse-echo (P-E) pairs with varied duration and amplitude difference. We specifically examine how duration selectivity may affect a neuron's recovery cycle. IC neurons have wide range of recovery cycle and best duration (BD) covering P-E intervals and duration occurring different phases of hunting. The recovery cycle of most IC neurons increases with P-E duration and amplitude difference. Most duration-selective IC neurons recover rapidly when stimulated with biologically relevant P-E pairs. As such, neurons with short BD recover rapidly when stimulated with P-E pairs of short duration and small P-E amplitude difference. Conversely, neurons with long BD recover rapidly when stimulated with P-E pairs of long duration and large P-E amplitude difference. These data suggest that bats may potentially utilize the response of IC neurons with different BD and recovery cycle to effectively perform echo detection, recognition of echo duration and echo ranging throughout a target approaching sequence.     

Adaptive mechanisms underlying the bat biosonar behavior

For survival, bats of the suborder Microchiropetra emit intense ultrasonic pulses and analyze the weak returning echoes to extract the direction, distance, velocity, size, and shape of the prey. Although these bats and other mammals share the common layout of the auditory pathway and sound coding mechanism, they have highly developed auditory systems to process biologically relevant pulses at the expense of a reduced visual system. During this active biosonar behavior, they progressively shorten the pulse duration, decrease the amplitude and pulse-echo gap as they search, approach and finally intercept the prey. Presumably, these changes in multiple pulse parameters throughout the entire course of hunting enable them to extract maximal information about localized prey from the returning echoes. To hunt successfully, the auditory system of these bats must be less sensitive to intense emitted pulses but highly sensitive to weak returning echoes. They also need to recognize and differentiate the echoes of their emitted pulses from echoes of pulses emitted by other conspecifics. Past studies have shown the following mechanical and neural adaptive mechanisms underlying the successful bat biosonar behavior: (1) Forward orienting and highly mobile pinnae for effective scanning, signal reception, sound pressure transformation and mobile auditory sensitivity; (2) Avoiding and detecting moving targets more successfully than stationary ones; (3) Coordinated activity of highly developed laryngeal and middle ear muscles during pulse emission and reception; (4) Mechanical and neural attenuation of intense emitted pulses to prepare for better reception of weak returning echoes; (5) Increasing pulse repetition rate to improve multiple-parametric selectivity to echoes; (6) Dynamic variation of duration selectivity and recovery cycle of auditory neurons with hunting phase for better echo analysis; (7) Maximal multiple-parametric selectivity to expected echoes returning within a time window after pulse emission; (8) Pulse-echo delaysensitive neurons in higher auditory centers for echo ranging; (9) Corticofugal modulation to improve on-going multiple-parametric signal processing and reorganize signal representation, and (10) A large area of the superior colliculus, pontine nuclei and cerebellum that is sensitive to sound for sensori-motor integration. All these adaptive mechanisms facilitate the bat to effectively extract prey features for successful hunting.     

Ear morphology of the frog-eating bat (Trachops cirrhosus,family: Phyllostomidae): Apparent specializations for low-freqency hearing

The frog-eating bat (Trachops cirrhosus) is unusual among bats studied because of its reliance on low-frequency (<5 kHz) sounds emitted by frogs for prey localization. We investigated the ear of this bat in order to identify anatomical features that might serve as adaptations for low-frequency hearing. Trachops cirrhosus has a variety of anatomical features that might enhance low-frequency hearing, either by increasing sensitivity to low-frequency sounds or expanding the total frequency range to include lower frequencies. These bats have long pinnae, and a long and wide basilar membrane. The basal portion of the basilar membrane is much stiffer than the apical portion, and the basal portion of the tectorial membrane is more massive than the apical portion. There is also a concentration of mass in the apical portion of the cochlea. T. cirrhosus possesses the largest number of cochlear neurons reported for any mammal, the second highest density of cochlear neurons innervation known among mammals, and three peaks of cochlear neuron density. Other bats have two peaks of cochlear neuron density, lacking the apical concentration, while other mammals usually have only one. T. cirrhosus differs from most other small mammals and bats in characteristics of the apical portion of the cochlea, i.e., that area where the place theory of hearing predicts that low frequencies are detected.