听觉中枢神经元对声信号的识别和处理

人类听觉的基本特性和机制与其他哺乳动物相似,因此,利用动物所作的听觉研究和获得的结果,有助于认识人类自身的听觉.围绕听觉中枢神经元对不同模式的声信号的识别和处理,简要综述了这方面的研究.声信号和声模式识别在听觉中枢对声信号的感受和加工中具有重要意义.听神经元作为声模式识别的结构和功能基础,对不同的声刺激模式产生不同反应,甚至是在同一声刺激模式下,改变其中的某个声参数,神经元的反应也会发生相应改变,而其反应的特性和机制均需要更多研究来解答.另外,声信号作为声信息的载体,不同的声信息寓于不同的声参数和声特征之中,研究发现,听觉中枢神经元存在相应的声信息甄别和选择的神经基础,能对动态变化的声频率、幅度和时程等进行反应和编码,并且,在不同种类动物上获得的研究结果极为相似,表明听觉中枢对不同声信号和声刺激模式的识别、分析和加工,具有共同性和普遍性.     

Coding of communication calls in the subcortical and cortical structures of the auditory system

The processing of species-specific communication signals in the auditory system represents an important aspect of animal behavior and is crucial for its social interactions, reproduction, and survival. In this article the neuronal mechanisms underlying the processing of communication signals in the higher centers of the auditory system--inferior colliculus (IC), medial geniculate body (MGB) and auditory cortex (AC)--are reviewed, with particular attention to the guinea pig. The selectivity of neuronal responses for individual calls in these auditory centers in the guinea pig is usually low--most neurons respond to calls as well as to artificial sounds; the coding of complex sounds in the central auditory nuclei is apparently based on the representation of temporal and spectral features of acoustical stimuli in neural networks. Neuronal response patterns in the IC reliably match the sound envelope for calls characterized by one or more short impulses, but do not exactly fit the envelope for long calls. Also, the main spectral peaks are represented by neuronal firing rates in the IC. In comparison to the IC, response patterns in the MGB and AC demonstrate a less precise representation of the sound envelope, especially in the case of longer calls. The spectral representation is worse in the case of low-frequency calls, but not in the case of broad-band calls. The emotional content of the call may influence neuronal responses in the auditory pathway, which can be demonstrated by stimulation with time-reversed calls or by measurements performed under different levels of anesthesia. The investigation of the principles of the neural coding of species-specific vocalizations offers some keys for understanding the neural mechanisms underlying human speech perception.     

Bilateral collicular interaction: modulation of auditory signal processing in amplitude domain

In the ascending auditory pathway, the inferior colliculus (IC) receives and integrates excitatory and inhibitory inputs from many lower auditory nuclei, intrinsic projections within the IC, contralateral IC through the commissure of the IC and from the auditory cortex. All these connections make the IC a major center for subcortical temporal and spectral integration of auditory information. In this study, we examine bilateral collicular interaction in modulating amplitude-domain signal processing using electrophysiological recording, acoustic and focal electrical stimulation. Focal electrical stimulation of one (ipsilateral) IC produces widespread inhibition (61.6%) and focused facilitation (9.1%) of responses of neurons in the other (contralateral) IC, while 29.3% of the neurons were not affected. Bilateral collicular interaction produces a decrease in the response magnitude and an increase in the response latency of inhibited IC neurons but produces opposite effects on the response of facilitated IC neurons. These two groups of neurons are not separately located and are tonotopically organized within the IC. The modulation effect is most effective at low sound level and is dependent upon the interval between the acoustic and electric stimuli. The focal electrical stimulation of the ipsilateral IC compresses or expands the rate-level functions of contralateral IC neurons. The focal electrical stimulation also produces a shift in the minimum threshold and dynamic range of contralateral IC neurons for as long as 150 minutes. The degree of bilateral collicular interaction is dependent upon the difference in the best frequency between the electrically stimulated IC neurons and modulated IC neurons. These data suggest that bilateral collicular interaction mainly changes the ratio between excitation and inhibition during signal processing so as to sharpen the amplitude sensitivity of IC neurons. Bilateral interaction may be also involved in acoustic-experience-dependent plasticity in the IC. Three possible neural pathways underlying the bilateral collicular interaction are discussed.     

GABA-mediated modulation of the discharge pattern and rate-level function of two simultaneously recorded neurons in the inferior colliculus of the big brown bat, Eptesicus fuscus

Neurons in the central nucleus of the inferior colliculus (IC) receive excitatory and inhibitory inputs from both lower and higher auditory nuclei. Interaction of these two opposing inputs shapes response properties of IC neurons. In this study, we examine the interaction of excitation and inhibition on the responses of two simultaneously recorded IC neurons using a probe and a masker under forward masking paradigm. We specifically study whether a sound that serves as a probe to elicit responses of one neuron might serve as a masker to suppress or facilitate the responses of the other neuron. For each pair of IC neurons, we deliver the probe at the best frequency (BF) of one neuron and the masker at the BF of the other neuron and vice versa. Among 33 pairs of IC neurons recorded, this forward masking produces response suppression in 29 pairs of IC neurons and response facilitation in 4 pairs of IC neurons. The degree of suppression decreases with recording depth, sound level and BF difference between each pair of IC neurons. During bicuculline application, the degree of response suppression decreases in the bicuculline-applied neuron but increases in the paired neuron. Our data indicate that the forward masking of responses of IC neurons observed in this study is mostly mediated through GABAergic inhibition which also shapes the discharge pattern of these neurons. These data suggest that interaction among individual IC neurons improves auditory sensitivity during auditory signal processing.     

The amplitude sensitivity of mouse inferior collicular neurons in the presence of weak noise

Natural auditory environment consists of multiple sound sources that are embedded in ambient strong and weak noise. For effective sound communication and signal analysis, animals must somehow extract biologically relevant signals from the inevitable interference of ambient noise. The present study examined how a weak noise may affect the amplitude sensitivity of neurons in the mouse central nucleus of the inferior colliculus (IC) which receives convergent excitatory and inhibitory inputs from both lower and higher auditory centers. Specifically, we studied the amplitude sensitivity of IC neurons using a probe (best frequency pulse) and a masker (weak noise) under simultaneous masking paradigm. For most IC neurons, weak noise masking increases the minimum threshold and decreases the number of impulses. Noise masking also increased the slope and decreased the dynamic range of the rate amplitude function of these IC neurons. The strength of this noise masking was greater at low than at high sound amplitudes. This variation in the amplitude sensitivity of IC neurons in the presence of the weak noise was mostly mediated through GABAergic inhibition. These data indicate that in the real world the ambient weak noise improves amplitude sensitivity of IC neurons through GABAergic inhibition while inevitably decreases the range of overall auditory sensitivity of IC neurons.     

Latency represents sound frequency in mouse IC

Frequency is one of the fundamental parameters of sound. The frequency of an acoustic stimulus can be represented by a neural response such as spike rate, and/or first spike latency (FSL) of a given neuron. The spike rates/frequency function of most neurons changes with different acoustic amplitudes, whereas FSL/frequency function is highly stable. This implies that FSL might represent the frequency of a sound stimulus more efficiently than spike rate. This study involved representations of acoustic frequency by spike rate and FSL of central inferior colliculus (IC) neurons responding to free-field pure-tone stimuli. We found that the FSLs of neurons responding to characteristic frequency (CF) of sound stimulus were usually the shortest, regardless of sound intensity, and that spike rates of most neurons showed a variety of function according to sound frequency, especially at high intensities.These results strongly suggest that FSL of auditory IC neurons can represent sound frequency more precisely than spike rate.     

Latency represents sound frequency in mouse IC

Frequency is one of the fundamental parameters of sound.The frequency of an acoustic stimulus can be represented by a neural response such as spike rate,and/or first spike latency(FSL)of a given neuron.The spike rates/frequency function of most neurons changes with different acoustic ampli-tudes,whereas FSL/frequency function is highly stable.This implies that FSL might represent the fre-quency of a sound stimulus more efficiently than spike rate.This study involved representations of acoustic frequency by spike rate and FSL of central inferior colliculus(IC)neurons responding to free-field pure-tone stimuli.We found that the FSLs of neurons responding to characteristic frequency(CF)of sound stimulus were usually the shortest,regardless of sound intensity,and that spike rates of most neurons showed a variety of function according to sound frequency,especially at high intensities.These results strongly suggest that FSL of auditory IC neurons can represent sound frequency more precisely than spike rate.     

后掩蔽效应对大棕蝠下丘神经元声反应的影响

以回声定位蝙蝠为模式动物,采用在体动物细胞外单位记录法,研究了后掩蔽效应对下丘神经元声反应的影响。结果显示,部分神经元(38％,12／31)对测试声刺激的反应明显受到掩蔽声的抑制,其后掩蔽效应强弱与掩蔽声和测试声的相对强度差(inter-stimulus level difference,SLD),以及测试声与掩蔽声之间的间隔时间(inter-stimulus onset asynchrony,SOA)有关：当掩蔽声强度升高或测试声强度降低时,后掩蔽效应增强;而SOA的缩短,亦可见后掩蔽效应增强。另外,相当数量的神经元(52%,16／31)对测试声刺激的反应并不受掩蔽声的影响,其中有的神经元只有在特定SLD和SOA时,才表现出后掩蔽效应。而少数下丘神经元(10％,3／31)在特定SLD和SOA时,掩蔽声对测试声反应有易化作用。上述结果表明,部分下丘神经元参与了声认知活动中的后掩蔽形成过程,推测下丘神经元在定型声反应特性中,对掩蔽声诱导的兴奋前抑制性输入与测试声诱导的兴奋性输入之间的时相性动态整合起关键作用。     

Eye position influences auditory responses in primate inferior colliculus

We examined the frame of reference of auditory responses in the inferior colliculus in monkeys fixating visual stimuli at different locations. Eye position modulated the level of auditory responses in 33% of the neurons we encountered, but it did not appear to shift their spatial tuning. The effect of eye position on auditory responses was substantial-comparable in magnitude to that of sound location. The eye position signal appeared to interact with the auditory responses in at least a partly multiplicative fashion. We conclude that the representation of sound location in primate IC is distributed and that the frame of reference is intermediate between head- and eye-centered coordinates. The information contained in these neurons appears to be sufficient for later neural stages to calculate the positions of sounds with respect to the eyes.     

Neural representation of spectral and temporal information in speech

Speech is the most interesting and one of the most complex sounds dealt with by the auditory system. The neural representation of speech needs to capture those features of the signal on which the brain depends in language communication. Here we describe the representation of speech in the auditory nerve and in a few sites in the central nervous system from the perspective of the neural coding of important aspects of the signal. The representation is tonotopic, meaning that the speech signal is decomposed by frequency and different frequency components are represented in different populations of neurons. Essential to the representation are the properties of frequency tuning and nonlinear suppression. Tuning creates the decomposition of the signal by frequency, and nonlinear suppression is essential for maintaining the representation across sound levels. The representation changes in central auditory neurons by becoming more robust against changes in stimulus intensity and more transient. However, it is probable that the form of the representation at the auditory cortex is fundamentally different from that at lower levels, in that stimulus features other than the distribution of energy across frequency are analysed.     

High-order auditory filters.

The past year has seen some important advances in our understanding of central auditory function. Several central auditory neurons that differ from those in the periphery in their selectivity for various spectral and temporal parameters of complex sound have been described. Although central specializations for the processing of complex sound have been known for some time, recent findings suggest that these high-order filter properties are more widespread than previously thought. Significant progress has been made in our understanding of the neural mechanisms by which some high-order filter properties, such as delay-tuning, amplitude-tuning, and complex frequency tuning are performed by the central auditory system. New evidence has clarified the role of high-order auditory filters in auditory learning and perception, and the regions in which they are found.     

Reduction of information redundancy in the ascending auditory pathway

Information processing by a sensory system is reflected in the changes in stimulus representation along its successive processing stages. We measured information content and stimulus-induced redundancy in the neural responses to a set of natural sounds in three successive stations of the auditory pathway-inferior colliculus (IC), auditory thalamus (MGB), and primary auditory cortex (A1). Information about stimulus identity was somewhat reduced in single A1 and MGB neurons relative to single IC neurons, when information is measured using spike counts, latency, or temporal spiking patterns. However, most of this difference was due to differences in firing rates. On the other hand, IC neurons were substantially more redundant than A1 and MGB neurons. IC redundancy was largely related to frequency selectivity. Redundancy reduction may be a generic organization principle of neural systems, allowing for easier readout of the identity of complex stimuli in A1 relative to IC.     

GABA能抑制调制大棕蝠下丘听神经元时间编码模式

大棕幅（Eptesicus fuscus）下丘神经元对重复率为10pps(pulse per second）、30pps的串声刺激均产生跟随反应,但对90pps串声刺激的跟随反应则不尽相同,微电泳bicuculline阻断GABA能抑制作用后,所记录的58个神经元中,有13个（22％）放电率及串声刺激反应模式无;45个（78％）神经元放电率有不同程度的增加。对10pps、30pps串声刺激仍能产生跟随反应,但对90pps串声刺激的跟随反应模式有多种变化。其中：17个（29％）神经元为放电率增加的跟随反应;9个（15％）神经元放电率增加,对前100ms的串刺激产生反应且放电密集,而对随后200ms的串刺激只产生少量的放电;15个（26％）神经元放电率增加,在前几十毫秒范围内有较多的放电反应,后续的反应很弱;4个（7％）神经元只对第一个声刺激产生反应,且放电率增加,随后放电急剧减少。结果提示中脑下丘神经元对听觉信息的时间编码可能具有更复杂的机理。     

Changes in neuronal activity of the inferior colliculus in rat after temporal inactivation of the auditory cortex

The role of cortico-tectal pathways in auditory signal processing was studied in anesthetized rats by comparing the extracellular single unit activity in the inferior colliculus (IC) before and after functional ablation of the auditory cortex (AC) by tetrodotoxin (TTX). The responses of several IC neurons to sound stimuli were simultaneously recorded with a 16-channel electrode probe introduced into the IC. Click-evoked middle latency responses (MLR) recorded from the AC were suppressed for several hours after TTX injection. During AC inactivation the firing rate of IC neurons increased (40 % of neurons), decreased (44 %) or did not change (16 %) in comparison with control conditions. In several IC neurons, TTX injection resulted in alterations in the shape of the rate-level functions. Response thresholds, tuning properties and the type of discharge pattern of IC neurons were not altered during AC inactivation. However, in one-third of the neurons, the initial part of the response was less altered than the later, sustained part. In two-thirds of neuronal pairs, functional decortication resulted in a change in the cross-correlation coefficient. The results reveal the complex changes that appear in IC neuronal activity after functional ablation of the ipsilateral auditory cortex.     

Selective and Efficient Neural Coding of Communication Signals Depends on Early Acoustic and Social Environment

Previous research has shown that postnatal exposure to simple, synthetic sounds can affect the sound representation in the auditory cortex as reflected by changes in the tonotopic map or other relatively simple tuning properties, such as AM tuning. However, their functional implications for neural processing in the generation of ethologically-based perception remain unexplored. Here we examined the effects of noise-rearing and social isolation on the neural processing of communication sounds such as species-specific song, in the primary auditory cortex analog of adult zebra finches. Our electrophysiological recordings reveal that neural tuning to simple frequency-based synthetic sounds is initially established in all the laminae independent of patterned acoustic experience; however, we provide the first evidence that early exposure to patterned sound statistics, such as those found in native sounds, is required for the subsequent emergence of neural selectivity for complex vocalizations and for shaping neural spiking precision in superficial and deep cortical laminae, and for creating efficient neural representations of song and a less redundant ensemble code in all the laminae. Our study also provides the first causal evidence for ‘sparse coding’, such that when the statistics of the stimuli were changed during rearing, as in noise-rearing, that the sparse or optimal representation for species-specific vocalizations disappeared. Taken together, these results imply that a layer-specific differential development of the auditory cortex requires patterned acoustic input, and a specialized and robust sensory representation of complex communication sounds in the auditory cortex requires a rich acoustic and social environment.     

Corollary discharge inhibition and audition in the stridulating cricket

The romantic notion of crickets singing on a warm summer’s evening is quickly dispelled when one comes ear to ear with a stridulating male. Remarkably, stridulating male crickets are able to hear sounds from the environment despite generating a 100 db song (Heiligenberg 1969; Jones and Dambach 1973). This review summarises recent work examining how they achieve this feat of sensory processing. While the responsiveness of the crickets’ peripheral auditory system (tympanic membrane, tympanic nerve, state of the acoustic spiracle) is maintained during sound production, central auditory neurons are inhibited by a feedforward corollary discharge signal precisely timed to coincide with the auditory neurons’ maximum response to self-generated sound. In this way, the corollary discharge inhibition prevents desensitisation of the crickets’ auditory pathway during sound production.     

Unilateral Tinnitus: Changes in Connectivity and Response Lateralization Measured with fMRI

Tinnitus is a percept of sound that is not related to an acoustic source outside the body. For many forms of tinnitus, mechanisms in the central nervous system are believed to play a role in the pathology. In this work we specifically assessed possible neural correlates of unilateral tinnitus. Functional magnetic resonance imaging (fMRI) was used to investigate differences in sound-evoked neural activity between controls, subjects with left-sided tinnitus, and subjects with right-sided tinnitus. We assessed connectivity patterns between auditory nuclei and the lateralization of the sound-evoked responses. Interestingly, these response characteristics did not relate to the laterality of tinnitus. The lateralization for left- or right ear stimuli, as expressed in a lateralization index, was considerably smaller in subjects with tinnitus compared to that in controls, reaching significance in the right primary auditory cortex (PAC) and the right inferior colliculus (IC). Reduced functional connectivity between the brainstem and the cortex was observed in subjects with tinnitus. These differences are consistent with two existing models that relate tinnitus to i) changes in the corticothalamic feedback loops or ii) reduced inhibitory effectiveness between the limbic system and the thalamus. The vermis of the cerebellum also responded to monaural sound in subjects with unilateral tinnitus. In contrast, no cerebellar response was observed in control subjects. This suggests the involvement of the vermis of the cerebellum in unilateral tinnitus.     

Psychophysiology and psychoacoustics of music: Perception of complex sound in normal subjects and psychiatric patients

Perception of complex sound is a process carried out in everyday life situations and contributes in the way one perceives reality. Attempting to explain sound perception and how it affects human beings is complicated. Physics of simple sound can be described as a function of frequency, amplitude and phase. Psychology of sound, also termed psychoacoustics, has its own distinct elements of pitch, intensity and tibre. An interconnection exists between physics and psychology of hearing.Music being a complex sound contributes to communication and conveys information with semantic and emotional elements. These elements indicate the involvement of the central nervous system through processes of integration and interpretation together with peripheral auditory processing.Effects of sound and music in human psychology and physiology are complicated. Psychological influences of listening to different types of music are based on the different characteristics of basic musical sounds. Attempting to explain music perception can be simpler if music is broken down to its basic auditory signals. Perception of auditory signals is analyzed by the science of psychoacoustics. Differences in complex sound perception have been found between normal subjects and psychiatric patients and between different types of psychopathologies.     

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.     

Encoding of Temporal Information by Timing,Rate, and Place in Cat Auditory Cortex

A central goal in auditory neuroscience is to understand the neural coding of species-specific communication and human speech sounds. Low-rate repetitive sounds are elemental features of communication sounds, and core auditory cortical regions have been implicated in processing these information-bearing elements. Repetitive sounds could be encoded by at least three neural response properties: 1) the event-locked spike-timing precision, 2) the mean firing rate, and 3) the interspike interval (ISI). To determine how well these response aspects capture information about the repetition rate stimulus, we measured local group responses of cortical neurons in cat anterior auditory field (AAF) to click trains and calculated their mutual information based on these different codes. ISIs of the multiunit responses carried substantially higher information about low repetition rates than either spike-timing precision or firing rate. Combining firing rate and ISI codes was synergistic and captured modestly more repetition information. Spatial distribution analyses showed distinct local clustering properties for each encoding scheme for repetition information indicative of a place code. Diversity in local processing emphasis and distribution of different repetition rate codes across AAF may give rise to concurrent feed-forward processing streams that contribute differently to higher-order sound analysis.