A Dominance Hierarchy of Auditory Spatial Cues in Barn Owls

Background

Barn owls integrate spatial information across frequency channels to localize sounds in space.

Methodology/Principal Findings

We presented barn owls with synchronous sounds that contained different bands of frequencies (3–5 kHz and 7–9 kHz) from different locations in space. When the owls were confronted with the conflicting localization cues from two synchronous sounds of equal level, their orienting responses were dominated by one of the sounds: they oriented toward the location of the low frequency sound when the sources were separated in azimuth; in contrast, they oriented toward the location of the high frequency sound when the sources were separated in elevation. We identified neural correlates of this behavioral effect in the optic tectum (OT, superior colliculus in mammals), which contains a map of auditory space and is involved in generating orienting movements to sounds. We found that low frequency cues dominate the representation of sound azimuth in the OT space map, whereas high frequency cues dominate the representation of sound elevation.

Conclusions/Significance

We argue that the dominance hierarchy of localization cues reflects several factors: 1) the relative amplitude of the sound providing the cue, 2) the resolution with which the auditory system measures the value of a cue, and 3) the spatial ambiguity in interpreting the cue. These same factors may contribute to the relative weighting of sound localization cues in other species, including humans.     

Optimal nonlinear cue integration for sound localization

Integration of multiple sensory cues can improve performance in detection and estimation tasks. There is an open theoretical question of the conditions under which linear or nonlinear cue combination is Bayes-optimal. We demonstrate that a neural population decoded by a population vector requires nonlinear cue combination to approximate Bayesian inference. Specifically, if cues are conditionally independent, multiplicative cue combination is optimal for the population vector. The model was tested on neural and behavioral responses in the barn owl’s sound localization system where space-specific neurons owe their selectivity to multiplicative tuning to sound localization cues interaural phase (IPD) and level (ILD) differences. We found that IPD and ILD cues are approximately conditionally independent. As a result, the multiplicative combination selectivity to IPD and ILD of midbrain space-specific neurons permits a population vector to perform Bayesian cue combination. We further show that this model describes the owl’s localization behavior in azimuth and elevation. This work provides theoretical justification and experimental evidence supporting the optimality of nonlinear cue combination.     

Sensory cues for sound localization in the cricket<Emphasis Type="Italic"> Teleogryllus oceanicus</Emphasis>: interaural difference in response strength versus interaural latency difference

Two potential sensory cues for sound location are interaural difference in response strength (firing rate and/or spike count) and in response latency of auditory receptor neurons. Previous experiments showed that these two cues are affected differently by intense prior stimulation; the difference in response strength declines and may even reverse in sign, but the difference in latency is unaffected. Here, I use an intense, constant tone to disrupt localization cues generated by a subsequent train of sound pulses. Recordings from the auditory nerve confirm that tone stimulation reduces, and sometimes reverses, the interaural difference in response strength to subsequent sound pulses, but that it enhances the interaural latency difference. If sound location is determined mainly from latency comparison, then behavioral responses to a pulse train following tone stimulation should be normal, but if the main cue for sound location is interaural difference in response strength, then post-tone behavioral responses should sometimes be misdirected. Initial phonotactic responses to the post-tone pulse train were frequently directed away from, rather than towards, the sound source, indicating that the dominant sensory cue for sound location is interaural difference in response strength.     

Distributed coding of sound locations in the auditory cortex

Although the auditory cortex plays an important role in sound localization, that role is not well understood. In this paper, we examine the nature of spatial representation within the auditory cortex, focusing on three questions. First, are sound-source locations encoded by individual sharply tuned neurons or by activity distributed across larger neuronal populations? Second, do temporal features of neural responses carry information about sound-source location? Third, are any fields of the auditory cortex specialized for spatial processing? We present a brief review of recent work relevant to these questions along with the results of our investigations of spatial sensitivity in cat auditory cortex. Together, they strongly suggest that space is represented in a distributed manner, that response timing (notably first-spike latency) is a critical information-bearing feature of cortical responses, and that neurons in various cortical fields differ in both their degree of spatial sensitivity and their manner of spatial coding. The posterior auditory field (PAF), in particular, is well suited for the distributed coding of space and encodes sound-source locations partly by modulations of response latency. Studies of neurons recorded simultaneously from PAF and/or A1 reveal that spatial information can be decoded from the relative spike times of pairs of neurons - particularly when responses are compared between the two fields - thus partially compensating for the absence of an absolute reference to stimulus onset.     

The Opponent Channel Population Code of Sound Location Is an Efficient Representation of Natural Binaural Sounds

In mammalian auditory cortex, sound source position is represented by a population of broadly tuned neurons whose firing is modulated by sounds located at all positions surrounding the animal. Peaks of their tuning curves are concentrated at lateral position, while their slopes are steepest at the interaural midline, allowing for the maximum localization accuracy in that area. These experimental observations contradict initial assumptions that the auditory space is represented as a topographic cortical map. It has been suggested that a “panoramic” code has evolved to match specific demands of the sound localization task. This work provides evidence suggesting that properties of spatial auditory neurons identified experimentally follow from a general design principle- learning a sparse, efficient representation of natural stimuli. Natural binaural sounds were recorded and served as input to a hierarchical sparse-coding model. In the first layer, left and right ear sounds were separately encoded by a population of complex-valued basis functions which separated phase and amplitude. Both parameters are known to carry information relevant for spatial hearing. Monaural input converged in the second layer, which learned a joint representation of amplitude and interaural phase difference. Spatial selectivity of each second-layer unit was measured by exposing the model to natural sound sources recorded at different positions. Obtained tuning curves match well tuning characteristics of neurons in the mammalian auditory cortex. This study connects neuronal coding of the auditory space with natural stimulus statistics and generates new experimental predictions. Moreover, results presented here suggest that cortical regions with seemingly different functions may implement the same computational strategy-efficient coding.     

Sound the alarm: learned association of predation risk with novel auditory stimuli by fathead minnows ( Pimephales promelas ) and glowlight tetras ( Hemigrammus erythrozonus ) after single simultaneous pairings with conspecific chemical alarm cues

Fathead minnows, Pimephales promelas, and glowlight tetras, Hemigrammus erythrozonus, were tested for their ability to associate predation risk with novel auditory stimuli after auditory stimuli were presented simultaneously with chemical alarm cues. Minnows and tetras gave a fright response when exposed to skin extract (alarm cue) and an artificial auditory sound stimulus, but no response to water (control) and sound, indicating that they did not have a pre-existing aversion to the auditory stimulus. When retested with sound stimuli alone, minnows and glowlight tetras that had previously been conditioned with water and sound showed no response, but those that had been conditioned with alarm cues and sound exhibited antipredator behaviour (reduced activity) in response to the auditory cue. This is the first known demonstration of learned association of an auditory cue with predation risk, and raises questions about the role of sound in mediating predator-prey interactions in fishes.     

听神经元的频率调谐

频率作为声音的一个重要参数,在听敏感神经元对声音进行分析和编码过程中扮演重要角色。一般用频率调谐曲线来表示听敏感神经元的频率调谐特性,并用Qn(10,30,50)值表达频率调谐曲线的尖锐程度,Qn值越大,频率调谐曲线也越尖锐,神经元的频率调谐能力越好,对频率的分辨能力越高。从听觉外周到中枢,听敏感神经元的频率调谐逐级锐化,而这种锐化主要是由听中枢的多种抑制性神经递质的作用而产生的,其中起主要作用的是GABA能和甘氨酸能神经递质。此外,离皮层调控,双侧下丘间的联合投射以及弱噪声前掩蔽等因素也会影响听敏感神经元的频率调谐特性。     

Dependence of the mouse inferior colliculus neurons activity on position and direction of movement of the spectral contrast

Response variability of the single neurons of the inferior colliculus of mouse (Mus musculus) to series of noise bands and of notch noises with regular 1/12 octave steps of the band/notch center frequency and width of noise band/notch 1/3 octave, was studied. Neurons with strong inhibitory influence in excitatory response area (inhibitory-dominated) show low impulse activity when noise band exceeded excitatory response area. Spectral contrasts crossing the center of excitatory response area (at CF or nearly CF) were found to be the most efficient stimuli for such neurons. Neuron responses to spectral contrasts derived both from noise band and noise notch were identical. Approaching of inhibitory and excitatory inputs is expected to sharpen the auditory neurons frequency tuning to position of spectral contrasts, similar to neuronal processing in visual system. Neuron selectivity to the direction of spectral contrasts movement was determined in neuron response differences when the noise band or notch shifted from excitatory area to inhibitory areas as compared with shift in the opposite direction. Functional role of contrast mechanism for sound localization on the base spectral cues related to external ear transfer characteristics is discussed.     

Location coding by opponent neural populations in the auditory cortex

Although the auditory cortex plays a necessary role in sound localization, physiological investigations in the cortex reveal inhomogeneous sampling of auditory space that is difficult to reconcile with localization behavior under the assumption of local spatial coding. Most neurons respond maximally to sounds located far to the left or right side, with few neurons tuned to the frontal midline. Paradoxically, psychophysical studies show optimal spatial acuity across the frontal midline. In this paper, we revisit the problem of inhomogeneous spatial sampling in three fields of cat auditory cortex. In each field, we confirm that neural responses tend to be greatest for lateral positions, but show the greatest modulation for near-midline source locations. Moreover, identification of source locations based on cortical responses shows sharp discrimination of left from right but relatively inaccurate discrimination of locations within each half of space. Motivated by these findings, we explore an opponent-process theory in which sound-source locations are represented by differences in the activity of two broadly tuned channels formed by contra- and ipsilaterally preferring neurons. Finally, we demonstrate a simple model, based on spike-count differences across cortical populations, that provides bias-free, level-invariant localization—and thus also a solution to the “binding problem” of associating spatial information with other nonspatial attributes of sounds.     

When and where of auditory spatial processing in cortex: a novel approach using electrotomography

The modulation of brain activity as a function of auditory location was investigated using electro-encephalography in combination with standardized low-resolution brain electromagnetic tomography. Auditory stimuli were presented at various positions under anechoic conditions in free-field space, thus providing the complete set of natural spatial cues. Variation of electrical activity in cortical areas depending on sound location was analyzed by contrasts between sound locations at the time of the N1 and P2 responses of the auditory evoked potential. A clear-cut double dissociation with respect to the cortical locations and the points in time was found, indicating spatial processing (1) in the primary auditory cortex and posterodorsal auditory cortical pathway at the time of the N1, and (2) in the anteroventral pathway regions about 100 ms later at the time of the P2. Thus, it seems as if both auditory pathways are involved in spatial analysis but at different points in time. It is possible that the late processing in the anteroventral auditory network reflected the sharing of this region by analysis of object-feature information and spectral localization cues or even the integration of spatial and non-spatial sound features.     

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.     

Robustness of neuronal tuning to binaural sound localization cues against age-related loss of inhibitory synaptic inputs

Sound localization relies on minute differences in the timing and intensity of sound arriving at both ears. Neurons of the lateral superior olive (LSO) in the brainstem process these interaural disparities by precisely detecting excitatory and inhibitory synaptic inputs. Aging generally induces selective loss of inhibitory synaptic transmission along the entire auditory pathways, including the reduction of inhibitory afferents to LSO. Electrophysiological recordings in animals, however, reported only minor functional changes in aged LSO. The perplexing discrepancy between anatomical and physiological observations suggests a role for activity-dependent plasticity that would help neurons retain their binaural tuning function despite loss of inhibitory inputs. To explore this hypothesis, we use a computational model of LSO to investigate mechanisms underlying the observed functional robustness against age-related loss of inhibitory inputs. The LSO model is an integrate-and-fire type enhanced with a small amount of low-voltage activated potassium conductance and driven with (in)homogeneous Poissonian inputs. Without synaptic input loss, model spike rates varied smoothly with interaural time and level differences, replicating empirical tuning properties of LSO. By reducing the number of inhibitory afferents to mimic age-related loss of inhibition, overall spike rates increased, which negatively impacted binaural tuning performance, measured as modulation depth and neuronal discriminability. To simulate a recovery process compensating for the loss of inhibitory fibers, the strength of remaining inhibitory inputs was increased. By this modification, effects of inhibition loss on binaural tuning were considerably weakened, leading to an improvement of functional performance. These neuron-level observations were further confirmed by population modeling, in which binaural tuning properties of multiple LSO neurons were varied according to empirical measurements. These results demonstrate the plausibility that homeostatic plasticity could effectively counteract known age-dependent loss of inhibitory fibers in LSO and suggest that behavioral degradation of sound localization might originate from changes occurring more centrally.     

Diverse processing underlying frequency integration in midbrain neurons of barn owls

Emergent response properties of sensory neurons depend on circuit connectivity and somatodendritic processing. Neurons of the barn owl’s external nucleus of the inferior colliculus (ICx) display emergence of spatial selectivity. These neurons use interaural time difference (ITD) as a cue for the horizontal direction of sound sources. ITD is detected by upstream brainstem neurons with narrow frequency tuning, resulting in spatially ambiguous responses. This spatial ambiguity is resolved by ICx neurons integrating inputs over frequency, a relevant processing in sound localization across species. Previous models have predicted that ICx neurons function as point neurons that linearly integrate inputs across frequency. However, the complex dendritic trees and spines of ICx neurons raises the question of whether this prediction is accurate. Data from in vivo intracellular recordings of ICx neurons were used to address this question. Results revealed diverse frequency integration properties, where some ICx neurons showed responses consistent with the point neuron hypothesis and others with nonlinear dendritic integration. Modeling showed that varied connectivity patterns and forms of dendritic processing may underlie observed ICx neurons’ frequency integration processing. These results corroborate the ability of neurons with complex dendritic trees to implement diverse linear and nonlinear integration of synaptic inputs, of relevance for adaptive coding and learning, and supporting a fundamental mechanism in sound localization.     

Training-induced plasticity of auditory localization in adult mammals

Accurate auditory localization relies on neural computations based on spatial cues present in the sound waves at each ear. The values of these cues depend on the size, shape, and separation of the two ears and can therefore vary from one individual to another. As with other perceptual skills, the neural circuits involved in spatial hearing are shaped by experience during development and retain some capacity for plasticity in later life. However, the factors that enable and promote plasticity of auditory localization in the adult brain are unknown. Here we show that mature ferrets can rapidly relearn to localize sounds after having their spatial cues altered by reversibly occluding one ear, but only if they are trained to use these cues in a behaviorally relevant task, with greater and more rapid improvement occurring with more frequent training. We also found that auditory adaptation is possible in the absence of vision or error feedback. Finally, we show that this process involves a shift in sensitivity away from the abnormal auditory spatial cues to other cues that are less affected by the earplug. The mature auditory system is therefore capable of adapting to abnormal spatial information by reweighting different localization cues. These results suggest that training should facilitate acclimatization to hearing aids in the hearing impaired.     

Plasticity and corticofugal modulation for hearing in adult animals

The descending (corticofugal) auditory system adjusts and improves auditory signal processing in the subcortical auditory nuclei. The auditory cortex and corticofugal system evoke small, short-term changes of the subcortical auditory nuclei in response to a sound repetitively delivered to an animal. These changes are specific to the parameters characterizing the sound. When the sound becomes significant to the animal through conditioning (associative learning), the changes are augmented and the cortical changes become long-term. There are two types of reorganizations: expanded reorganization resulting from centripetal shifts in tuning curves of neurons toward the values of the parameters characterizing a sound and compressed reorganization resulting from centrifugal shifts in tuning curves of neurons away from these values. The two types of reorganizations are based on a single mechanism consisting of two components: facilitation and inhibition.     

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.     

Processing of spectral localization-informative changes in sound signals by neurons of inferior colliculus and auditory cortex of the house mouse Mus musculus

Comparative analysis was performed of sensitivity of three populations of neurons of the inferior colliculus central nucleus and of neurons of the auditory cortex A1 and AAF fields of the house mouse Mus musculus to series of signals of wideband noise with spectral notch shifting along the frequency axis and to series of the band noise signals with shifting band. Sensitivity to spectral notches in noise was estimated from a change of impulse activity depending on notch location on the frequency axis (modulation coefficients were determined as the normalized difference between the maximal and minimal spike number in neuronal responses to all noises with notch exposed in the series). It was shown that the highest modulation coefficient values and accordingly the highest frequency-dependent sensitivity to spectral notches in the noise were peculiar to inhibition-dependent inferior colliculus neurons. Statistical analysis confirmed that distribution of modulation coefficients for the group of the inhibition-dependent neurons differed statistically significantly from the distribution for groups of primary-like and V-shaped inferior colliculus neurons as well as of cortical neurons (U-test, p < 0.0001). The lowest sensitivity to spectral notches was revealed in the V-shaped inferior colliculus neurons and cortical neurons; in these groups, distribution of modulation coefficients did not differed statistically significantly (p > 0.3). Thus, although a part of cortical neurons does have the frequency-dependent selectivity to spectral localizationally informative changes in sound signals, its formation needs participation of the inferior colliculus and its inhibition-dependent neurons. Selectivity to direction of the shift of spectral changes in noise signals in neurons of the inferior colliculus and auditory cortex was similar and was manifested mainly as shift along the frequency axis of dependences of the spike number in the neuronal responses and latent periods on central frequency of notch in noise (the noise band).     

Sound-localization experiments with barn owls in virtual space: influence of broadband interaural level difference on head-turning behavior

Interaural level differences play an important role for elevational sound localization in barn owls. The changes of this cue with sound location are complex and frequency dependent. We exploited the opportunities offered by the virtual space technique to investigate the behavioral relevance of the overall interaural level difference by fixing this parameter in virtual stimuli to a constant value or introducing additional broadband level differences to normal virtual stimuli. Frequency-specific monaural cues in the stimuli were not manipulated. We observed an influence of the broadband interaural level differences on elevational, but not on azimuthal sound localization. Since results obtained with our manipulations explained only part of the variance in elevational turning angle, we conclude that frequency-specific cues are also important. The behavioral consequences of changes of the overall interaural level difference in a virtual sound depended on the combined interaural time difference contained in the stimulus, indicating an indirect influence of temporal cues on elevational sound localization as well. Thus, elevational sound localization is influenced by a combination of many spatial cues including frequency-dependent and temporal features.     

Multiplicative Auditory Spatial Receptive Fields Created by a Hierarchy of Population Codes

A multiplicative combination of tuning to interaural time difference (ITD) and interaural level difference (ILD) contributes to the generation of spatially selective auditory neurons in the owl''s midbrain. Previous analyses of multiplicative responses in the owl have not taken into consideration the frequency-dependence of ITD and ILD cues that occur under natural listening conditions. Here, we present a model for the responses of ITD- and ILD-sensitive neurons in the barn owl''s inferior colliculus which satisfies constraints raised by experimental data on frequency convergence, multiplicative interaction of ITD and ILD, and response properties of afferent neurons. We propose that multiplication between ITD- and ILD-dependent signals occurs only within frequency channels and that frequency integration occurs using a linear-threshold mechanism. The model reproduces the experimentally observed nonlinear responses to ITD and ILD in the inferior colliculus, with greater accuracy than previous models. We show that linear-threshold frequency integration allows the system to represent multiple sound sources with natural sound localization cues, whereas multiplicative frequency integration does not. Nonlinear responses in the owl''s inferior colliculus can thus be generated using a combination of cellular and network mechanisms, showing that multiple elements of previous theories can be combined in a single system.     

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。