Fast detection of unexpected sound intensity decrements as revealed by human evoked potentials

The detection of deviant sounds is a crucial function of the auditory system and is reflected by the automatically elicited mismatch negativity (MMN), an auditory evoked potential at 100 to 250 ms from stimulus onset. It has recently been shown that rarely occurring frequency and location deviants in an oddball paradigm trigger a more negative response than standard sounds at very early latencies in the middle latency response of the human auditory evoked potential. This fast and early ability of the auditory system is corroborated by the finding of neurons in the animal auditory cortex and subcortical structures, which restore their adapted responsiveness to standard sounds, when a rare change in a sound feature occurs. In this study, we investigated whether the detection of intensity deviants is also reflected at shorter latencies than those of the MMN. Auditory evoked potentials in response to click sounds were analyzed regarding the auditory brain stem response, the middle latency response (MLR) and the MMN. Rare stimuli with a lower intensity level than standard stimuli elicited (in addition to an MMN) a more negative potential in the MLR at the transition from the Na to the Pa component at circa 24 ms from stimulus onset. This finding, together with the studies about frequency and location changes, suggests that the early automatic detection of deviant sounds in an oddball paradigm is a general property of the auditory system.     

A blueprint for vocal learning: auditory predispositions from brains to genomes

Memorizing and producing complex strings of sound are requirements for spoken human language. We share these behaviours with likely more than 4000 species of songbirds, making birds our primary model for studying the cognitive basis of vocal learning and, more generally, an important model for how memories are encoded in the brain. In songbirds, as in humans, the sounds that a juvenile learns later in life depend on auditory memories formed early in development. Experiments on a wide variety of songbird species suggest that the formation and lability of these auditory memories, in turn, depend on auditory predispositions that stimulate learning when a juvenile hears relevant, species-typical sounds. We review evidence that variation in key features of these auditory predispositions are determined by variation in genes underlying the development of the auditory system. We argue that increased investigation of the neuronal basis of auditory predispositions expressed early in life in combination with modern comparative genomic approaches may provide insights into the evolution of vocal learning.     

Constructing Noise-Invariant Representations of Sound in the Auditory Pathway

Identifying behaviorally relevant sounds in the presence of background noise is one of the most important and poorly understood challenges faced by the auditory system. An elegant solution to this problem would be for the auditory system to represent sounds in a noise-invariant fashion. Since a major effect of background noise is to alter the statistics of the sounds reaching the ear, noise-invariant representations could be promoted by neurons adapting to stimulus statistics. Here we investigated the extent of neuronal adaptation to the mean and contrast of auditory stimulation as one ascends the auditory pathway. We measured these forms of adaptation by presenting complex synthetic and natural sounds, recording neuronal responses in the inferior colliculus and primary fields of the auditory cortex of anaesthetized ferrets, and comparing these responses with a sophisticated model of the auditory nerve. We find that the strength of both forms of adaptation increases as one ascends the auditory pathway. To investigate whether this adaptation to stimulus statistics contributes to the construction of noise-invariant sound representations, we also presented complex, natural sounds embedded in stationary noise, and used a decoding approach to assess the noise tolerance of the neuronal population code. We find that the code for complex sounds in the periphery is affected more by the addition of noise than the cortical code. We also find that noise tolerance is correlated with adaptation to stimulus statistics, so that populations that show the strongest adaptation to stimulus statistics are also the most noise-tolerant. This suggests that the increase in adaptation to sound statistics from auditory nerve to midbrain to cortex is an important stage in the construction of noise-invariant sound representations in the higher auditory brain.     

Neural Correlates of Auditory Perceptual Awareness under Informational Masking

Our ability to detect target sounds in complex acoustic backgrounds is often limited not by the ear's resolution, but by the brain's information-processing capacity. The neural mechanisms and loci of this “informational masking” are unknown. We combined magnetoencephalography with simultaneous behavioral measures in humans to investigate neural correlates of informational masking and auditory perceptual awareness in the auditory cortex. Cortical responses were sorted according to whether or not target sounds were detected by the listener in a complex, randomly varying multi-tone background known to produce informational masking. Detected target sounds elicited a prominent, long-latency response (50–250 ms), whereas undetected targets did not. In contrast, both detected and undetected targets produced equally robust auditory middle-latency, steady-state responses, presumably from the primary auditory cortex. These findings indicate that neural correlates of auditory awareness in informational masking emerge between early and late stages of processing within the auditory cortex.     

Neural correlates of auditory perceptual awareness under informational masking

Our ability to detect target sounds in complex acoustic backgrounds is often limited not by the ear's resolution, but by the brain's information-processing capacity. The neural mechanisms and loci of this “informational masking” are unknown. We combined magnetoencephalography with simultaneous behavioral measures in humans to investigate neural correlates of informational masking and auditory perceptual awareness in the auditory cortex. Cortical responses were sorted according to whether or not target sounds were detected by the listener in a complex, randomly varying multi-tone background known to produce informational masking. Detected target sounds elicited a prominent, long-latency response (50–250 ms), whereas undetected targets did not. In contrast, both detected and undetected targets produced equally robust auditory middle-latency, steady-state responses, presumably from the primary auditory cortex. These findings indicate that neural correlates of auditory awareness in informational masking emerge between early and late stages of processing within the auditory cortex.     

Modeling complex tone perception: grouping harmonics with combination-sensitive neurons

 Perception of complex communication sounds is a major function of the auditory system. To create a coherent percept of these sounds the auditory system may instantaneously group or bind multiple harmonics within complex sounds. This perception strategy simplifies further processing of complex sounds and facilitates their meaningful integration with other sensory inputs. Based on experimental data and a realistic model, we propose that associative learning of combinations of harmonic frequencies and nonlinear facilitation of responses to those combinations, also referred to as “combination-sensitivity,” are important for spectral grouping. For our model, we simulated combination sensitivity using Hebbian and associative types of synaptic plasticity in auditory neurons. We also provided a parallel tonotopic input that converges and diverges within the network. Neurons in higher-order layers of the network exhibited an emergent property of multifrequency tuning that is consistent with experimental findings. Furthermore, this network had the capacity to “recognize” the pitch or fundamental frequency of a harmonic tone complex even when the fundamental frequency itself was missing. Received: 6 October 2001 / Accepted in revised form: 21 January 2002     

Encoding properties of auditory neurons in the brain of a soniferous damselfish: response to simple tones and complex conspecific signals

The fish auditory system encodes important acoustic stimuli used in social communication, but few studies have examined response properties of central auditory neurons to natural signals. We determined the features and responses of single hindbrain and midbrain auditory neurons to tone bursts and playbacks of conspecific sounds in the soniferous damselfish, Abudefduf abdominalis. Most auditory neurons were either silent or had slow irregular resting discharge rates <20 spikes s⁻¹. Average best frequency for neurons to tone stimuli was ~130 Hz but ranged from 80 to 400 Hz with strong phase-locking. This low-frequency sensitivity matches the frequency band of natural sounds. Auditory neurons were also modulated by playbacks of conspecific sounds with thresholds similar to 100 Hz tones, but these thresholds were lower than that of tones at other test frequencies. Thresholds of neurons to natural sounds were lower in the midbrain than the hindbrain. This is the first study to compare response properties of auditory neurons to both simple tones and complex stimuli in the brain of a recently derived soniferous perciform that lacks accessory auditory structures. These data demonstrate that the auditory fish brain is most sensitive to the frequency and temporal components of natural pulsed sounds that provide important signals for conspecific communication.     

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.     

Auditory processing of complex sounds: an overview.

The past 30 years has seen a remarkable development in our understanding of how the auditory system--particularly the peripheral system--processes complex sounds. Perhaps the most significant has been our understanding of the mechanisms underlying auditory frequency selectivity and their importance for normal and impaired auditory processing. Physiologically vulnerable cochlear filtering can account for many aspects of our normal and impaired psychophysical frequency selectivity with important consequences for the perception of complex sounds. For normal hearing, remarkable mechanisms in the organ of Corti, involving enhancement of mechanical tuning (in mammals probably by feedback of electro-mechanically generated energy from the hair cells), produce exquisite tuning, reflected in the tuning properties of cochlear nerve fibres. Recent comparisons of physiological (cochlear nerve) and psychophysical frequency selectivity in the same species indicate that the ear's overall frequency selectivity can be accounted for by this cochlear filtering, at least in bandwidth terms. Because this cochlear filtering is physiologically vulnerable, it deteriorates in deleterious conditions of the cochlea--hypoxia, disease, drugs, noise overexposure, mechanical disturbance--and is reflected in impaired psychophysical frequency selectivity. This is a fundamental feature of sensorineural hearing loss of cochlear origin, and is of diagnostic value. This cochlear filtering, particularly as reflected in the temporal patterns of cochlear fibres to complex sounds, is remarkably robust over a wide range of stimulus levels. Furthermore, cochlear filtering properties are a prime determinant of the 'place' and 'time' coding of frequency at the cochlear nerve level, both of which appear to be involved in pitch perception. The problem of how the place and time coding of complex sounds is effected over the ear's remarkably wide dynamic range is briefly addressed. In the auditory brainstem, particularly the dorsal cochlear nucleus, are inhibitory mechanisms responsible for enhancing the spectral and temporal contrasts in complex sounds. These mechanisms are now being dissected neuropharmacologically. At the cortical level, mechanisms are evident that are capable of abstracting biologically relevant features of complex sounds. Fundamental studies of how the auditory system encodes and processes complex sounds are vital to promising recent applications in the diagnosis and rehabilitation of the hearing impaired.     

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.     

Dynamic characteristics of the auditory cortex of guinea pigs observed with multichannel optical recording

The spatiotemporal characteristics of neural activity in the guinea pig auditory cortex are investigated to determine their importance in neural processing and coding of the complex sounds. A multi-channel optical recording system has been developed for observing the cortical field of the mammalian brain in vivo. Using the voltage-sensitive dye: RH795, optical imaging was used to visualize neural activity in the guinea pig auditory cortex. Experimental results reveal a boomerang-shaped pattern of movement of activated neural cell regions for the evoked response to click as complex sounds. Parallel and sequential neural processing structure was observed. Although the exact frequency selectivities of single cells and tonotopical organization observed using microelectrode were not visible, the similar feature to the microelectrode evidences was imaged by extracting the strongly response field from the optical data.     

Representation of complex vocalizations in the Lusitanian toadfish auditory system: evidence of fine temporal,frequency and amplitude discrimination

Many fishes rely on their auditory skills to interpret crucial information about predators and prey, and to communicate intraspecifically. Few studies, however, have examined how complex natural sounds are perceived in fishes. We investigated the representation of conspecific mating and agonistic calls in the auditory system of the Lusitanian toadfish Halobatrachus didactylus, and analysed auditory responses to heterospecific signals from ecologically relevant species: a sympatric vocal fish (meagre Argyrosomus regius) and a potential predator (dolphin Tursiops truncatus). Using auditory evoked potential (AEP) recordings, we showed that both sexes can resolve fine features of conspecific calls. The toadfish auditory system was most sensitive to frequencies well represented in the conspecific vocalizations (namely the mating boatwhistle), and revealed a fine representation of duration and pulsed structure of agonistic and mating calls. Stimuli and corresponding AEP amplitudes were highly correlated, indicating an accurate encoding of amplitude modulation. Moreover, Lusitanian toadfish were able to detect T. truncatus foraging sounds and A. regius calls, although at higher amplitudes. We provide strong evidence that the auditory system of a vocal fish, lacking accessory hearing structures, is capable of resolving fine features of complex vocalizations that are probably important for intraspecific communication and other relevant stimuli from the auditory scene.     

Auditory processing in anurans.

Anurans (frogs and toads) represent an example of peripheral specialization of the auditory systems. Their inner ear contains two distinct auditory organs: the amphibian papilla and the basilar papilla. Each organ is tuned to different species-specific frequency ranges. Because of this peripheral specialization, anurans offer an excellent opportunity to explore neural decoding of complex sounds in the central auditory system.     

Event-related potentials in an auditory oddball situation in the rat

Evoked potentials were recorded from the auditory cortex of both freely moving and anesthetized rats when deviant sounds were presented in a homogenous series of standard sounds (oddball condition). A component of the evoked response to deviant sounds, the mismatch negativity (MMN), may underlie the ability to discriminate acoustic differences, a fundamental aspect of auditory perception. Whereas most MMN studies in animals have been done using simple sounds, this study involved a more complex set of sounds (synthesized vowels). The freely moving rats had previously undergone behavioral training in which they learned to respond differentially to these sounds. Although we found little evidence in this preparation for the typical, epidurally recorded, MMN response, a significant difference between deviant and standard evoked potentials was noted for the freely moving animals in the 100-200 ms range following stimulus onset. No such difference was found in the anesthetized animals.     

On the Relevance of Natural Stimuli for the Study of Brainstem Correlates: The Example of Consonance Perception

Some combinations of musical tones sound pleasing to Western listeners, and are termed consonant, while others sound discordant, and are termed dissonant. The perceptual phenomenon of consonance has been traced to the acoustic property of harmonicity. It has been repeatedly shown that neural correlates of consonance can be found as early as the auditory brainstem as reflected in the harmonicity of the scalp-recorded frequency-following response (FFR). “Neural Pitch Salience” (NPS) measured from FFRs—essentially a time-domain equivalent of the classic pattern recognition models of pitch—has been found to correlate with behavioral judgments of consonance for synthetic stimuli. Following the idea that the auditory system has evolved to process behaviorally relevant natural sounds, and in order to test the generalizability of this finding made with synthetic tones, we recorded FFRs for consonant and dissonant intervals composed of synthetic and natural stimuli. We found that NPS correlated with behavioral judgments of consonance and dissonance for synthetic but not for naturalistic sounds. These results suggest that while some form of harmonicity can be computed from the auditory brainstem response, the general percept of consonance and dissonance is not captured by this measure. It might either be represented in the brainstem in a different code (such as place code) or arise at higher levels of the auditory pathway. Our findings further illustrate the importance of using natural sounds, as a complementary tool to fully-controlled synthetic sounds, when probing auditory perception.     

Auditory neuroscience: sound segregation in the brainstem?

Separating a mixture of sounds into its constituent parts is a complex process likely to involve many processing stages. A new study suggests that the first steps in that process may occur already at the level of the first auditory processing centre in the brainstem.     

Directed attention eliminates 'change deafness' in complex auditory scenes

In natural environments that contain multiple sound sources, acoustic energy arising from the different sources sums to produce a single complex waveform at each of the listener's ears. The auditory system must segregate this waveform into distinct streams to permit identification of the objects from which the signals emanate [1]. Although the processes involved in stream segregation are now reasonably well understood [1, 2 and 3], little is known about the nature of our perception of complex auditory scenes. Here, we examined complex scene perception by having listeners detect a discrete change to an auditory scene comprising multiple concurrent naturalistic sounds. We found that listeners were remarkably poor at detecting the disappearance of an individual auditory object when listening to scenes containing more than four objects, but they performed near perfectly when their attention was directed to the identity of a potential change. In the absence of directed attention, this "change deafness" [4] was greater for objects arising from a common location in space than for objects separated in azimuth. Change deafness was also observed for changes in object location, suggesting that it may reflect a general effect of the dependence of human auditory perception on attention.     

Representation of Sound Objects within Early-Stage Auditory Areas: A Repetition Effect Study Using 7T fMRI

Environmental sounds are highly complex stimuli whose recognition depends on the interaction of top-down and bottom-up processes in the brain. Their semantic representations were shown to yield repetition suppression effects, i. e. a decrease in activity during exposure to a sound that is perceived as belonging to the same source as a preceding sound. Making use of the high spatial resolution of 7T fMRI we have investigated the representations of sound objects within early-stage auditory areas on the supratemporal plane. The primary auditory cortex was identified by means of tonotopic mapping and the non-primary areas by comparison with previous histological studies. Repeated presentations of different exemplars of the same sound source, as compared to the presentation of different sound sources, yielded significant repetition suppression effects within a subset of early-stage areas. This effect was found within the right hemisphere in primary areas A1 and R as well as two non-primary areas on the antero-medial part of the planum temporale, and within the left hemisphere in A1 and a non-primary area on the medial part of Heschl’s gyrus. Thus, several, but not all early-stage auditory areas encode the meaning of environmental sounds.     

Large-Scale Analysis of Auditory Segregation Behavior Crowdsourced via a Smartphone App

The human auditory system is adept at detecting sound sources of interest from a complex mixture of several other simultaneous sounds. The ability to selectively attend to the speech of one speaker whilst ignoring other speakers and background noise is of vital biological significance—the capacity to make sense of complex ‘auditory scenes’ is significantly impaired in aging populations as well as those with hearing loss. We investigated this problem by designing a synthetic signal, termed the ‘stochastic figure-ground’ stimulus that captures essential aspects of complex sounds in the natural environment. Previously, we showed that under controlled laboratory conditions, young listeners sampled from the university subject pool (n = 10) performed very well in detecting targets embedded in the stochastic figure-ground signal. Here, we presented a modified version of this cocktail party paradigm as a ‘game’ featured in a smartphone app (The Great Brain Experiment) and obtained data from a large population with diverse demographical patterns (n = 5148). Despite differences in paradigms and experimental settings, the observed target-detection performance by users of the app was robust and consistent with our previous results from the psychophysical study. Our results highlight the potential use of smartphone apps in capturing robust large-scale auditory behavioral data from normal healthy volunteers, which can also be extended to study auditory deficits in clinical populations with hearing impairments and central auditory disorders.