A common periodic representation of interaural time differences in mammalian cortex

Binaural hearing, the ability to detect small differences in the timing and level of sounds at the two ears, underpins the ability to localize sound sources along the horizontal plane, and is important for decoding complex spatial listening environments into separate objects - a critical factor in 'cocktail-party listening'. For human listeners, the most important spatial cue is the interaural time difference (ITD). Despite many decades of neurophysiological investigations of ITD sensitivity in small mammals, and computational models aimed at accounting for human perception, a lack of concordance between these studies has hampered our understanding of how the human brain represents and processes ITDs. Further, neural coding of spatial cues might depend on factors such as head-size or hearing range, which differ considerably between humans and commonly used experimental animals. Here, using magnetoencephalography (MEG) in human listeners, and electro-corticography (ECoG) recordings in guinea pig-a small mammal representative of a range of animals in which ITD coding has been assessed at the level of single-neuron recordings-we tested whether processing of ITDs in human auditory cortex accords with a frequency-dependent periodic code of ITD reported in small mammals, or whether alternative or additional processing stages implemented in psychoacoustic models of human binaural hearing must be assumed. Our data were well accounted for by a model consisting of periodically tuned ITD-detectors, and were highly consistent across the two species. The results suggest that the representation of ITD in human auditory cortex is similar to that found in other mammalian species, a representation in which neural responses to ITD are determined by phase differences relative to sound frequency rather than, for instance, the range of ITDs permitted by head size or the absolute magnitude or direction of ITD

The organization of frequency and binaural cues in the gerbil inferior colliculus: GRAÑA et al.

The inferior colliculus (IC) is the common target of separate pathways that transmit different types of auditory information. Beyond tonotopy, little is known about the organization of response properties within the 3-dimensional layout of the auditory midbrain in most species. Through study of interaural time difference (ITD) processing, the functional properties of neurons can be readily characterized and related to specific pathways. To characterize the representation of ITDs relative to the frequency and hodological organization of the IC, the properties of neurons were recorded and the sites recovered histologically. Subdivisions of the IC were identified based on cytochrome oxidase (CO) histochemistry. The results were plotted within a framework formed by an MRI atlas of the gerbil brain. The central nucleus was composed of two parts, and lateral and dorsal cortical areas were identified. The lateral part of the central nucleus had the highest CO activity in the IC and a high proportion of neurons sensitive to ITDs. The medial portion had lower CO activity and fewer ITD-sensitive neurons. A common tonotopy with a dorsolateral to ventromedial gradient of low to high frequencies spanned the two regions. The distribution of physiological responses was in close agreement with known patterns of ascending inputs. An understanding of the 3-dimensional organization of the IC is needed to specify how the single tonotopic representation in the IC central nucleus leads to the multiple tonotopic representations in core areas of the auditory cortex

J Neurosci

The brainstem auditory pathway is obligatory for all aural information. Brainstem auditory neurons must encode the level and timing of sounds, as well as their time-dependent spectral properties, the fine structure, and envelope, which are essential for sound discrimination. This study focused on envelope coding in the two cochlear nuclei of the barn owl, nucleus angularis (NA) and nucleus magnocellularis (NM). NA and NM receive input from bifurcating auditory nerve fibers and initiate processing pathways specialized in encoding interaural time (ITD) and level (ILD) differences, respectively. We found that NA neurons, although unable to accurately encode stimulus phase, lock more strongly to the stimulus envelope than NM units. The spectrotemporal receptive fields (STRFs) of NA neurons exhibit a pre-excitatory suppressive field. Using multilinear regression analysis and computational modeling, we show that this feature of STRFs can account for enhanced across-trial response reliability, by locking spikes to the stimulus envelope. Our findings indicate a dichotomy in envelope coding between the time and intensity processing pathways as early as at the level of the cochlear nuclei. This allows the ILD processing pathway to encode envelope information with greater fidelity than the ITD processing pathway. Furthermore, we demonstrate that the properties of the STRFs of the neurons can be quantitatively related to spike timing reliability.CD007690/CD/ODCDC CDC HHS/United StatesR01 DC007690/DC/NIDCD NIH HHS/United StatesR01 DC007690-06A1/DC/NIDCD NIH HHS/United StatesR01 DC007690-07/DC/NIDCD NIH HHS/United StatesT32 GM007288/GM/NIGMS NIH HHS/United States2011-09-02T00:00:00Z21368035PMC305980

Importance of spike timing in touch: an analogy with hearing?

Touch is often conceived as a spatial sense akin to vision. However, touch also involves the transduction and processing of signals that vary rapidly over time, inviting comparisons with hearing. In both sensory systems, first order afferents produce spiking responses that are temporally precise and the timing of their responses carries stimulus information. The precision and informativeness of spike timing in the two systems invites the possibility that both implement similar mechanisms to extract behaviorally relevant information from these precisely timed responses. Here, we explore the putative roles of spike timing in touch and hearing and discuss common mechanisms that may be involved in processing temporal spiking patterns

Neural coding of pitch cues in the auditory midbrain of unanesthetized rabbits

Pitch is an important attribute of auditory perception that conveys key features in music, speech, and helps listeners extract useful information from complex auditory environments. Although the psychophysics of pitch perception has been extensively studied for over a century, the underlying neural mechanisms are still poorly understood. This thesis examines pitch cues in the inferior colliculus (IC), which is the core processing center in the mammalian auditory midbrain that relays and transforms convergent inputs from peripheral brainstem nuclei to the auditory cortex. Previous studies have shown that IC can encode low-frequency fluctuations in stimulus envelope that are related to pitch, but most experiments were conducted in anesthetized animals using stimuli that only evoked weak pitch sensations and only investigated a limited frequency range. Here, we used single-neuron recordings from the IC in normal hearing, unanesthetized rabbits in response to a comprehensive set of complex auditory stimuli to explore the role of IC in the neural processing of pitch. We characterized three neural codes for pitch cues: a temporal code for the stimulus envelope repetition rate (ERR) below 900 Hz, a rate code for ERR between 60 and 1600 Hz, and a rate-place code for frequency components individually resolved by the cochlea that is mainly available above 800 Hz. While the temporal code and the rate-place code are inherited from the auditory periphery, the rate code for ERR has not been currently characterized in processing stages prior to the IC. To help interpret our experimental findings, we used computational models to show that the IC rate code for ERR likely arises via temporal interaction of multiple synaptic inputs, and thus the IC performs a temporal-to-rate code transformation from peripheral to cortical representations of pitch cues. We also show that the IC rate-place code is robust across a 40 dB range of sound levels, and is likely strengthened by inhibitory synaptic inputs. Together, these three codes could provide neural substrates for pitch of stimuli with various temporal and spectral compositions over the entire frequency range

Neural Models of Subcortical Auditory Processing

An important feature of the auditory system is its ability to distinguish many simultaneous sound sources. The primary goal of this work was to understand how a robust, preattentive analysis of the auditory scene is accomplished by the subcortical auditory system. Reasonably accurate modelling of the morphology and organisation of the relevant auditory nuclei, was seen as being of great importance. The formulation of plausible models and their subsequent simulation was found to be invaluable in elucidating biological processes and in highlighting areas of uncertainty. In the thesis, a review of important aspects of mammalian auditory processing is presented and used as a basis for the subsequent modelling work. For each aspect of auditory processing modelled, psychophysical results are described and existing models reviewed, before the models used here are described and simulated. Auditory processes which are modelled include the peripheral system, and the production of tonotopic maps of the spectral content of complex acoustic stimuli, and of modulation frequency or periodicity. A model of the formation of sequential associations between successive sounds is described, and the model is shown to be capable of emulating a wide range of psychophysical behaviour. The grouping of related spectral components and the development of pitch perception is also investigated. Finally a critical assessment of the work and ideas for future developments are presented. The principal contributions of this work are the further development of a model for pitch perception and the development of a novel architecture for the sequential association of those groups. In the process of developing these ideas, further insights into subcortical auditory processing were gained, and explanations for a number of puzzling psychophysical characteristics suggested.Royal Naval Engineering College, Manadon, Plymout

Towards understanding the role of central processing in release from masking

People with normal hearing have the ability to listen to a desired target sound while filtering out unwanted sounds in the background. However, most patients with hearing impairment struggle in noisy environments, a perceptual deficit which current hearing aids and cochlear implants cannot resolve. Even though peripheral dysfunction of the ears undoubtedly contribute to this deficit, surmounting evidence has implicated central processing in the inability to detect sounds in background noise. Therefore, it is essential to better understand the underlying neural mechanisms by which target sounds are dissociated from competing maskers. This research focuses on two phenomena that help suppress background sounds: 1) dip-listening, and 2) directional hearing. When background noise fluctuates slowly over time, both humans and animals can listen in the dips of the noise envelope to detect target sound, a phenomenon referred to as dip-listening. Detection of target sound is facilitated by a central neuronal mechanism called envelope locking suppression. At both positive and negative signal-to-noise ratios (SNRs), the presence of target energy can suppress the strength by which neurons in auditory cortex track background sound, at least in anesthetized animals. However, in humans and animals, most of the perceptual advantage gained by listening in the dips of fluctuating noise emerges when a target is softer than the background sound. This raises the possibility that SNR shapes the reliance on different processing strategies, a hypothesis tested here in awake behaving animals. Neural activity of Mongolian gerbils is measured by chronic implantation of silicon probes in the core auditory cortex. Using appetitive conditioning, gerbils detect target tones in the presence of temporally fluctuating amplitude-modulated background noise, called masker. Using rate- vs. timing-based decoding strategies, analysis of single-unit activity show that both mechanisms can be used for detecting tones at positive SNR. However, only temporal decoding provides an SNR-invariant readout strategy that is viable at both positive and negative SNRs. In addition to dip-listening, spatial cues can facilitate the dissociation of target sounds from background noise. Specifically, an important cue for computing sound direction is the time difference in arrival of acoustic energy reaching each ear, called interaural time difference (ITD). ITDs allow localization of low frequency sounds from left to right inside the listener\u27s head, also called sound lateralization. Models of sound localization commonly assume that sound lateralization from interaural time differences is level invariant. Here, two prevalent theories of sound localization are observed to make opposing predictions. The labelled-line model encodes location through tuned representations of spatial location and predicts that perceived direction is level invariant. In contrast, the hemispheric-difference model encodes location through spike-rate and predicts that perceived direction becomes medially biased at low sound levels. In this research, through behavioral experiments on sound lateralization, the computation of sound location with ITDs is tested. Four groups of normally hearing listeners lateralize sounds based on ITDs as a function of sound intensity, exposure hemisphere, and stimulus history. Stimuli consists of low-frequency band-limited white noise. Statistical analysis, which partial out overall differences between listeners, is inconsistent with the place-coding scheme of sound localization, and supports the hypothesis that human sound localization is instead encoded through a population rate-code