Coding of auditory space

Behavioral, anatomical, and physiological approaches can be integrated in the study of sound localization in barn owls. Space representation in owls provides a useful example for discussion of place and ensemble coding. Selectivity for space is broad and ambiguous in low-order neurons. Parallel pathways for binaural cues and for different frequency bands converge on high-order space-specific neurons, which encode space more precisely. An ensemble of broadly tuned place-coding neurons may converge on a single high-order neuron to create an improved labeled line. Thus, the two coding schemes are not alternate methods. Owls can localize sounds by using either the isomorphic map of auditory space in the midbrain or forebrain neural networks in which space is not mapped

The functional role of GABA and glycine in monaural and binaural processing in the inferior colliculus of horseshoe bats

The functional role of GABA and glycine in monaural and binaural signal analysis was studied in single unit recordings from the central nucleus of the inferior colliculus (IC) of horseshoe bats (Rhinolophus rouxi) employing microiontophoresis of the putative neurotransmitters and their antagonists bicuculline and strychnine. Most neurons were inhibited by GABA (98%; N= 107) and glycine (92%; N = 118). Both neurotransmitters appear involved in several functional contexts, but to different degrees. Bicuculline-induced increases of discharge activity (99% of cells; N= 191) were accompanied by changes of temporal response patterns in 35 % of neurons distributed throughout the IC. Strychnine enhanced activity in only 53% of neurons (N= 147); cells exhibiting response pattern changes were rare (9%) and confined to greater recording depths. In individual cells, the effects of both antagonists could markedly differ, suggesting a differential supply by GABAergic and glycinergic networks. Bicuculline changed the shape of the excitatory tuning curve by antagonizing lateral inhibition at neighboring frequencies and/or inhibition at high stimulation levels. Such effects were rarely observed with strychnine. Binaural response properties of single units were influenced either by antagonization of inhibition mediated by ipsilateral stimulation (bicuculline) or by changing the strength of the main excitatory input (bicuculline and strychnine)

On the mechanism of response latencies in auditory nerve fibers

Despite the structural differences of the middle and inner ears, the latency pattern in auditory nerve fibers to an identical sound has been found similar across numerous species. Studies have shown the similarity in remarkable species with distinct cochleae or even without a basilar membrane. This stimulus-, neuron-, and species- independent similarity of latency cannot be simply explained by the concept of cochlear traveling waves that is generally accepted as the main cause of the neural latency pattern. An original concept of Fourier pattern is defined, intended to characterize a feature of temporal processing—specifically phase encoding—that is not readily apparent in more conventional analyses. The pattern is created by marking the first amplitude maximum for each sinusoid component of the stimulus, to encode phase information. The hypothesis is that the hearing organ serves as a running analyzer whose output reflects synchronization of auditory neural activity consistent with the Fourier pattern. A combined research of experimental, correlational and meta-analysis approaches is used to test the hypothesis. Manipulations included phase encoding and stimuli to test their effects on the predicted latency pattern. Animal studies in the literature using the same stimulus were then compared to determine the degree of relationship. The results show that each marking accounts for a large percentage of a corresponding peak latency in the peristimulus-time histogram. For each of the stimuli considered, the latency predicted by the Fourier pattern is highly correlated with the observed latency in the auditory nerve fiber of representative species. The results suggest that the hearing organ analyzes not only amplitude spectrum but also phase information in Fourier analysis, to distribute the specific spikes among auditory nerve fibers and within a single unit. This phase-encoding mechanism in Fourier analysis is proposed to be the common mechanism that, in the face of species differences in peripheral auditory hardware, accounts for the considerable similarities across species in their latency-by-frequency functions, in turn assuring optimal phase encoding across species. Also, the mechanism has the potential to improve phase encoding of cochlear implants

Sparse Codes for Speech Predict Spectrotemporal Receptive Fields in the Inferior Colliculus

We have developed a sparse mathematical representation of speech that minimizes the number of active model neurons needed to represent typical speech sounds. The model learns several well-known acoustic features of speech such as harmonic stacks, formants, onsets and terminations, but we also find more exotic structures in the spectrogram representation of sound such as localized checkerboard patterns and frequency-modulated excitatory subregions flanked by suppressive sidebands. Moreover, several of these novel features resemble neuronal receptive fields reported in the Inferior Colliculus (IC), as well as auditory thalamus and cortex, and our model neurons exhibit the same tradeoff in spectrotemporal resolution as has been observed in IC. To our knowledge, this is the first demonstration that receptive fields of neurons in the ascending mammalian auditory pathway beyond the auditory nerve can be predicted based on coding principles and the statistical properties of recorded sounds.Comment: For Supporting Information, see PLoS website: http://www.ploscompbiol.org/article/info%3Adoi%2F10.1371%2Fjournal.pcbi.100259

Computation of Interaural Time Difference in the Owl's Coincidence Detector Neurons

Both the mammalian and avian auditory systems localize sound sources by computing the interaural time difference (ITD) with submillisecond accuracy. The neural circuits for this computation in birds consist of axonal delay lines and coincidence detector neurons. Here, we report the first in vivo intracellular recordings from coincidence detectors in the nucleus laminaris of barn owls. Binaural tonal stimuli induced sustained depolarizations (DC) and oscillating potentials whose waveforms reflected the stimulus. The amplitude of this sound analog potential (SAP) varied with ITD, whereas DC potentials did not. The amplitude of the SAP was correlated with firing rate in a linear fashion. Spike shape, synaptic noise, the amplitude of SAP, and responsiveness to current pulses differed between cells at different frequencies, suggesting an optimization strategy for sensing sound signals in neurons tuned to different frequencies

Enhancement of forward suppression begins in the ventral cochlear nucleus.

A neuron׳s response to a sound can be suppressed by the presentation of a preceding sound. It has been suggested that this suppression is a direct correlate of the psychophysical phenomenon of forward masking, however, forward suppression, as measured in the responses of the auditory nerve, was insufficient to account for behavioural performance. In contrast the neural suppression seen in the inferior colliculus and auditory cortex was much closer to psychophysical performance. In anaesthetised guinea-pigs, using a physiological two-interval forced-choice threshold tracking algorithm to estimate suppressed (masked) thresholds, we examine whether the enhancement of suppression can occur at an earlier stage of the auditory pathway, the ventral cochlear nucleus (VCN). We also compare these responses with the responses from the central nucleus of the inferior colliculus (ICc) using the same preparation. In both nuclei, onset-type neurons showed the greatest amounts of suppression (16.9-33.5dB) and, in the VCN, these recovered with the fastest time constants (14.1-19.9ms). Neurons with sustained discharge demonstrated reduced masking (8.9-12.1dB) and recovery time constants of 27.2-55.6ms. In the VCN the decrease in growth of suppression with increasing suppressor level was largest for chopper units and smallest for onset-type units. The threshold elevations recorded for most unit types are insufficient to account for the magnitude of forward masking as measured behaviourally, however, onset responders, in both the cochlear nucleus and inferior colliculus demonstrate a wide dynamic range of suppression, similar to that observed in human psychophysics.This work was supported by Wellcome Trust and BBSRC Project Grants to IMW and first presented in preliminary form by Ingham et al. (2006b). We thank Elinor Gunning and Catherine Slattery for their help and input during pilot experiments and Mark Sayles for help in data collection in later experiments.This is the final version of the article. It first appeared from Elsevier via https://doi.org/10.1016/j.brainres.2016.02.04

Dual Coding of Frequency Modulation in the Ventral Cochlear Nucleus.

Frequency modulation (FM) is a common acoustic feature of natural sounds and is known to play a role in robust sound source recognition. Auditory neurons show precise stimulus-synchronized discharge patterns that may be used for the representation of low-rate FM. However, it remains unclear whether this representation is based on synchronization to slow temporal envelope (ENV) cues resulting from cochlear filtering or phase locking to faster temporal fine structure (TFS) cues. To investigate the plausibility of those encoding schemes, single units of the ventral cochlear nucleus of guinea pigs of either sex were recorded in response to sine FM tones centered at the unit's best frequency (BF). The results show that, in contrast to high-BF units, for modulation depths within the receptive field, low-BF units (<4 kHz) demonstrate good phase locking to TFS. For modulation depths extending beyond the receptive field, the discharge patterns follow the ENV and fluctuate at the modulation rate. The receptive field proved to be a good predictor of the ENV responses for most primary-like and chopper units. The current in vivo data also reveal a high level of diversity in responses across unit types. TFS cues are mainly conveyed by low-frequency and primary-like units and ENV cues by chopper and onset units. The diversity of responses exhibited by cochlear nucleus neurons provides a neural basis for a dual-coding scheme of FM in the brainstem based on both ENV and TFS cues.SIGNIFICANCE STATEMENT Natural sounds, including speech, convey informative temporal modulations in frequency. Understanding how the auditory system represents those frequency modulations (FM) has important implications as robust sound source recognition depends crucially on the reception of low-rate FM cues. Here, we recorded 115 single-unit responses from the ventral cochlear nucleus in response to FM and provide the first physiological evidence of a dual-coding mechanism of FM via synchronization to temporal envelope cues and phase locking to temporal fine structure cues. We also demonstrate a diversity of neural responses with different coding specializations. These results support the dual-coding scheme proposed by psychophysicists to account for FM sensitivity in humans and provide new insights on how this might be implemented in the early stages of the auditory pathway

Impact of aging on the auditory system and related cognitive functions: A narrative review

Age-related hearing loss (ARHL), presbycusis, is a chronic health condition that affects approximately one-third of the world’s population. The peripheral and central hearing alterations associated with age-related hearing loss have a profound impact on perception of verbal and non-verbal auditory stimuli. The high prevalence of hearing loss in the older adults corresponds to the increased frequency of dementia in this population. Therefore, researchers have focused their attention on age-related central effects that occur independent of the peripheral hearing loss as well as central effects of peripheral hearing loss and its association with cognitive decline and dementia. Here we review the current evidence for the age-related changes of the peripheral and central auditory system and the relationship between hearing loss and pathological cognitive decline and dementia. Furthermore, there is a paucity of evidence on the relationship between ARHL and established biomarkers of Alzheimer’s disease, as the most common cause of dementia. Such studies are critical to be able to consider any causal relationship between dementia and ARHL. While this narrative review will examine the pathophysiological alterations in both the peripheral and central auditory system and its clinical implications, the question remains unanswered whether hearing loss causes cognitive impairment or vice versa