Christian J. Sumner

A revised model of the inner-hair cell and auditory-nerve complex

A revised computational model of the inner-hair cell (IHC) and auditory-nerve (AN) complex is presented and evaluated. Building on previous models, the algorithm is intended as a component for use in more comprehensive models of the auditory periphery. It combines smaller components that aim to be faithful to physiology in so far as is practicable and known. Transduction between cochlear mechanical motion and IHC receptor potential (RP) is simulated using a modification of an existing biophysical IHC model. Changes in RP control the opening of calcium ion channels near the synapse, and local calcium levels determine the probability of the release of neurotransmitter. AN adaptation results from transmitter depletion. The exact timing of AN action potentials is determined by the quantal and stochastic release of neurotransmitter into the cleft. The model reproduces a wide range of animal RP and AN observations. When the input to the model is taken from a suitably nonlinear simulation of the motion of the cochlear partition, the new algorithm is able to simulate the rate-intensity functions of low-, medium-, and high-spontaneous rate AN fibers in response to stimulation both at best frequency and at other frequencies. The variation in fiber type arises in large part from the manipulation of a single parameter in the model: maximum calcium conductance. The model also reproduces quantitatively phase-locking characteristics, relative refractory effects, mean-to-variance ratio, and first- and second-order discharge history effects.

A nonlinear filter-bank model of the guinea-pig cochlear nerve: Rate responses

The aim of this study is to produce a functional model of the auditory nerve (AN) response of the guinea-pig that reproduces a wide range of important responses to auditory stimulation. The model is intended for use as an input to larger scale models of auditory processing in the brain-stem. A dual-resonance nonlinear filter architecture is used to reproduce the mechanical tuning of the cochlea. Transduction to the activity on the AN is accomplished with a recently proposed model of the inner-hair-cell. Together, these models have been shown to be able to reproduce the response of high-, medium-, and low-spontaneous rate fibers from the guinea-pig AN at high best frequencies (BFs). In this study we generate parameters that allow us to fit the AN model to data from a wide range of BFs. By varying the characteristics of the mechanical filtering as a function of the BF it was possible to reproduce the BF dependence of frequency-threshold tuning curves, AN rate-intensity functions at and away from BF, compression of the basilar membrane at BF as inferred from AN responses, and AN iso-intensity functions. The model is a convenient computational tool for the simulation of the range of nonlinear tuning and rate-responses found across the length of the guinea-pig cochlear nerve.

Examining the role of frequency specificity in the enhancement and suppression of human cortical activity by auditory selective attention

This study examined the neural basis of auditory selective attention using functional magnetic resonance imaging. The main hypothesis stated that attending to a particular sound frequency would significantly enhance the neural response within those tonotopic regions of the auditory cortex sensitive to that frequency. To test this prediction, low- and high-frequency sound sequences were interleaved to produce two concurrent auditory streams. Six normally hearing participants either performed a task which required them to attend to one or the other stream or listened passively to the sounds while functional images were acquired using a high-resolution (1.5 mm x 1.5 mm x 2.5 mm) sequence. Two statistical comparisons identified the attention-specific and general effects of enhancement. The first controlled for task-related processes, while the second did not. Results demonstrated frequency-specific, attention-specific enhancement in the response to the attended frequency, but no response suppression for the unattended frequency. Instead, a general effect of suppression was found in several posterior sites, possibly related to resting-state processes. Furthermore, there was widespread general enhancement across auditory cortex when performing the task compared to passive listening. This enhancement did include frequency-sensitive regions, but was not restricted to them. In conclusion, our results show partial support for frequency-specific enhancement.

Olivocochlear Efferent Control in Sound Localization and Experience-Dependent Learning

Efferent auditory pathways have been implicated in sound localization and its plasticity. We examined the role of the olivocochlear system (OC) in horizontal sound localization by the ferret and in localization learning following unilateral earplugging. Under anesthesia, adult ferrets underwent olivocochlear bundle section at the floor of the fourth ventricle, either at the midline or laterally (left). Lesioned and control animals were trained to localize 1 s and 40 ms amplitude-roved broadband noise stimuli from one of 12 loudspeakers. Neither type of lesion affected normal localization accuracy. All ferrets then received a left earplug and were tested and trained over 10 d. The plug profoundly disrupted localization. Ferrets in the control and lateral lesion groups improved significantly during subsequent training on the 1 s stimulus. No improvement (learning) occurred in the midline lesion group. Markedly poorer performance and failure to learn was observed with the 40 ms stimulus in all groups. Plug removal resulted in a rapid resumption of normal localization in all animals. Insertion of a subsequent plug in the right ear produced similar results to left earplugging. Learning in the lateral lesion group was independent of the side of the lesion relative to the earplug. Lesions in all reported cases were verified histologically. The results suggest the OC system is not needed for accurate localization, but that it is involved in relearning localization during unilateral conductive hearing loss.

Forward Masking Estimated by Signal Detection Theory Analysis of Neuronal Responses in Primary Auditory Cortex

Psychophysical forward masking is an increase in threshold of detection of a sound (probe) when it is preceded by another sound (masker). This is reminiscent of the reduction in neuronal responses to a sound following prior stimulation. Studies in the auditory nerve and cochlear nucleus using signal detection theory techniques to derive neuronal thresholds showed that in centrally projecting neurons, increases in masked thresholds were significantly smaller than the changes measured psychophysically. Larger threshold shifts have been reported in the inferior colliculus of awake marmoset. The present study investigated the magnitude of forward masking in primary auditory cortical neurons of anaesthetised guinea-pigs. Responses of cortical neurons to unmasked and forward masked tones were measured and probe detection thresholds estimated using signal detection theory methods. Threshold shifts were larger than in the auditory nerve, cochlear nucleus and inferior colliculus. The larger threshold shifts suggest that central, and probably cortical, processes contribute to forward masking. However, although methodological differences make comparisons difficult, the threshold shifts in cortical neurons were, in contrast to subcortical nuclei, actually larger than those observed psychophysically. Masking was largely attributable to a reduction in the responses to the probe, rather than either a persistence of the masker responses or an increase in the variability of probe responses.

Auditory nerve fibre responses in the ferret

The ferret (Mustela putorius) is a medium‐sized, carnivorous mammal with good low‐frequency hearing; it is relatively easy to train, and there is therefore a good body of behavioural data detailing its detection thresholds and localization abilities. However, despite extensive studies of the physiology of the central nervous system of the ferret, even extending to the prefrontal cortex, little is known of the functioning of the auditory periphery. Here, we provide an insight into this peripheral function by detailing responses of single auditory nerve fibres. Our expectation was that the ferret auditory nerve responsiveness would be similar that of its near relative, the cat. However, by comparing a range of variables (the frequency tuning, the variation of rate–level functions with spontaneous rate, and the high‐frequency cut‐off of phase locking) across several species, we show that the auditory nerve (and hence cochlea) in the ferret is more similar to that of the guinea‐pig and chinchilla than to that of the cat. Animal models of hearing are often chosen on the basis of the similarity of their audiogram to that of the human, particularly in the low‐frequency region. We show here that whereas the ferret hears well at low frequencies, this is likely to occur via fibres with higher characteristic frequencies. These qualitative differences in response characteristics in auditory nerve fibres are important in interpreting data across all of auditory science, as it has been argued recently that tuning in animals is broader than in humans.

Forward suppression in the auditory cortex is frequency‐specific

We investigated how physiologically observed forward suppression interacts with stimulus frequency in neuronal responses in the guinea pig auditory cortex. The temporal order and frequency proximity of sounds influence both their perception and neuronal responses. Psychophysically, preceding sounds (conditioners) can make successive sounds (probes) harder to hear. These effects are larger when the two sounds are spectrally similar. Physiological forward suppression is usually maximal for conditioner tones near to a unit’s characteristic frequency (CF), the frequency to which a neuron is most sensitive. However, in most physiological studies, the frequency of the probe tone and CF are identical, so the role of unit CF and probe frequency cannot be distinguished. Here, we systemically varied the frequency of the probe tone, and found that the tuning of suppression was often more closely related to the frequency of the probe tone than to the unit’s CF, i.e. suppressed tuning was specific to probe frequency. This relationship was maintained for all measured gaps between the conditioner and the probe tones. However, when the probe frequency and CF were similar, CF tended to determine suppressed tuning. In addition, the bandwidth of suppression was slightly wider for off‐CF probes. Changes in tuning were also reflected in the firing rate in response to probe tones, which was maximally reduced when probe and conditioner tones were matched in frequency. These data are consistent with the idea that cortical neurons receive convergent inputs with a wide range of tuning properties that can adapt independently.

Mode-Locked Spike Trains in Responses of Ventral Cochlear Nucleus Chopper and Onset Neurons to Periodic Stimuli

We report evidence of mode-locking to the envelope of a periodic stimulus in chopper units of the ventral cochlear nucleus (VCN). Mode-locking is a generalized description of how responses in periodically forced nonlinear systems can be closely linked to the input envelope, while showing temporal patterns of higher order than seen during pure phase-locking. Re-analyzing a previously unpublished dataset in response to amplitude modulated tones, we find that of 55% of cells (6/11) demonstrated stochastic mode-locking in response to sinusoidally amplitude modulated (SAM) pure tones at 50% modulation depth. At 100% modulation depth SAM, most units (3/4) showed mode-locking. We use interspike interval (ISI) scattergrams to unravel the temporal structure present in chopper mode-locked responses. These responses compared well to a leaky integrate-and-fire model (LIF) model of chopper units. Thus the timing of spikes in chopper unit responses to periodic stimuli can be understood in terms of the complex dynamics of periodically forced nonlinear systems. A larger set of onset (33) and chopper units (24) of the VCN also shows mode-locked responses to steady-state vowels and cosine-phase harmonic complexes. However, while 80% of chopper responses to complex stimuli meet our criterion for the presence of mode-locking, only 40% of onset cells show similar complex-modes of spike patterns. We found a correlation between a units regularity and its tendency to display mode-locked spike trains as well as a correlation in the number of spikes per cycle and the presence of complex-modes of spike patterns. These spiking patterns are sensitive to the envelope as well as the fundamental frequency of complex sounds, suggesting that complex cell dynamics may play a role in encoding periodic stimuli and envelopes in the VCN.

Classification of frequency response areas in the inferior colliculus reveals continua not discrete classes

•  Neurons in the auditory midbrain, the inferior colliculus, are selectively sensitive to combinations of sound frequency and level as illustrated by their frequency/level receptive fields. Different receptive field shapes have been described, but we do not know if these represent discrete classes reflecting afferent inputs from individual sources, or a more complex pattern of integration. •  In this study we used objective methods to analyse the receptive fields of over 2000 neurons in the guinea pig inferior colliculus. •  Subjectively we identified seven different receptive field classes, but objectively these classes formed continua with many neurons having receptive field shapes intermediate to these extremes. •  These findings are consistent with neurons receiving inhibitory inputs of different strength and frequency disposition but not consistent with neurons reflecting inputs only from individual brainstem nuclei. •  These results are important for understanding the functional organisation of the inferior colliculus and its role in auditory processing.

The temporal representation of speech in a nonlinear model of the guinea pig cochlea

The temporal representation of speechlike stimuli in the auditory-nerve output of a guinea pig cochlea model is described. The model consists of a bank of dual resonance nonlinear filters that simulate the vibratory response of the basilar membrane followed by a model of the inner hair cell/auditory nerve complex. The model is evaluated by comparing its output with published physiological auditory nerve data in response to single and double vowels. The evaluation includes analyses of individual fibers, as well as ensemble responses over a wide range of best frequencies. In all cases the model response closely follows the patterns in the physiological data, particularly the tendency for the temporal firing pattern of each fiber to represent the frequency of a nearby formant of the speech sound. In the model this behavior is largely a consequence of filter shapes; nonlinear filtering has only a small contribution at low frequencies. The guinea pig cochlear model produces a useful simulation of the measured physiological response to simple speech sounds and is therefore suitable for use in more advanced applications including attempts to generalize these principles to the response of human auditory system, both normal and impaired.