Ian M. Winter

The psychophysics and physiology of comodulation masking release

The ability to detect auditory signals from background noise may be enhanced by the addition of energy in frequency regions well removed from the frequency of the signal. However, it is important that this energy is amplitude-modulated in a coherent way across frequencies, i.e. comodulated. This enhancement of signal detectability is known as comodulation masking release (CMR), and in this review we show that CMR is largest if: (1) the total maskers bandwidth is large, (2) the modulation frequency is low, (3) the modulation depth is high, (4) the envelope is regular and, (5) the maskers spectrum level is high. Possible physiological correlates of CMR have been found at different levels of the auditory pathway. Current hypotheses for the underlying physiological mechanisms, including wide-band inhibition or the disruption of masker modulation envelope response, are discussed.

Intensity coding in low-frequency auditory-nerve fibers of the guinea pig.

Rate-level functions from 130 auditory-nerve fibers with characteristic frequencies below 3.5 kHz have been recorded. The relationship between rate-level function type and other properties of auditory-nerve fibers was similar to that previously reported for a high-frequency population in the same species [characteristic frequencies greater than 8 kHz-Winter et al., Hear. Res. 45, 191-202 (1990)]. To estimate whether there is sufficient information in the changes in discharge rate from auditory-nerve fibers to account for the intensity discrimination performance observed in humans (for 1-kHz tone bursts), the Sachs-Abbas model was modified to produce the variation in rate-level functions found in guinea pig auditory-nerve fibers. The ability of modeled, single auditory-nerve fibers and populations of these fibers to signal differences in intensity has been calculated. Optimal combination of information from those fibers assumed to synapse beneath just one inner hair cell resulted in a discrimination performance that exceeded human psychophysical performance up to sound levels of 113 dB SL. It is concluded from these results that there is more than sufficient information present in the changes in discharge rate of a localized population of guinea pig auditory-nerve fibers to account for the intensity discrimination performance of humans as measured psychophysically.

Reverberation challenges the temporal representation of the pitch of complex sounds.

Accurate neural coding of the pitch of complex sounds is an essential part of auditory scene analysis; differences in pitch help segregate concurrent sounds, while similarities in pitch can help group sounds from a common source. In quiet, nonreverberant backgrounds, pitch can be derived from timing information in broadband high-frequency auditory channels and/or from frequency and timing information carried in narrowband low-frequency auditory channels. Recording from single neurons in the cochlear nucleus of anesthetized guinea pigs, we show that the neural representation of pitch based on timing information is severely degraded in the presence of reverberation. This degradation increases with both increasing reverberation strength and channel bandwidth. In a parallel human psychophysical pitch-discrimination task, reverberation impaired the ability to distinguish a high-pass harmonic sound from noise. Together, these findings explain the origin of perceptual difficulties experienced by both normal-hearing and hearing-impaired listeners in reverberant spaces.

The temporal representation of the delay of iterated rippled noise in the ventral cochlear nucleus of the guinea-pig

1 We have examined the temporal discharge patterns of single units from the ventral cochlear nucleus (VCN) of anaesthetized guinea‐pigs in response to iterated rippled noise (IRN). The pitch range evoked by the stimuli was from 32 to 1000 Hz. 2 Single units were classified into four groups using existing classification schemes: primary‐like (PL), onset (O), sustained chopper (CS) and transient chopper (CT). For all unit types the delay of the IRN stimuli was well represented in the all‐order interspike interval histograms (ISIHs). 3 A subset of the onset units (onset‐chopper, OC) showed a clear preference for some delays of the IRN in their first‐order interval statistics. We describe this delay preference as ‘periodicity tuning’. The delay at which the pitch estimate was at its maximum was designated its best periodicity. The range of best periodicities for OC units was 3.75‐13 ms (between 77 and 267 Hz). 4 The other unit types also showed enhancement of the first‐order interval statistics at the delay of the IRN. The range of best periodicities was 1.4‐8.8 ms (113‐714 Hz) for the CT group, 2.25‐10.8 ms (93‐444 Hz) for the CS group and 0.5‐4.6 ms (217‐2000 Hz) for the PL group. 5 The correlation between the maximum interval enhancement observed in response to the IRN stimuli and the peak in the first‐order ISIH in response to white noise was 0.81 for OC units, 0.72 for CS units, 0.44 for CT units and ‐0.15 for PL units. 6 These results demonstrate that all unit types in the VCN can enhance the representation of the delay of IRN using first‐order interspike intervals (ISIs) over a range of periodicities. CS and OC units show the greatest range of best periodicities and they are well‐suited to encode the delay of IRN in their first‐order ISIs for a wide range of pitches.

Responses of Dorsal Cochlear Nucleus Neurons to Signals in the Presence of Modulated Maskers

The detection of a signal in noise is enhanced when the masking noise is coherently modulated over a wide range of frequencies. This phenomenon, known as comodulation masking release (CMR), has been attributed to across-channel processing; however, the relative contribution of different stages in the auditory system to such across-channel processing is unknown. It has been hypothesized that wideband or lateral inhibition may underlie a physiological correlate of CMR. To further test this hypothesis, we have measured the responses of single units from the dorsal cochlear nucleus in which wideband inhibition is particularly pronounced. Using a sinusoidally amplitude-modulated tone at the best frequency of each unit as a masker, a pure-tone signal was added in the dips of the masker modulation. Flanking bands (FBs, also amplitude-modulated pure tones) were positioned to fall within the inhibitory sidebands of the receptive field of the unit. The FBs were either in phase (comodulated) or out of phase (codeviant) with the on-frequency masker. For the majority of units, the addition of the comodulated FBs produced a strong reduction in the response to the masker modulation, making the signal more salient in the post stimulus time histograms. The change in spike rate in response to the signal between the masker and signal-plus-masker conditions was greatest for the comodulated condition for 29 of 45 units. These results are consistent with the hypothesis that wideband inhibition may play a role in across-channel processing at an early stage in the auditory pathway.

Contralateral inhibitory and excitatory frequency response maps in the mammalian cochlear nucleus

There is increasing evidence that the responses of single units in the mammalian cochlear nucleus can be altered by the presentation of contralateral stimuli, although the functional significance of this binaural responsiveness is unknown. To further our understanding of this phenomenon we recorded single‐unit (n = 110) response maps from the cochlear nucleus (ventral and dorsal divisions) of the anaesthetized guinea pig in response to presentation of ipsilateral and contralateral pure tones. Many neurones showed no evidence of input from the contralateral ear (n = 41) but other neurones from both ventral and dorsal cochlear nucleus showed clear evidence of contralateral inhibitory input (n = 61). Inhibitory response patterns were divided into two groups. In 36 neurones, contralateral tone‐evoked inhibition was closely aligned with the ipsilateral excitatory response map (± 0.33 octaves) often extending to low stimulus levels. In 25 neurones, higher threshold contralateral inhibitory responses were found, mostly centred at frequencies greater than 0.33 octaves below the ipsilateral excitation. A few neurones (n = 8) exhibited responses consistent with excitatory input from the contralateral ear, which was closely aligned with the ipsilateral excitation, and were found exclusively in the dorsal cochlear nucleus. The latency of the contralateral interaction was, on average, longer than the ipsilateral latency. Interaural level difference curves are similar to other reports from the cochlear nucleus. Our results are consistent with the idea that contralateral interactions arise from a variety of direct and indirect neuronal projections.

The time course of recovery from suppression and facilitation from single units in the mammalian cochlear nucleus.

The responses to two identical, consecutive pure tone stimuli with varying inter-stimulus intervals (delta ts) were measured for 89 neurons in the cochlear nucleus of the anaesthetised guinea pig. We observed two main effects; either a decrease (suppression) or an increase (facilitation) in response to the second tone followed by an exponential recovery. Response behaviour correlated with the unit type; primary-like, primary-like with notch and transient-chopper units showed a recovery from suppression that was very similar to that already reported in the auditory nerve. For chopper units the strength of the adaptation was correlated with the units regularity of spike discharge; sustained chopper (CS) units showed less suppression than transient choppers. Onset units showed complete suppression at short delta ts. Pause/Build (PB) units responded with increased activity to the second tone. In contrast to previous studies in the cochlear nucleus the recovery from suppression or facilitation was well described by a single exponential function, enabling us to define a recovery time constant and a maximum suppression/facilitation. There appeared to be a hierarchy in the time constant of recovery with PB and CS units showing the longest recovery times and onset units showing the shortest.

The responses of single units in the ventral cochlear nucleus of the guinea pig to damped and ramped sinusoids

Human listeners hear an asymmetry in the perception of damped and ramped sinusoids; the partial loudness of the envelope component is greater than the partial loudness of the carrier component for damped sinusoids. Here we show that an asymmetry also occurs in the physiological responses of most units in the ventral cochlear nucleus to these same sounds. The activity elicited by damped sinusoids is mainly restricted to the beginning of each envelope period, which is not the case for ramped sinusoids. This can be quantified by computing the ratio of the tallest bin of the modulation period histogram to the total number of spikes (the peak-to-total ratio, p/t). Damped sinusoids produce a higher p/t than ramped sinusoids, which demonstrates physiological temporal asymmetry. It is also the case that ramped sinusoids typically elicit more spikes than damped sinusoids. The physiological asymmetry occurs where the perceptual asymmetry is present. It is maximal at modulation half-lives of 4 and 16 ms, greatly reduced at 1 ms and absent at 64 ms. Different unit types exhibit differing degrees of temporal asymmetry. Onset units produce the greatest p/t asymmetry, primary-like units produce the least asymmetry and chopper units are in-between. With regard to total spike count, the maximal asymmetry occurs with chopper units. If primary-like units are assumed to reflect the activity in primary auditory nerve fibres, then there is enhancement of temporal asymmetry in the ventral cochlear nucleus by both onset and chopper units.

Temporal coding of the pitch of complex sounds by presumed multipolar cells in the ventral cochlear nucleus

Extensive studies of the encoding of fundamental frequency (f0) in the auditory nerve indicate that f0 can be represented by either the timing of the neuronal discharges or the mean discharge rate as a function of characteristic frequency. It is therefore of considerable interest to examine what happens to this information at the next level of the auditory pathway, the cochlear nucleus. Both physiologically and anatomically the cochlear nucleus is considerably more heterogenous than the auditory nerve. There are two main cell types in the ventral division of the cochlear nucleus: bushy and multipolar. Bushy cells give rise to primary-like responses whereas multipolar cells may be characterised by either onset or chopper type responses. Physiological studies have suggested that onset and chopper units may be good at representing the f0 of complex sounds in their temporal discharge properties. However, in these studies the pitch-producing sounds were usually characterised by highly modulated envelopes and it was not possible to tell if the units were simply responding to the modulation or the temporal fine structure. In this paper we examine the ability of onset and chopper units to encode the f0 of complex sounds when the modulation cue has been greatly reduced. These stimuli were steady-state vowels in the presence of background noise, and iterated rippled noise (IRN). The response of onset units to the vowel f0 in the presence of background noise was varied but many still maintained a strong response. In contrast, the majority of chopper units showed a greater reduction in their response to vowel f0 in the presence of background noise. In keeping with the vowel study, the responses of both types of unit to the delay of the IRN was reduced in comparison with their response to more highly modulated stimuli. Increasing anatomical, pharmacological and physiological evidence would seem to argue against onset units playing a direct role in pitch perception. However, some units, identified as sustained choppers, may be able to represent the pitch of complex sounds in their temporal discharges.

Dual action of olivocochlear collaterals in the guinea pig cochlear nucleus.

Axons of olivocochlear neurones in the superior olivary complex terminate on hair cells of the cochlea, reducing the sensitivity to sound. These axons also have collateral branches to neurones in the cochlear nucleus, the first processing centre in the brainstem. Anatomical data show that these collaterals terminate mainly in the granule cell area but their precise neuronal targets and the effects they might have are unknown. We have studied the effects of these collaterals in guinea pigs, by electrically stimulating the olivocochlear axons at the floor of the IVth ventricle while recording single neurone responses in the cochlear nucleus. We eliminated the peripheral effects of olivocochlear stimulation either by destruction of the target receptor cells using chronic administration of kanamycin, or by acute perfusion of the cochlea with strychnine, a specific blocker of the postsynaptic receptors. Electrical stimulation of the olivocochlear axons in normal animals caused a variety of effects on cochlear nucleus neurones. In some neurones, there was suppression of spontaneous firing and a reduction in sensitivity to sound, while in others there was an excitatory effect of olivocochlear axon stimulation. When the peripheral olivocochlear action was eliminated, we still found both inhibition and excitation in the cochlear nucleus. These results show that the effects of olivocochlear stimulation on cochlear nucleus responses are not a simple passive reflection of peripheral changes but are a result of complex interactions between peripheral suppression of afferent input and collateral-mediated excitation and possibly also inhibition.