Sharp Frequency Tuning Research Articles

How the owl resolves auditory coding ambiguity.

The barn owl (Tyto alba) uses interaural time difference (ITD) cues to localize sounds in the horizontal plane. Low-order binaural auditory neurons with sharp frequency tuning act as narrow-band coincidence detectors; such neurons respond equally well to sounds with a particular ITD and its phase equivalents and are said to be phase ambiguous. Higher-order neurons with broad frequency tuning are unambiguously selective for single ITDs in response to broad-band sounds and show little or no response to phase equivalents. Selectivity for single ITDs is thought to arise from the convergence of parallel, narrow-band frequency channels that originate in the cochlea. ITD tuning to variable bandwidth stimuli was measured in higher-order neurons of the owl's inferior colliculus to examine the rules that govern the relationship between frequency channel convergence and the resolution of phase ambiguity. Ambiguity decreased as stimulus bandwidth increased, reaching a minimum at 2-3 kHz. Two independent mechanisms appear to contribute to the elimination of ambiguity: one suppressive and one facilitative. The integration of information carried by parallel, distributed processing channels is a common theme of sensory processing that spans both modality and species boundaries. The principles underlying the resolution of phase ambiguity and frequency channel convergence in the owl may have implications for other sensory systems, such as electrolocation in electric fish and the computation of binocular disparity in the avian and mammalian visual systems.

Sharpening of Frequency Tuning by Inhibition in the Thalamic Auditory Nucleus of the Mustached Bat

Unlike the quasitriangular frequency-tuning curves of peripheral neurons, pencil- or spindle-shaped frequency-tuning curves (excitatory areas) have been found in the central auditory systems of many species of animals belonging to different classes. Inhibitory tuning curves (areas) are commonly found on both sides of such "level-tolerant" sharp frequency-tuning curves. However, it has not yet been examined whether sharpening of frequency tuning takes place in the medial geniculate body (MGB). We injected an inhibitory transmitter antagonist, bicuculline methiodide (BMI), into the MGB of the mustached bat to examine whether frequency tuning is sharpened by inhibition in the MGB and whether this sharpening, if any, occurs in addition to that performed in prethalamic auditory nuclei. Thirty-seven percent of thalamic Doppler-shifted constant frequency (DSCF) neurons mostly showing a level-tolerant frequency-tuning curve had an inhibitory area or areas. BMI changed the inhibitory areas of these neurons into excitatory areas, so that their excitatory frequency-tuning curves became broader. However, the BMI-broadened excitatory frequency-tuning curves were still much narrower than those of peripheral neurons. Our results indicate that level-tolerant frequency tuning of thalamic DSCF neurons is mostly created by prethalamic auditory nuclei and that it is further sharpened in 37% of thalamic DSCF neurons by lateral inhibition occurring in the MGB. The comparisons in sharpness (quality factors) of frequency-tuning curves between peripheral, thalamic, and cortical DSCF neurons indicate that the skirt portion of tuning curves is sharper in the above order, and that their tip portion is not significantly different between the peripheral and thalamic DSCF neurons, but significantly sharper in the cortical DSCF neurons than in the thalamic DSCF neurons. Therefore the central auditory system has inhibitory mechanisms for the progressive sharpening of frequency tuning. DSCF neurons in the primary auditory cortex were recently found to show facilitative responses to paired sounds. That is, they are combination sensitive. In the present studies, we found that thalamic DSCF neurons also showed facilitative responses to paired sounds. The responses of thalamic DSCF neurons to acoustic stimuli consisted of a slow and a fast component. BMI mainly increased the slow component and an excitatory transmitter antagonist, D-2-amino-5-phosphonovalerate mainly suppressed the slow component. Therefore the response pattern of these thalamic neurons is shaped by both gamma-aminobutyric acid-mediated inhibition and N-methyl-D-aspartate-mediated facilitation.

Tribute to Yasuji Katsuki's Major Findings: Sharpening of Frequency Tuning in the Central Auditory System

(1997). Tribute to Yasuji Katsuki's Major Findings: Sharpening of Frequency Tuning in the Central Auditory System. Acta Oto-Laryngologica: Vol. 117, No. sup532, pp. 9-12.

ELECTROPHYSIOLOGICAL MEASURES OF AUDITORY PROCESSING IN ODONTOCETES

ABSTRACT The preponderance of our knowledge concerning hearing in the Cetacea has come from psychophysical studies. The most widely used alternative to psychophysical studies are neurophysiological studies utilizing auditory evoked potentials (AEPs). Due in part to the hypertrophy of auditory structures exhibited by the Cetacea, AEPs are highly robust and rapidly and easily obtained. Moreover, because AEPs reflect the synchronized activity of large neuronal assemblies, they offer a high level window onto auditory processing and allow for across-species comparison of responses. Recent studies utilizing AEP techniques have demonstrated that the cetaceans have extremely high temporal resolution with integration times in the order of 300 msec. Remarkably, these animals also exhibit extremely sharp frequency tuning with auditory filters having Q10 of 20–30.

A functional map of the pigeon basilar papilla: correlation of the properties of single auditory nerve fibres and their peripheral origin

The purpose of the investigation was to correlate the functional properties of primary auditory fibres with the location of appertaining receptor cells in the avian basilar papilla. The functional properties of 425 single afferent fibres from the auditory nerve of adult pigeons were measured. The peripheral innervation site of 39 fibres was identified by intracellular labelling and correlated with the fibre's functional properties. Mean spontaneous firing rate (SR, 0.1–250/s) was distributed monomodally (mean: 91 ± 47/s) but not normally. Characteristics frequencies (CFs) were in the range of 0.02–4 kHz. SR, threshold at CF (4–76 dB SPL) and sharpness of tuning (Q 10 dB, 0.1–8.8) varied systematically with CF. For a given CF there was a strong correlation of threshold and Q 10 dB and of threshold and SR. Labelled fibres innervated different hair cell types over 93% of the length and 97% of the width of the basilar papilla. The majority of fibres innervated hair cells located between 30 and 70% distance from the apex and 0 and 30% distance from the neural edge of the papilla. CFs are mapped tonotopically from high at the base to low at the apex of the papilla, with a mean mapping constant of 0.63 ± 0.05 mm/octave (in vivo). The highest CF at the base extrapolates to 5.98 ± 1.17 kHz. The lowest CF mapped at the apex is 0.021 kHz. From the data, together with data from mechanical measurements (Gummer et al., 1987), a frequency-place function of the pigeon papilla was calculated. Tranverse gradients of threshold at CF and of Q 10 dB were observed across the width of the papilla. Thresholds were lowest and sharpness of tuning was highest above the neural limbus at a distance of 23% from the neural edge of the papilla. Hair cells in this sensitive strip are the tallest and narrowest ones across the width of the papilla. They are packed most densely and receive the largest number of afferent fibres. Fibres innervating (mostly short) hair cells on the free basilar membrane were spontaneously active and responsive to sound. Their Q 10 dB was less than average but their sensitivity and SR were comparable to the mean population values. It is concluded that functional properties change gradually not only along the length but also across the width of the pigeon basilar papilla. The results support the idea that sharp frequency tuning of avian primary auditory fibres involves tuning mechanisms supplementary to the tuning of the free part of the basilar membrane.

Frequency tuning and response latencies at three levels in the brainstem of the echolocating bat, Eptesicus fuscus.

To determine the level at which certain response characteristics originate, we compared monaural auditory responses of neurons in ventral cochlear nucleus, nuclei of lateral lemniscus and inferior colliculus. Characteristics examined were sharpness of frequency tuning, latency variability for individual neurons and range of latencies across neurons. Exceptionally broad tuning curves were found in the nuclei of the lateral lemniscus, while exceptionally narrow tuning curves were found in the inferior colliculus. Neither specialized tuning characteristic was found in the ventral cochlear nuclei. All neurons in the columnar division of the ventral nucleus of the lateral lemniscus maintained low variability of latency over a broad range of stimulus conditions. Some neurons in the cochlear nucleus (12%) and some in the inferior colliculus (15%) had low variability in latency but only at best frequency. Range of latencies across neurons was small in the ventral cochlear nucleus (1.3-5.7 ms), intermediate in the nuclei of the lateral lemniscus (1.7-19.8 ms) and greatest in the inferior colliculus (2.9-42.0 ms). We conclude that, in the nuclei of the lateral lemniscus and in the inferior colliculus, unique tuning and timing properties are built up from ascending inputs.

Evidence of sharp frequency tuning in the human auditory cortex

The frequency tuning of the human auditory cortex was studied by masking 100-ms tones of 1 and 2 kHz by continuous white-noise maskers with frequency notches around the tone frequencies. The subjects ignored the stimuli and concentrated on a reading task. The neuronal activity elicited by the test tones in the auditory cortex was measured with a 24-channel neuromagnetometer. The masker affected the amplitude and latency of the neuromagnetic N 100m response, peaking about at 100 ms after stimulus onset, in a systematic way: the wider the notch, the shorter was the latency and the larger the amplitude. The source location of N 100m in the auditory cortex did not depend on the notch width. Auditory filters at 1 and 2 kHz were modelled by a single-parameter rounded-exponential [Roex( p)] filter, based on the amplitude changes of N 100m. The filters revealed sharp tuning of the auditory cortex, resembling that obtained in psychoacoustical masking studies. The results demonstrate that frequency tuning of the neurons or neuron ensembles in the human auditory cortex can be studied completely noninvasively. Moreover, since the stimuli were ignored by the subjects, the filter shape is not affected by the criterion adopted by the subject in the discrimination task.

Otoacoustic emissions and cochlear function.

Otoacoustic emissions are sounds produced by the inner ear. In humans, and other mammal species, all normal ears produce otoacoustic emissions in response to sound stimuli. Within the inner ear, a mechanism called the cochlear amplifier utilizes metabolic energy to enhance the sound-induced vibration of the basilar membrane. The enhanced basilar-membrane vibration forms the basis of normal hearing sensitivity. The operation of the cochlear amplifier is impaired by a variety of traumas, resulting in reduced basilar-membrane vibration and, thus, hearing loss. Impaired operation of the cochlear amplifier is associated with reduced or abolished otoacoustic emissions. Otoacoustic emissions and the action of the cochlear amplifier are both characterized by sharp frequency tuning and a high degree of nonlinearity. Thus, otoacoustic-emission generation is intimately related to the normal function of the cochlea, and appears to reflect the action of the cochlear amplifier. Otoacoustic emissions are in widespread use for the assessment of cochlear function in basic-science studies, and in clinical applications. Nevertheless, the cochlear processes underlying the enhancement of basilarmembrane motion and the generation of otoacoustic emissions are not well understood.

Functional topography of cat primary auditory cortex: representation of tone intensity.

The neuronal response to tones as a function of intensity was topographically studied with multiple-unit recordings in the primary auditory cortex (AI) of barbiturate-anesthetized cats. The spatial distribution of the characteristics of rate/level functions was determined in each of three intensely studied cases and their relationship to the distribution of spectral parameters (sharpness of tuning and responses to broadband transients) in the same animals was determined. The growth of the high-intensity portion of rate/level functions was estimated by linear regression. Locations with monotonically growing high-intensity portions were spatially segregated from locations with nonmonotonic rate/level functions. Two noncontiguous areas with a high degree of nonmonotonicity were observed. One was located at the dorsoventral center of AI, and a second in the dorsal third of AI. The more ventral aggregate of high nonmonotonicity coincided with the region of sharp frequency tuning. The stimulus levels that produced the highest firing rate (strongest response level, SRL) at any sampled location ranged from 10 to 80 dB sound pressure level (SPL). Several spatial aggregates with either high or low SRLs were observed in AI. The region of sharpest tuning was always associated with a region of low SRLs. The response threshold to contralateral tones at the characteristic frequency (CF) ranged from -10 dB SPL to 85 dB SPL with the majority between 0 and 40 dB SPL. The spatial distribution of response thresholds indicated several segregated areas containing clusters with either higher or lower response thresholds. The correlation of response threshold with integrated bandwidth and transient responses was only weak. Low- and high-intensity tones of the same frequency are represented at different locations in AI as judged by the amount of evoked neuronal activity and are largely independent of the frequency organization. The spatial distribution of locations with high monotonicity and low strongest response levels were aligned with the organization of the integrated excitatory bandwidth and covaried with the response strength to broadband stimuli.

Sensitivity of neurons in cat primary auditory cortex to tones and frequency-modulated stimuli. II: Organization of response properties along the ‘isofrequency’ dimension

The spatial distribution of neuronal responses to tones and frequency-modulated (FM) stimuli was mapped along the ‘isofrequency’ dimension of the primary auditory cortex (AI) of barbiturate-anesthetized cats. In each cat, electrode penetrations roughly orthogonal to the cortical surface were closely spaced (average separation ≈ 130 μm) along the dorsoventral extent of a single ‘isofrequency’ strip in high frequency parts of AI (> 15 kHz). Characteristic frequency (CF), minimum threshold, sharpness of frequency tuning ( Q 10 and Q 20), the dynamic range of the spike count-intensity function at CF, sensitivity to the rate of change of frequency (RCF) and to the direction of frequency-modulation (DS) were determined for contralaterally-presented tone and FM stimuli. Sharpness of tuning attained maximum values at central loci along the dorsoventral ‘isofrequency’ axis and values declined towards more dorsal and more ventral locations. Minimum threshold and dynamic range varied between high and low values in a similar and correlated periodic fashion. Their combined organization yielded an orderly spatial representation of response strength, relative to maximum, as a function of stimulus amplitude. The distributions of the most common forms of FM rate sensitivity (RCF response categories) and best RCF along ‘isofrequency’ strips were significantly non-random although there was a considerable degree of variability between cats. FM directional preference and sensitivity appeared to be randomly distributed. Sharpness of tuning may be related to the analysis of the spectral content of an acoustic stimulus, both minimum threshold and dynamic range are related to the encoding of stimulus intensity, and measures of FM rate and directional sensitivity assess the coding of temporal changes of stimulus spectra. The independent, or for minimum threshold and dynamic range dependent, topographic organizations of these neuronal parameters therefore suggest parallel and independent processing of these aspects of acoustic signals in AI.

Responses to sound of the basilar membrane of the mammalian cochlea

Recent evidence shows that the frequency-specific non-linear properties of auditory nerve and inner hair cell responses to sound, including their sharp frequency tuning, are fully established in the vibration of the basilar membrane. In turn, the sensitivity, frequency selectivity and non-linear properties of basilar membrane responses probably result from an influence of the outer hair cells.

Auditory responses in the nucleus basalis of the pigeon

Single-unit responses and field potentials evoked by sound stimuli were recorded from the nucleus basalis in the frontal lobe of the pigeon brain. Auditory units in this nucleus showed phasic responses to tonal stimuli and sharp frequency tuning. The latency of responses was 5.8±0.6 ms. The response properties of these units were similar to those of units in the nucleus mesencephalicus lateralis, pars dorsalis (a mesencephalic auditory nucleus), where fibers from the auditory nuclei in the medulla terminate. This suggests that the nucleus basalis receives projections from medullary auditory neurons. Averaged auditory field potentials in the frontal lobe had three prominent components. Regional changes in the polarity of each component suggest that auditory neurons in the medulla project directly to the nucleus basalis, which in turn projects to the frontal neostriatum.

Silent periodic cells in the cat striate cortex

A class of neurons called silent periodic cells, having properties intermediate between those in the simple and complex families, has been discriminated in the cat striate cortex. Silent periodic cells have relatively small receptive fields, a low spontaneous activity (i.e. relatively silent) and a preference for relatively slow stimulus velocities (< 3° /sec). In addition they give a mixed on/off response to a stationary flashing bar over virtually the whole of the receptive field with usually somewhat stronger on responses in some locations and stronger off responses in others (partial phase sensitivity). The most characteristic properties of these cells are, however, found in their responses to gratings, namely the nonlinearity manifested by the absence of a null point to a stationary flashing grating, a spatial periodicity revealed by a clearly modulated discharge to drifting gratings of medium and high spatial frequencies and, finally, a very sharp spatial frequency tuning curve with a half-sensitivity bandwidth between 0.5 and 0.95 octave, i.e. narrower than that of simple cells whose bandwidths are usually above 1 octave. Silent periodic cells resemble B-cells that have been described in other studies.