Directionality of auditory nerve fiber responses to pure tone stimuli in the grassfrog, Rana temporaria. II. Spike timing

We studied the directionality of spike timing in the responses of single auditory nerve fibers of the grass frog, Rana temporaria, to tone burst stimulation. Both the latency of the first spike after stimulus onset and the preferred firing phase during the stimulus were studied. In addition, the directionality of the phase of eardrum vibrations was measured. The response latency showed systematic and statistically significant changes with sound direction at both low and high frequencies. The latency changes were correlated with response strength (spike rate) changes and were probably the result of directional changes in effective stimulus intensity. Systematic changes in the preferred firing phase were seen in all fibers that showed phaselocking (i.e., at frequencies below 500–700 Hz). The mean phase lead for stimulation from the contralateral side was approximately 140° at 200 Hz and decreased to approximately 100° at 700 Hz. These phaseshifts correspond to differences in spike timing of approximately 2 ms and 0.4 ms respectively. The phaseshifts were nearly independent of stimulus intensity. The phase directionality of eardrum vibrations was smaller than that of the nerve fibers. Hence, the strong directional phaseshifts shown by the nerve fibers probably reflect the directional characteristics of extratympanic pathways. Accepted: 23 November 1996     

Selectivity of the peripheral auditory system of spadefoot toads (Scaphiopus couchi) for sounds of biological significance

Summary Scaphiopus couchi is a primitive anuran whose vocal repertoire consists of a mating call and a release call. The two calls are distinct and differ in trill rate. Reception of airborne sound is achieved by means of a poorly differentiated region of skin on the head which serves as an eardrum.Whereas more modern anurans possessthree distinct types of auditory nerve fibers, spadefoot toads possess onlytwo types: a low-frequency-sensitive group which exhibits tone-on-tone inhibition and a high-frequency-sensitive group which is not inhibitable. The sharpness of frequency tuning of primary fibers in each group is comparable to more advanced vertebrate species. While the response properties of auditory fibers in the high-frequency-sensitive group are well matched to the spectral and temporal features in the spadefoot's mating call and release call, the low-frequency-sensitive fibers do not respond to these calls. Instead they may be involved in detection of bodily transmitted sounds during clasping, as well as other low-frequency sounds in the environment. The two groups of auditory fibers probably derive from separate auditory organs within the inner ear. Thresholds of auditory nerve fibers in spadefoot toads are relatively poorer than in more advanced anurans, which likely is due to their less developed eardrum. The role of tone-on-tone inhibition in the peripheral auditory system is questioned with regard to its significance in processing sounds of biological value.We wish to dedicate this paper to Jasper J. Loftus-Hills who was killed in a tragic accident near Austin, Texas on June 11, 1974. His post-doctoral appointment in our laboratory and his assistance in collecting spadefoot toads in the field recall fond memories.We also wish to thank R. Sage for helping us collect animals and W. F. Blair for supplying tape recordings ofScaphiopus mating calls. The assistance of J. Paton in photographing the animal in Fig. 1 is gratefully appreciated. This research was supported by the U.S. Public Health Service (NIH Research Grant NS-09244) and the National Science Foundation (Grant GB-18836); travel expenses involved in collecting animals were supported by a Cornell University Research Grant.     

Directionality of phase locking in auditory nerve fibers of the leopard frog Rana pipiens pipiens

Summary A dorsal approach to the eighth nerve and free-field stimulation were used to investigate the effect of sound direction and intensity on phase locking in auditory nerve fibers of the leopard frog Rana pipiens pipiens.Tuning curves of 75 auditory neurons were analyzed (Fig. 2). Amphibian papillar neurons, but not basilar papillar neurons, exhibit significant phase locking to short tone bursts at the characteristic frequency (CF), the degree of phase locking (vector strength) decreasing with the neuron's CF (Figs. 3, 4 and 10E). Vector strength increases with sound pressure level to saturate about 20 dB above threshold, while the preferred firing phase is only slightly affected (Figs. 5 and 6).In contrast, sound direction hardly affects vector strength (Figs. 7, 8, 9A and 10A and C), but has a strong influence on the preferred firing phase (Figs. 7, 8, 9B and C, 10B and D): With respect to anterior tone presentation there are phase lags for ipsilateral and phase leads for posterior and contralateral presentation. Phase differences between both ears show a sinusoidal or cardioid/ovoidal directional characteristic; maximum differences are found with antero-lateral tone presentation (Fig. 11). The directionality of phase locking decreases with the neuron's CF (Fig. 10F) and only slightly changes with sound pressure level (Fig. 12). Thus, phase locking of amphibian papilla neurons can potentially provide intensity-independent information for sound localization.Abbreviations SPL sound pressure level - FTC frequency threshold curve - CF characteristic frequency - TF test frequency - VS vector strength - AP amphibian papilla - BP basilar papilla     

Manifestations of dynamic coding of the amplitude-modulated sounds on the level of auditory nerve fibres

Average firing rate of the auditory nerve fiber as function of the level of the tone with the frequency equal to characteristic frequency of the fibers, can be defined as an input-output characteristic. It is known that the steepening of the input-output characteristic of the real auditory nerve fiber is more, and the width is less than the spontaneous activity of the fiber. The latter characterizes fiber's ability to generate spikes, if the stimulus is absent. However it is known, that the real auditory nerve fibers with low spontaneous activity reproduce amplitude modulation of the signals much better, than the fibers with high spontaneous activity. From the results of simulation experiments, it follows that the dynamic properties of the auditory nerve fibers, providing fine tuning or adaptation of a fiber threshold under the stimulus level but not the static input-output characteristics, are the reason of fibers reproduction of stimuli amplitude modulations. However the auditory nerve fibers with high spontaneous activity due to abrupt input-output characteristic are capable to reproduce modulations of sounds whose levels are lower than a threshold of the fiber, if a weak signal adds to a weak broadband noise. This is a phenomenon of stochastic resonance found in the reactions of auditory nerve fibers.     

Fast negative feedback enables mammalian auditory nerve fibers to encode a wide dynamic range of sound intensities

Mammalian auditory nerve fibers (ANF) are remarkable for being able to encode a 40 dB, or hundred fold, range of sound pressure levels into their firing rate. Most of the fibers are very sensitive and raise their quiescent spike rate by a small amount for a faint sound at auditory threshold. Then as the sound intensity is increased, they slowly increase their spike rate, with some fibers going up as high as ～300 Hz. In this way mammals are able to combine sensitivity and wide dynamic range. They are also able to discern sounds embedded within background noise. ANF receive efferent feedback, which suggests that the fibers are readjusted according to the background noise in order to maximize the information content of their auditory spike trains. Inner hair cells activate currents in the unmyelinated distal dendrites of ANF where sound intensity is rate-coded into action potentials. We model this spike generator compartment as an attenuator that employs fast negative feedback. Input current induces rapid and proportional leak currents. This way ANF are able to have a linear frequency to input current (f-I) curve that has a wide dynamic range. The ANF spike generator remains very sensitive to threshold currents, but efferent feedback is able to lower its gain in response to noise.     

Lateral line nerve fibers do not code bulk water flow direction in turbulent flow

The discharges of anterior and posterior lateral line nerve afferents were recorded while stimulating goldfish, Carassius auratus, with bulk water flow. With increasing flow velocity lateral line afferents increased their discharge rates. However, an increased response to flow rates occurred even if flow direction was reversed. Thus, individual lateral line afferents did not encode the direction of running water. Frequency spectra of the water motions quantified with particle image velocimetry revealed flow fluctuations that increased with increasing flow velocity. Maximal spectral amplitudes of the flow fluctuations were below 5 Hz (bulk flow velocity 4–15 cm s⁻¹). The frequency spectra of the firing rates of lateral line afferents also showed an increase in amplitude when fish were exposed to running water. The maximal spectral amplitudes of the recorded data were in the frequency range 3–8 Hz. This suggests that the lateral line afferents mainly responded to the higher frequency fluctuations that developed under flow conditions, but not to the direct current flow or the lower frequency fluctuations. Although individual lateral line afferents encoded neither flow velocity nor flow direction we suggest that higher order lateral line neurons can do so by monitoring flow fluctuations as they move across the surface of the fish.     

Adaptations to the acoustic environment by the squirrelfishes Myripristis violaceus and M. Pralinius

Three sounds naturally produced by squirrelfish of the genus Myripristis were recorded and analyzed sonographically. Captive Myripristis violaceus responded acoustically and behaviorally to playbacks of calls by conspecifics. Acoustic characteristics (velocity and pressure levels, and their attenuation as a function of frequency and distance) of grunt sounds, produced by hand held fish, were determined for M. violaceus and M. pralinius. Background noise components were analyzed for four different environments of these fish. Background noise and grunt sounds had high velocity levels, relative to pressure levels, expected in acoustic near fields, but attenuated at rates characteristic of acoustic far fields. Electrophysiological recordings from the lateral line organs of M. violaceus indicated that the lateral line system is directionally sensitive to a vector component (e.g., displacement or velocity) of the sound field, and is capable of mediating the observed behavioral responses.     

Directional hearing in the gray tree frog Hyla versicolor: Eardrum vibrations and phonotaxis

1. We used laser vibrometry to study the vibrational frequency response of the eardrum of female gray tree frogs for different positions of the sound source in three-dimensional space. Furthermore, we studied the accuracy of 3-D phonotaxis in the same species for sounds with different frequency contents. 2. The directionality of the eardrum was most pronounced in a narrow frequency range between 1.3 and 1.8 kHz. 3. The average 3-D, horizontal and vertical jump error angles for phonotactic approaches with a sound similar to the natural advertisement call (1.1 and 2.2 kHz frequency components) were 23 degrees, 19 degrees and 12 degrees, respectively. 4. 3-D jump error angle distributions for the 1.4 + 2.2 kHz, 1.0 kHz and 2.0 kHz sounds were not significantly different from that for the 1.1 + 2.2 kHz sound. 5. The average 3-D jump error angle for the 1.4 kHz sound was 36 degrees, and the distribution was significantly different from that for the 1.1 + 2.2 kHz sound. Hence, phonotactic accuracy was poorer in the frequency range of maximum eardrum directionality. 6. Head scanning was not observed and is apparently unnecessary for accurate sound localization in three-dimensional space. 7. Changes in overall sound pressure level experienced by the frog during phonotactic approaches are not an important cue for sound localization.     

Explanation of octave and diplacusis effects

The study is based on the model of sound perception that involves two systems of measuring the frequency of the sound being perceived. The system of analyzing the periodicity of spike sequence in axons of neurons innervating the internal auditory hair cells excited by the running wave is less precise, but it provides the estimation of the frequency of any periodical sounds. Exact measurement of the frequency of the sinusoidal sound occurs from the spikes in axons of neurones innervating the internal hair cells of the auditory reception field, which uses the entire train of waves excited by this sound in the critical layer of the waveguide of the internal ear cochlea, which corresponds to the frequency of the sound. The octave effect is explained in terms of the fact that the spectrum of frequencies of speech sounds, singing and music coincides with the region of the audibility range in which the impulses of the auditory nerve fibers are synchronized by incoming signals. The octave similarity, i.e., the similarity in the sounding of harmonic signals, whose frequencies relate as even numbers (2:1, etc.), is explained by an unambiguous match between the sound frequency and pulse rate in auditory fibers coming from the auditory reception field. The presence in the brain posterior tubercles of multipeak neurons whose peaks are in octave ratio, confirm the crucial role of the system of exact measurement of frequency in the phenomenon of octave similarity. The phenomenon of diplacusis, which is particularly pronounced in persons with Menier disease, is caused by changes in the position of the auditory reception field in the diseased ear as compared with the healthy ear. The alternating switching of reception from one ear to the other is related to a disturbance of the unitary image of pitch.     

Functional correlates of characteristic frequency in single cochlear nerve fibers of the Mongolian gerbil

Summary Single-unit recordings obtained from the auditory nerve of the Mongolian gerbil, Meriones unguiculatus, revealed functional differences in the response properties of neurons tuned to low and high frequencies. The distribution of neural thresholds displayed a distinct rise for auditory nerve fibers with characteristic frequencies] (CFs) between 3–5 kHz. This frequency band also marked abrupt changes in both the distribution of spontaneous discharge rates and the shape of the neural tuning curve. For neurons of all CFs, spontaneous firing rates were inversely related to neural threshold but unrelated to sharpness of neural tuning. The range of CF thresholds encountered, even when data from many animals were combined, rarely exceeded 20 dB, suggesting that cochlear nerve responses obtained from this species display little inter-animal variability. These results are compared with similar data from other species and discussed in terms of recent studies on sound communication and cochlear anatomy in gerbils.Abbreviations CF characteristic frequency - SR spontaneous discharge rate     

Encoding of Temporal Information by Timing,Rate, and Place in Cat Auditory Cortex

A central goal in auditory neuroscience is to understand the neural coding of species-specific communication and human speech sounds. Low-rate repetitive sounds are elemental features of communication sounds, and core auditory cortical regions have been implicated in processing these information-bearing elements. Repetitive sounds could be encoded by at least three neural response properties: 1) the event-locked spike-timing precision, 2) the mean firing rate, and 3) the interspike interval (ISI). To determine how well these response aspects capture information about the repetition rate stimulus, we measured local group responses of cortical neurons in cat anterior auditory field (AAF) to click trains and calculated their mutual information based on these different codes. ISIs of the multiunit responses carried substantially higher information about low repetition rates than either spike-timing precision or firing rate. Combining firing rate and ISI codes was synergistic and captured modestly more repetition information. Spatial distribution analyses showed distinct local clustering properties for each encoding scheme for repetition information indicative of a place code. Diversity in local processing emphasis and distribution of different repetition rate codes across AAF may give rise to concurrent feed-forward processing streams that contribute differently to higher-order sound analysis.     

Conditional Probability Analyses of the Spike Activity of Single Neurons

With the objective of separating stimulus-related effects from refractory effects in neuronal spike data, various conditional probability analyses have been developed. These analyses are introduced and illustrated with examples based on electrophysiological data from auditory nerve fibers. The conditional probability analyses considered here involve the estimation of the conditional probability of a firing in a specified time interval (defined relative to the time of the stimulus presentation), given that the last firing occurred during an earlier specified time interval. This calculation enables study of the stimulus-related effects in the spike data with the time-since-the-last-firing as a controlled variable. These calculations indicate that auditory nerve fibers “recover” from the refractory effects that follow a firing in the following sense: after a “recovery time” of approximately 20 msec, the firing probabilities no longer depend on the time-since-the-last-firing. Probabilities conditional on this minimum time since the last firing are called “recovered probabilities.” The recovered probabilities presented in this paper are contrasted with the corresponding poststimulus time histograms, and the differences are related to the refractory properties of the nerve fibers.     

Constructing Noise-Invariant Representations of Sound in the Auditory Pathway

Identifying behaviorally relevant sounds in the presence of background noise is one of the most important and poorly understood challenges faced by the auditory system. An elegant solution to this problem would be for the auditory system to represent sounds in a noise-invariant fashion. Since a major effect of background noise is to alter the statistics of the sounds reaching the ear, noise-invariant representations could be promoted by neurons adapting to stimulus statistics. Here we investigated the extent of neuronal adaptation to the mean and contrast of auditory stimulation as one ascends the auditory pathway. We measured these forms of adaptation by presenting complex synthetic and natural sounds, recording neuronal responses in the inferior colliculus and primary fields of the auditory cortex of anaesthetized ferrets, and comparing these responses with a sophisticated model of the auditory nerve. We find that the strength of both forms of adaptation increases as one ascends the auditory pathway. To investigate whether this adaptation to stimulus statistics contributes to the construction of noise-invariant sound representations, we also presented complex, natural sounds embedded in stationary noise, and used a decoding approach to assess the noise tolerance of the neuronal population code. We find that the code for complex sounds in the periphery is affected more by the addition of noise than the cortical code. We also find that noise tolerance is correlated with adaptation to stimulus statistics, so that populations that show the strongest adaptation to stimulus statistics are also the most noise-tolerant. This suggests that the increase in adaptation to sound statistics from auditory nerve to midbrain to cortex is an important stage in the construction of noise-invariant sound representations in the higher auditory brain.     

Responses of the goldfish head lateral line to moving objects

We investigated how fibers in the anterior lateral line nerve of goldfish, Carassius auratus, respond to water motions generated by an object that was moved alongside the fish. Motion direction was from anterior to posterior or opposite, object diameter was between 0.1 and 4 cm and the distance between object and fish varied between 1 and 6 cm. Fibers exhibited monophasic responses characterized by a transient increase in discharge rate, biphasic responses consisting of an increase followed by a decrease in discharge rate or vice versa, or triphasic responses characterized by a rate increase followed by a decrease and again an increase or by the inverse pattern. In two-thirds of the fibers response patterns depended on object motion direction. Of these, about 60% responded to a reversal of motion direction with an inversion of the response pattern. Our results differ from previous data obtained from posterior lateral line nerve fibers in the relative proportions of the observed response patterns, and by a much smaller proportion of fibers that exhibited a direction-dependent response. These differences can be explained by the fact that the spatial orientations of the neuromasts on the head are more heterogenuous than on the trunk.     

Multiple-band trigger features of midbrain auditory neurons revealed in composite spectro-temporal receptive fields

Receptive fields of single units in the auditory midbrain of anesthetized rats were studied using random FM-tone stimuli of narrow frequency-ranges. Peri-spike averaging of the modulating waveform first produced a spectro-temporal receptive field (STRF). Combining STRFs obtained from the same unit at different frequency regions generated a composite receptive field covering a wider frequency range of 2 to 3 octaves. About 20% of the composite STRFs (26/122) showed a pattern of multiple-bands which were not clear in the non-composite maps. Multiple-bands in a given composite map were often oriented in the same direction (representing upward or downward FM ramp) separated at rather regular frequency intervals. They reflect multiple FM trigger features in the stimulus rather than repetitive firing to a single trigger feature. Results showed that the subcortical auditory pathways are capable of detecting multiple FM features and such sensitivity could be useful in detecting multiple-harmonic FM bands present in the vocalization sounds.     

Activation of Auditory Cortex by Anticipating and Hearing Emotional Sounds: An MEG Study

To study how auditory cortical processing is affected by anticipating and hearing of long emotional sounds, we recorded auditory evoked magnetic fields with a whole-scalp MEG device from 15 healthy adults who were listening to emotional or neutral sounds. Pleasant, unpleasant, or neutral sounds, each lasting for 6 s, were played in a random order, preceded by 100-ms cue tones (0.5, 1, or 2 kHz) 2 s before the onset of the sound. The cue tones, indicating the valence of the upcoming emotional sounds, evoked typical transient N100m responses in the auditory cortex. During the rest of the anticipation period (until the beginning of the emotional sound), auditory cortices of both hemispheres generated slow shifts of the same polarity as N100m. During anticipation, the relative strengths of the auditory-cortex signals depended on the upcoming sound: towards the end of the anticipation period the activity became stronger when the subject was anticipating emotional rather than neutral sounds. During the actual emotional and neutral sounds, sustained fields were predominant in the left hemisphere for all sounds. The measured DC MEG signals during both anticipation and hearing of emotional sounds implied that following the cue that indicates the valence of the upcoming sound, the auditory-cortex activity is modulated by the upcoming sound category during the anticipation period.     

Auditory nerve and interneurone responses to natural sounds in several species of cicadas

ABSTRACT. The calling and courtship songs of 17-year cicadas and of Say's cicadas differ both in the sound frequency spectrum and in temporal pattern. Multiunit recordings with hook electrodes from the whole auditory nerve show that the hearing organs are especially sensitive to transient stimuli occurring in natural sounds. Artificially produced clicks elicit bursts of spikes synchronized among various primary sensory fibres. These fibres respond to natural calling and courtship songs with a specificity dependent on carrier frequency, rhythm and transient content of the sound, following sound pulses (i.e. tymbal actions) up to repetition rates of 200 Hz. An ascending, plurisegmental interneurone was characterized by intracellular recording and simultaneously stained with cobalt. Its main arborization spatially overlaps the anterior part of the sensory auditory neuropile, and the axon was traced as far as the prothoracic ganglion. Direct input from primary auditory fibres was suggested by latency measurements. Intracellular recordings from such neurons in different species show distinct auditory input, with phasic-tonic spike responses to tones. In general, the interneurone response is more species-specific to calling than to courtship songs, and the preferential response to the conspecific calling song is based primarily upon sound frequency content.     

Studies of directional sensitivity of neurons in the cat primary auditory cortex

A set of impulsive transient signals has been synthesized for earphone delivery whose waveform and amplitude spectra, measured at the eardrum, mimic those of sounds arriving from a free-field source. The complete stimulus set forms a "virtual acoustic space" (VAS) for the cat. VAS stimuli are delivered via calibrated earphones sealed into the external meatus in cats under barbiturate anesthesia. Neurons recorded extracellularly in primary (AI) auditory cortex exhibit sensitivity to the direction of sound in VAS. The aggregation of effective sound directions forms a virtual space receptive field (VSRF). At about 20 dB above minimal threshold, VSRFs recorded in otherwise quiet and anechoic space fall into categories based on spatial dimension and location. The size, shape and location of VSRFs remain stable over many hours of recording and are found to be shaped by excitatory and inhibitory interactions of activity arriving from the two ears. Within the VSRF response latency and strength vary systematically with stimulus direction. In an ensemble of such neurons these functional gradients provide information about stimulus direction, which closely accounts for a human listener's spatial acuity. Raising stimulus intensity, introducing continuous background noise or presenting a conditioning stimulus all influence the extent of the VSRF but leave intact the gradient structure of the field. These and other findings suggest that such functional gradients in VSRFs of ensembles of AI neurons are instrumental in coding sound direction and robust enough to overcome interference from competing environmental sounds.     

The Opponent Channel Population Code of Sound Location Is an Efficient Representation of Natural Binaural Sounds

In mammalian auditory cortex, sound source position is represented by a population of broadly tuned neurons whose firing is modulated by sounds located at all positions surrounding the animal. Peaks of their tuning curves are concentrated at lateral position, while their slopes are steepest at the interaural midline, allowing for the maximum localization accuracy in that area. These experimental observations contradict initial assumptions that the auditory space is represented as a topographic cortical map. It has been suggested that a “panoramic” code has evolved to match specific demands of the sound localization task. This work provides evidence suggesting that properties of spatial auditory neurons identified experimentally follow from a general design principle- learning a sparse, efficient representation of natural stimuli. Natural binaural sounds were recorded and served as input to a hierarchical sparse-coding model. In the first layer, left and right ear sounds were separately encoded by a population of complex-valued basis functions which separated phase and amplitude. Both parameters are known to carry information relevant for spatial hearing. Monaural input converged in the second layer, which learned a joint representation of amplitude and interaural phase difference. Spatial selectivity of each second-layer unit was measured by exposing the model to natural sound sources recorded at different positions. Obtained tuning curves match well tuning characteristics of neurons in the mammalian auditory cortex. This study connects neuronal coding of the auditory space with natural stimulus statistics and generates new experimental predictions. Moreover, results presented here suggest that cortical regions with seemingly different functions may implement the same computational strategy-efficient coding.     

Broadband Onset Inhibition Can Suppress Spectral Splatter in the Auditory Brainstem

In vivo intracellular responses to auditory stimuli revealed that, in a particular population of cells of the ventral nucleus of the lateral lemniscus (VNLL) of rats, fast inhibition occurred before the first action potential. These experimental data were used to constrain a leaky integrate-and-fire (LIF) model of the neurons in this circuit. The post-synaptic potentials of the VNLL cell population were characterized using a method of triggered averaging. Analysis suggested that these inhibited VNLL cells produce action potentials in response to a particular magnitude of the rate of change of their membrane potential. The LIF model was modified to incorporate the VNLL cells’ distinctive action potential production mechanism. The model was used to explore the response of the population of VNLL cells to simple speech-like sounds. These sounds consisted of a simple tone modulated by a saw tooth with exponential decays, similar to glottal pulses that are the repeated impulses seen in vocalizations. It was found that the harmonic component of the sound was enhanced in the VNLL cell population when compared to a population of auditory nerve fibers. This was because the broadband onset noise, also termed spectral splatter, was suppressed by the fast onset inhibition. This mechanism has the potential to greatly improve the clarity of the representation of the harmonic content of certain kinds of natural sounds.