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Sound direction modifies the inhibitory as well as the excitatory frequency tuning characteristics of single neurons in the frog torus semicircularis (inferior colliculus).

Single-unit recordings were made from the frog inferior colliculus to determine whether or not the direction-dependent sharpening of a unit's free-field excitatory frequency-threshold curve (FTCe) was accompanied by a broadening of its inhibitory frequency-threshold curve (FTCi). To determine the FTCi, a two-tone-suppression paradigm was employed. The unit's FTCis and FTCes were collected at three azimuths: contralateral to the recording site, ipsilateral to the recording site, and frontal midline. The result showed that: (1) most inferior colliculus neurons (95%) displayed two-tone suppression, (2) the majority (54%) of neurons displayed stronger two-tone-suppression leading to broader FTCis when the sound was presented from the ipsilateral side than from the contralateral side, (3) for some neurons, the borders of the FTCes and FTCis were closely aligned, and this juxtaposition persisted at all sound azimuths (namely, when a change in sound direction produced a narrowing of a unit's FTCe, its FTCi was broadened concomitantly). For the remaining neurons, however, direction-dependent sharpening of the FTCe was not accompanied by an increase in two-tone-suppression. The neural mechanisms that underlie the direction-dependent changes in the FTCes and FTCis are discussed.

Animals↗

Encoding of acoustic directional information by saccular afferents of the sleeper goby, Dormitator latifrons.

This paper reports on directional response properties of saccular afferents of the sleeper goby, Dormitator latifrons, to 100-Hz acoustic particle motions with a focus on testing the hypothesis that the response directionality of a fish's auditory afferents derives from the morphological polarity of sensory hair cells in the otolithic organs. Spontaneous rates (SR) and best sensitivities (BS) of saccular afferents ranged from 0 to 162 spikes/sec and from 0.2-to 100-nm RMS displacement. SR did not vary with BS. Most saccular afferents were phase-locked to sinusoidal stimulation and had sustained temporal response patterns with some adaptation. All saccular afferents were directionally sensitive to the stimulus, and the sharpness of directional response curves was determined by a directionality index (DI). The DI ranged from 0.64 to 1.50 (mean = 1.02, SE = 0.02, n = 100) and gradually decreased with stimulus level throughout afferents' response dynamic range. Many afferents had approximately symmetric directional response curves relative to their best response axes (BRA). BRA of most afferents remained constant with stimulus level. The BRA distribution had a peak along an axis that correlates closely with the morphological polarity of saccular hair cells. Therefore, our results strongly support the hypothesis.

Acoustic Stimulation↗

Corticofugal regulation of auditory sensitivity in the bat inferior colliculus.

Under free-field stimulation conditions, corticofugal regulation of auditory sensitivity of neurons in the central nucleus of the inferior colliculus of the big brown bat, Eptesicus fuscus, was studied by blocking activities of auditory cortical neurons with Lidocaine or by electrical stimulation in auditory cortical neuron recording sites. The corticocollicular pathway regulated the number of impulses, the auditory spatial response areas and the frequency-tuning curves of inferior colliculus neurons through facilitation or inhibition. Corticofugal regulation was most effective at low sound intensity and was dependent upon the time interval between acoustic and electrical stimuli. At optimal inter-stimulus intervals, inferior colliculus neurons had the smallest number of impulses and the longest response latency during corticofugal inhibition. The opposite effects were observed during corticofugal facilitation. Corticofugal inhibitory latency was longer than corticofugal facilitatory latency. Iontophoretic application of gamma-aminobutyric acid and bicuculline to inferior colliculus recording sites produced effects similar to what were observed during corticofugal inhibition and facilitation. We suggest that corticofugal regulation of central auditory sensitivity can provide an animal with a mechanism to regulate acoustic signal processing in the ascending auditory pathway.

Animals↗

Neural inhibition sharpens auditory spatial selectivity of bat inferior collicular neurons.

This study examines the role of neural inhibition in auditory spatial selectivity of inferior collicular neurons of the big brown bat, Eptesicus fuscus, using a two-tone inhibition paradigm. Two-tone inhibition decreases auditory spatial response areas but increases the slopes of directional sensitivity curves of inferior collicular neurons. Inferior collicular neurons have either directionally-selective or hemifield directional sensitivity curves. A directionally-selective curve always has a peak which is at least 50% larger than the minimum. A hemifield directional sensitivity curve rises from an ipsilateral angle by more than 50% and either reaches a plateau or declines by less than 50% over a range of contralateral angles. Two-tone inhibition does not change directionally-selective curves but changes most hemifield directional sensitivity curves into directionally-selective curves. Auditory spatial selectivity determined both with and without two-tone inhibition increases with increasing best-excitatory frequency. Sharpening of auditory spatial selectivity by two-tone inhibition is larger for neurons with smaller differences between excitatory and inhibitory best frequencies. The effect of two-tone inhibition on auditory spatial selectivity increases with increasing inhibitory tone intensity but decreases with increasing intertone interval. The implications of these findings in bat echolocation are discussed.

Animals↗

A neural network model of the inferior colliculus with modifiable lateral inhibitory synapses for human echolocation.

We propose a neural network model of the inferior colliculus (IC) for human echolocation. Neuronal mechanisms for human echolocation were investigated by simulating the model. The model consists of the neural networks of the central nucleus (ICc) and external nucleus (ICx) of the inferior colliculus. The neurons of the ICc receive interaural sound stimuli via multiple contralateral delay lines and a single ipsilateral delay line. The neurons of the ICc send output signals to the neurons of the ICx in a convergent manner. We stimulated the ICc with pairs of a direct sound (a sonar sound) and an echo sound (the reflection from an object). Information about the distance between the model and the object is expressed by the delay time of the echo sound with respect to the direct sound. The results presented here show that neurons of the ICc responsive to interaural onset time differences contribute to the creation of an auditory distance map in the ICx. We trained the model with various pairs of direct-echo sounds and modified synaptic connection strengths of the networks according to the Hebbian rule. It is shown that self-organized long-term depression of lateral inhibitory synaptic connections plays an important role in enhancing echolocation skills.

Acoustic Stimulation↗

The synthesis and use of the owl's auditory space map.

The barn owl ( Tyto alba) is capable of capturing prey by passive hearing alone, guided by a topographic map of auditory space in the external nucleus of its inferior colliculus. The neurons of this auditory space map have discrete spatial receptive fields that result from the computation of interaural differences in the level (ILD) and time-of-arrival (ITD) of sounds. Below we review the synthesis of the spatial receptive fields from the frequency-specific ITDs and ILDs to which the neurons are tuned, concentrating on recent studies exploiting virtual auditory space techniques to analyze the contribution of ILD. We then compared the owl's spatial discrimination, assessed behaviorally, with that of its space map neurons. Spatial discrimination was assessed using a novel paradigm involving the pupillary dilation response (PDR), and neuronal acuity was assessed by measuring the changes in firing rate resulting from changes in source location, scaled to the variance. This signal-detection-based approach revealed that the change in the position of the neural image on this map best explains the spatial discrimination measured using the PDR. We compare this result to recent studies in mammalian systems.

Animals↗

Modeling coincidence detection in nucleus laminaris.

A biologically detailed model of the binaural avian nucleus laminaris is constructed, as a two-dimensional array of multicompartment, conductance-based neurons, along tonotopic and interaural time delay (ITD) axes. The model is based primarily on data from chick nucleus laminaris. Typical chick-like parameters perform ITD discrimination up to 2 kHz, and enhancements for barn owl perform ITD discrimination up to 6 kHz. The dendritic length gradient of NL is explained concisely. The response to binaural out-of-phase input is suppressed well below the response to monaural input (without any spontaneous activity on the opposite side), implicating active potassium channels as crucial to good ITD discrimination.

Animals↗

Stochastic correlative firing for figure-ground segregation.

Segregation of sensory inputs into separate objects is a central aspect of perception and arises in all sensory modalities. The figure-ground segregation problem requires identifying an object of interest in a complex scene, in many cases given binaural auditory or binocular visual observations. The computations required for visual and auditory figure-ground segregation share many common features and can be cast within a unified framework. Sensory perception can be viewed as a problem of optimizing information transmission. Here we suggest a stochastic correlative firing mechanism and an associative learning rule for figure-ground segregation in several classic sensory perception tasks, including the cocktail party problem in binaural hearing, binocular fusion of stereo images, and Gestalt grouping in motion perception.

Acoustic Stimulation↗

A simple latency-dependent spiking-neuron model of cricket phonotaxis.

A simple hypothesis regarding the recognition behaviour of crickets for conspecific songs is implemented in a dynamic simulation of spiking neurons and tested on a robot base. The model draws on data from cricket neurophysiology but requires only four neurons to reproduce a wide range of the observed behaviour. The directional response depends on relative latencies in firing onset, and the 'recognition' emerges from the implicit filtering properties of leaky-integrate-and-fire neurons. Experimental conditions reproduced include tests of syllable rate preference, song from above with sound from one side, and choice between songs. The robot produces behaviour closely comparable to the cricket in all but a 'split-song' condition. A number of properties can be observed in the neural circuit that correspond to cricket neurophysiology including apparent 'recognition neurons'. Limitations of the model, extensions and alternative models are discussed.

Action Potentials↗

The role of instructions, practice, and stimulus-hand correspondence on the Simon effect.

Numerous studies of two-choice reaction tasks, including auditory and visual Simon tasks (i.e., tasks in which stimulus location is irrelevant) and visual compatibility tasks, have found that only spatial stimulus-response (S-R) correspondence affected S-R compatibility. Their results provided no indication that stimulus-hand correspondence was a significant factor. However, Wascher et al. (2001) suggested that hand coding plays a role in visual and auditory Simon tasks when the instructions are in terms of the finger/hand used for responding. The present experiments examined whether instructing subjects in terms of response locations or fingers/hands influenced the Simon effect for visual and auditory tasks. In Experiments 1-3, only spatial S-R correspondence contributed significantly to the Simon effect, even when the instructions were in terms of the fingers/hands. However, in Experiment 4, which used auditory stimuli and finger/hand instructions, the contribution of stimulus-hand correspondence increased with practice.

Acoustic Stimulation↗

Stimulus and response repetition effects in the detection of sounds: evidence of obligatory retrieval and use of a prior event.

Three experiments were performed to examine the extent to which the time required to detect a probe sound is determined by the acoustic characteristics of a preceding prime sound and by the nature of the response made to the prime. The results of Experiment 1 revealed that the effect of frequency repetition was facilitative when a response was made to the occurrence of both the prime and the probe, but was inhibitory when a response was made only to the probe. In contrast, there was no significant effect of location repetition when responses were made to both prime and probe but there was a strongly inhibitory effect when a response was required only to the probe. These results suggest that the acoustic characteristics of the prime along with information about any response made to it, are used in preparing and executing a response to the probe. Experiment 2 was designed to disrupt the temporal link between prime and probe as a way to discourage such retrieval. The results of the experiment revealed that although a response was required to both the prime and probe, no significant effect of frequency repetition was apparent but a robust inhibitory effect of location repetition emerged. In the third experiment repetition effects both within a trial (i.e., prime to probe) and between trials (i.e., probe to prime) were examined. A facilitative effect of frequency repetition was apparent when the interval between sounds was brief, and an inhibitory effect of location repetition was apparent when the interval between sounds was relatively lengthy. Taken together these results suggest that even simple perceptual judgments may be influenced by retrieval of information about a previous processing episode and that effects of frequency repetition and location repetition may be mediated by different mechanisms.

Association Learning↗

The medial nucleus of the trapezoid body in the gerbil is more than a relay: comparison of pre- and postsynaptic activity.

The medial nucleus of the trapezoid body (MNTB) plays an important role in the processing of interaural intensity differences, a feature that is critical for the localization of sound sources. It is generally believed that the MNTB functions primarily as a passive relay in converting excitatory input originating from the contralateral cochlear nucleus (CN) into an inhibitory input to the ipsilateral lateral superior olive. However, studies showing that the MNTB itself is also the target of inhibitory input suggest that the MNTB may serve more than a sign-converting function. To examine the fidelity of signal transmission at the CN-MNTB synapse, presynaptic calyceal potentials ("prepotentials"), reflecting the excitatory input to the MNTB neuron, and postsynaptic action potentials were simultaneously monitored with the same electrode during in vivo extracellular recordings from the gerbil's MNTB. Presynaptic activity differed from postsynaptic activity in several respects: (1) Spontaneous and sound-evoked discharge rates were greater presynaptically than postsynaptically. (2) Frequency tuning was sharper postsynaptically than presynaptically. (3) Calyceal terminals and MNTB neurons both showed phasic-tonic response patterns to tonal stimulation, but the duration of the onset response and the level of the tonic component were reduced postsynaptically. (4) Phase-locking to sound frequencies up to 1 kHz was greater postsynaptically than presynaptically. (5) The rate-intensity characteristics of pre- and postsynaptic activities differed significantly from each other in half of the MNTB neurons. To test the hypothesis that acoustically evoked inhibition of MNTB neurons contributed to the relatively lower levels of postsynaptic discharge, two-tone stimulation was applied, wherein the response to one tone-burst, set at the neuron's characteristic frequency, can be reduced by addition of a second "inhibitory" tone. The inhibitory tone caused a much larger reduction in post- than in presynaptic activity, indicating an acoustically evoked inhibitory influence directly on MNTB units. These findings show that transmission at the CN-MNTB synapse does not occur in a fixed one-to-one manner and that the response of MNTB neurons reflects the integration of their excitatory and inhibitory inputs.

Action Potentials↗

Sensitivity to interaural correlation of single neurons in the inferior colliculus of guinea pigs.

Sensitivity to changes in the interaural correlation of 50-ms bursts of narrowband or broadband noise was measured in single neurons in the inferior colliculus of urethane-anaesthetized guinea pigs. Rate vs. interaural correlation functions (rICFs) were measured using two methods. These methods compensated in different ways for the inherent variance in interaural correlation between tokens with the same expected correlation. The shape of all rICFs could be best described by power functions allowing them to be summarized by two parameters. Most rICFs were best fit by a power below 2, indicating that they were only slightly nonlinear. However, there were a few fitted functions that had a power of 3-6, indicating marked curvature. Modeling results indicate that the nonlinearity of the majority of rICFs was explicable in terms of the monaural transduction stages; however, some of the rICFs with power greater than 2 require either multiple inputs to the coincidence detector or additional nonlinearities to be included in the model. Discrimination thresholds were estimated at reference correlations of -1, 0, and +1 using receiver operating characteristic (ROC) analysis of the spike-count distribution at each correlation. Thresholds spanned the full possible range, from a minimum of 0.1 to the maximum possible of 2. Thresholds were generally highest with a reference correlation of -1, intermediate with a reference of 0, and lowest with a reference correlation of +1. Thresholds were lowest for the most steeply sloped rICFs, but thresholds were not strongly correlated to the spike rate variance. The lowest thresholds occurred using narrowband noise that was compensated for internal delays, but they were still about three times larger than human psychophysical thresholds measured using similar stimuli. The data suggest that, unlike pure tone interaural time difference, discrimination of a population measure is required to account for behavioral interaural correlation discrimination performance.

Anesthesia↗

Effects of stimulation mode, level and location on forward-masked excitation patterns in cochlear implant patients.

In multi-channel cochlear implants, electrical current is delivered to appropriate electrodes in the cochlea to approximate the spatial representation of speech. Theoretically, electrode configurations that restrict the current spread within the cochlea (e.g., bi- or tri-polar stimulation) may provide better spatial selectivity, and in turn, better speech recognition than configurations that produce a broader current spread (e.g., monopolar stimulation). However, the effects of electrode configuration on supra-threshold excitation patterns have not been systematically studied in cochlear implant patients. In the present study, forward-masked excitation patterns were measured in cochlear implant patients as functions of stimulation mode, level and location within the cochlea. All stimuli were 500 pulses-per-second biphasic pulse trains (200 micros/phase, 20 micros inter-phase gap). Masker stimuli were 200 ms in duration; the bi-polar configuration was varied from narrow (BP+1) to wide (BP+17), depending on the test condition. Probe stimuli were 20 ms in duration and the masker-probe delay was 5 ms; the probe configuration was fixed at BP+1. The results indicated that as the distance between the active and return electrodes in a bi-polar pair was increased, the excitation pattern broadened within the cochlea. When the distance between active and return electrodes was sufficiently wide, two peaks were often observed in the excitation pattern, comparable to non-overlapping electric fields produced by widely separated dipoles. Analyses of the normalized data showed little effect of stimulation level on the shape of the excitation pattern.

Adult↗

Discrimination of direction in fast frequency-modulated tones by rats.

Fast frequency modulations (FM) are an essential part of species-specific auditory signals in animals as well as in human speech. Major parameters characterizing non-periodic frequency modulations are the direction of frequency change in the FM sweep (upward/downward) and the sweep speed, i.e., the speed of frequency change. While it is well established that both parameters are represented in the mammalian central auditory pathway, their importance at the perceptual level in animals is unclear. We determined the ability of rats to discriminate between upward and downward modulated FM-tones as a function of sweep speed in a two-alternative-forced-choice-paradigm. Directional discrimination in logarithmic FM-sweeps was reduced with increasing sweep speed between 20 and 1,000 octaves/s following a psychometric function. Average threshold sweep speed for FM directional discrimination was 96 octaves/s. This upper limit of perceptual FM discrimination fits well the upper limit of preferred sweep speeds in auditory neurons and the upper limit of neuronal direction selectivity in the rat auditory cortex and midbrain, as it is found in the literature. Influences of additional stimulus parameters on FM discrimination were determined using an adaptive testing-procedure for efficient threshold estimation based on a maximum likelihood approach. Directional discrimination improved with extended FM sweep range between two and five octaves. Discrimination performance declined with increasing lower frequency boundary of FM sweeps, showing an especially strong deterioration when the boundary was raised from 2 to 4 kHz. This deterioration corresponds to a frequency-dependent decline in direction selectivity of FM-encoding neurons in the rat auditory cortex, as described in the literature. Taken together, by investigating directional discrimination of FM sweeps in the rat we found characteristics at the perceptual level that can be related to several aspects of FM encoding in the central auditory pathway.

Acoustic Stimulation↗

Auditory processing deficits in reading disabled adults.

The nature of the auditory processing deficit of disabled readers is still an unresolved issue. The quest for a fundamental, nonlinguistic, perceptual impairment has been dominated by the hypothesis that the difficulty lies in processing sequences of stimuli at presentation rates of tens of milliseconds. The present study examined this hypothesis using tasks that require processing of a wide range of stimulus time constants. About a third of the sampled population of disabled readers (classified as "poor auditory processors") had difficulties in most of the tasks tested: detection of frequency differences, detection of tones in narrowband noise, detection of amplitude modulation, detection of the direction of sound sources moving in virtual space, and perception of the lateralized position of tones based on their interaural phase differences. Nevertheless, across-channel integration was intact in these poor auditory processors since comodulation masking release was not reduced. Furthermore, phase locking was presumably intact since binaural masking level differences were normal. In a further examination of temporal processing, participants were asked to discriminate two tones at various intervals where the frequency difference was ten times each individual's frequency just noticeable difference (JND). Under these conditions, poor auditory processors showed no specific difficulty at brief intervals, contrary to predictions under a fast temporal processing deficit assumption. The complementary subgroup of disabled readers who were not poor auditory processors showed some difficulty in this condition when compared with their direct controls. However, they had no difficulty on auditory tasks such as amplitude modulation detection, which presumably taps processing of similar time scales. These two subgroups of disabled readers had similar reading performance but those with a generally poor auditory performance scored lower on some cognitive tests. Taken together, these results suggest that a large portion of disabled readers suffer from diverse difficulties in auditory processing. No parsimonious explanation based on current models of low-level auditory processing can account simultaneously for all these results, though increased within-channel noise is consistent with the majority of the deficits found in the subgroup of poorer auditory processors.

Adult↗

A modeling study of notch noise responses of type III units in the gerbil dorsal cochlear nucleus.

A computational model of the neural circuitry of the gerbil dorsal cochlear nucleus (DCN), based on the MacGregor's neuromime model, was used to simulate type III unit (P-cell) responses to notch noise stimuli. The DCN patch model is based on a previous computational model of the cat DCN [Hancock, K. E., and H. F. Voigt. Ann. Biomed. Eng. 27:73-87, 1999]. According to the experimental study of Parsons et al. [Ann. Biomed. Eng. 29:887-896, 2001], the responses of gerbil DCN type III units to notch noise stimuli are similar to those of cat DCN type IV units, which are thought to be spectral notch detectors. This suggests that type III units in the gerbil DCN may serve as spectral notch detectors. In this modeling study, a simplified notch noise response plot--spike discharge rate vs. notch cutoff frequency plot--was used to compare model responses to the experimental results. Parameter estimation and sensitivity analysis of three connection parameters within the DCN patch have been studied and shows the model is robust, providing reasonable fits to the experimental data from 14 of 15 type III units examined.

Acoustic Stimulation↗

Auditory detection of motion velocity in humans: a magnetoencephalographic study.

To investigate the cerebral mechanisms of auditory detection of motion velocity in the human brain, neuromagnetic fields elicited by six moving sounds and one stationary sound were investigated with a whole-cortex magnetoencephalography (MEG) system. The stationary sound evoked only one clear response at a latency of 109+/-6 ms (first response, or M100), but the six moving sounds evoked two clear responses: an earlier response at a latency of 116+/-7 ms (M100) and a later response at a latency ranging from 180 to 760 ms (magnetic motion response, or MM). The latency and amplitude of the MM were inversely related to the velocity of the moving sounds (p<0.02). The magnetic source of MM was related to the velocity of the moving sounds (p<0.05). A dynamic neuromagnetic response, MM, was elicited by the moving sounds, which likely encoded the neural processing of auditory detection of motion velocity. A specific neural network that processes the motion velocity in the human brain probably includes the bilateral superior temporal cortices and the brainstem. The left posterior and lateral part of the auditory cortex may play a pivotal role in the auditory detection of motion velocity.

Acoustic Stimulation↗