Auditory Midbrain Neurons Research Articles

Temporal peculiarities of responses of auditory system neurons of the frog Rana temporaria to tone bursts with different modulation frequencies

Activity of medullar and midbrain auditory neurons at action of amplitude-modulated tone burst was recorded in immobilized common frogs Rana temporaria. Depth of modulation amounted to 10% or 80%, frequency of modulation varied from 5 to 150 Hz, and carrier intensity was in the range of 20-30 dB. Phasic neurons in medulla clearly reproduced the modulation frequency, but only at the 80% modulation depth. However, during presentation of signal with the 10% modulation depth, these neurons practically did not respond. Tonic neurons were able to reproduce the modulation frequency up to 10-150 Hz, but at the 10% modulation depth, the degree of reproduction of envelope was rather low, although for several first modulation periods it rose statistically significantly. In midbrain, the highest frequency of the reproduced modulation sharply fell. At greater modulation frequencies, the response of these neurons qualitatively reminds that of medullar neurons. At the low modulation frequencies, there is identified a group of midbrain neurons with a prominent increase of the signal modulation. This occurs in the frequency diapason up to 60 Hz; at an increase of the modulation frequency the time of achievement of maximal synchronization decreases. The optimal modulation frequency in many neurons of semicircular torus corresponds to parameters of the male mating call.

The predictive power of spectrotemporal receptive fields at the single spike train level

Event Abstract Back to Event The predictive power of spectrotemporal receptive fields at the single spike train level Auditory neurons encode the acoustic features of complex sounds according to tuning properties that make them particularly responsive to specific spectral and temporal cues. Reverse correlation models of tuning such as spectrotemporal receptive fields (STRFs) estimate the spectral and temporal tuning properties of neurons from responses to complex sounds. The accuracy of a STRF in capturing the response properties of a neuron is assessed by using the STRF to predict responses to novel sounds and comparing those predictions to peristimulus time histograms (PSTHs) of the actual responses. A PSTH averages the neural response over multiple trials and has lower temporal precision than individual spikes. Because an animal can identify a complex sound after hearing it only once, neural responses at the single spike train level, as opposed to averaged over many trials, may be highly relevant to perception. Therefore, accurate models of neural tuning should predict neural responses to a sound at the single spike train level. We asked how accurately STRFs predict individual responses to complex communication sounds. Songbirds reliably discriminate among the unique songs of individual birds. Songbird auditory midbrain neurons reliably produce spike trains that share precise temporal structure across trials. These neurons encode spectrotemporal features of songs, and their STRFs predict responses at the PSTH level well. We tested the accuracy of STRFs in predicting neural responses at the single spike train level. We recorded the responses of single auditory midbrain neurons in male zebra finches to song from 20 other males. We modeled single spike trains from those songs using a linear-nonlinear-Poisson cascade model (LNP). Using an inhomogeneous Poisson process, simulated spike trains were generated based on a STRF convolved with a song spectrogram. Simulated spike trains share temporal structure with actual spike trains, but are less reliable across trials and are therefore less temporally precise. We quantified the temporal precision of spike trains across the actual and simulated trials, and between actual and simulated spike trains from the same songs. The k-means neurometric applies the k-means clustering algorithm to Euclidean distances between spike trains as defined in the van Rossum spike timing metric. Spike trains were sorted into k groups, where k is the number of unique stimuli used to generate spike trains. Accuracy in discriminating among songs was calculated as the percentage of spike trains that cluster into the appropriate group. As a population, actual responses of MLd neurons to songs demonstrate highly accurate k-means discriminability. STRF-based LNP simulations typically fail to capture the stimulus discriminating capacity of actual neurons. This is largely due to the temporal imprecision generated by the STRF-based model. Simulated spike train clusters were more scattered than actual spike trains, and clusters were generally closer under the simulated condition. The deficiency of the STRF-based model may be due in part to an inability to resolve rapid temporal features of the stimulus. We propose methods for supplementing and improving the STRF-based LNP model, such as incorporating parameters that capture the neural response to amplitude modulations within a stimulus. Conference: Computational and systems neuroscience 2009, Salt Lake City, UT, United States, 26 Feb - 3 Mar, 2009. Presentation Type: Poster Presentation Topic: Poster Presentations Citation: (2009). The predictive power of spectrotemporal receptive fields at the single spike train level. Front. Syst. Neurosci. Conference Abstract: Computational and systems neuroscience 2009. doi: 10.3389/conf.neuro.06.2009.03.245 Copyright: The abstracts in this collection have not been subject to any Frontiers peer review or checks, and are not endorsed by Frontiers. They are made available through the Frontiers publishing platform as a service to conference organizers and presenters. The copyright in the individual abstracts is owned by the author of each abstract or his/her employer unless otherwise stated. Each abstract, as well as the collection of abstracts, are published under a Creative Commons CC-BY 4.0 (attribution) licence (https://creativecommons.org/licenses/by/4.0/) and may thus be reproduced, translated, adapted and be the subject of derivative works provided the authors and Frontiers are attributed. For Frontiers’ terms and conditions please see https://www.frontiersin.org/legal/terms-and-conditions. Received: 03 Feb 2009; Published Online: 03 Feb 2009. Login Required This action requires you to be registered with Frontiers and logged in. To register or login click here. Abstract Info Abstract The Authors in Frontiers Google Google Scholar PubMed Related Article in Frontiers Google Scholar PubMed Abstract Close Back to top Javascript is disabled. Please enable Javascript in your browser settings in order to see all the content on this page.

Mechanisms of Long-Interval Selectivity in Midbrain Auditory Neurons: Roles of Excitation, Inhibition, and Plasticity

Stereotyped intervals between successive sound pulses characterize the acoustic signals of anurans and other organisms and provide critical information to receivers. One class of midbrain neuron responds selectively when pulses are repeated at slow rates (long intervals). To examine the mechanisms that underlie long-interval selectivity, we made whole cell recordings, in vivo, from neurons in the anuran inferior colliculus (anuran IC). In most cases, long-pass interval selectivity appeared to arise from interplay between excitation and inhibition; in approximately 25% of these cases, the delayed inhibition to a pulse overlapped with the excitation to the following pulse at fast pulse repetition rates (PRRs), resulting in a phasic "onset" response. In the remaining cases, inhibition appeared to precede excitation. These neurons did not respond to fast PRRs apparently because delayed excitation to a pulse overlapped with the inhibition to the following pulse. These results suggest that the relative timing of inhibition and excitation govern differences in the response properties of these two cell types. Loading cells with cesium increased their responses to fast AM rates, supporting a role for inhibition in long-interval selectivity. Three cells showed little or no evidence of inhibition and exhibited strong depression of excitation. These findings are discussed in the context of current models for long-pass interval selectivity.

Midbrain Auditory Neurons Integrate Excitation and Inhibition to Generate Duration Selectivity: AnIn VivoWhole-Cell Patch Study in Anurans

Sound duration can play a pivotal role in the reproductive behavior of anuran amphibians. Here, we report the first whole-cell recordings from duration-selective neurons in the anuran torus semicircularis, in vivo. We show that most short-pass duration-selective cells exhibited short-latency inhibition and delayed excitation. The duration of the inhibition increased with tone burst duration. Hence, for long-duration tone bursts, inhibition overlapped with excitation, reducing or eliminating spikes; no postinhibitory rebound was present. Other short-pass cells, however, showed inhibition only for long-duration tone bursts. Bandpass duration selectivity also involved interplay between inhibition and excitation; inhibition negated excitation with tone bursts that exceeded the optimum duration. Additionally, however, bandpass selectivity arose from stimulus-dependent excitation; tone bursts of sufficiently long duration were required to elicit excitation. Similarly, long-pass neurons showed inhibition and duration-dependent enhancement of excitation; long-pass selectivity resulted from enhanced excitation outlasting the transient inhibition or, in some cases, excitation overriding concurrent inhibition. Last, we evaluated the stimulus specificity of duration-selective neurons to variations in pulse repetition rate. We show that (1) most neurons that exhibited long-pass selectivity for tone-burst duration nonetheless responded to short-duration pulses when repeated at particular rates, and (2) some neurons that showed selectivity for tone burst duration also showed selectivity for pulse train duration. These novel response profiles appear to result from interplay between inhibition and time- and activity-dependent changes in excitation strength. These findings are discussed in the context of prevailing models of duration selectivity and acoustic communication in anurans.

Representation of Harmonic Sounds in the Helix of the Lateral Lemniscus

The percept of pitch of harmonic sounds is based on temporal processing. This explains also our ability to recognize harmonic relationships between different sounds, because as a result of a neuronal correlation analysis in the auditory midbrain neurons are tuned not only to a certain pitch but to a certain degree also to integer multiples of that pitch. The responses to harmonics of a pitch are suppressed within 30 ms after signal onset by inhibition with the likely source being the ventral nucleus of the lateral lemniscus (VNLL). An investigation of spatial representation of periodicity information with the 2-Deoxyglucose method in gerbils showed that low pitch is represented dorsally and high pitch ventrally along the length-axis of the VNLL. Three-dimensional computer reconstructions of the VNLL (program AMIRA) gave evidence for a helical periodicity map with 7 to 8 turns, reminiscent of the pitch helix known from music psychology. Moreover, the spatial organization of the VNLL suggests that it is organized as a double-helix representing musical octaves and fifths. Reconstructions of the VNLL of Nissl-stained human brains gave evidence of a similar organization and therefore of a similar functional role of the VNLL for pitch processing in humans.

Sound production and hearing ability in the Hawaiian sergeant fish

Sounds provide important signals for inter‐ and intraspecific communication in fishes, but few studies examine behavioral contexts of sound production and hearing ability within a single species. This study characterized the sounds and their behavioral contexts in a wild population of Hawaiian sergeant damselfishes (Abudefduf abdominalis), and compared their features to hearing sensitivity measured by both auditory‐evoked potentials (AEP) and single‐cell recordings in the auditory midbrain. The sergeant fish produces low intensity (∼85–115 dB rms re: 1 μPa), low‐frequency (∼100–400 Hz) sounds during nest preparation, courtship an agonistic interactions. Both AEP and single‐cell recordings show that fish are most sensitive to these frequencies (80–300 Hz) with best frequency at 100 Hz. However, auditory thresholds to tonal stimuli were approximately 20 dB lower for single‐cell recordings than those measured by AEP experiments. Further, midbrain auditory neurons were on average more sensitive to playbacks of conspecific sounds than to pure tones. These experiments show that the hearing ability of this damselfish closely matches the intensity and spectral characteristics of sounds produced in the wild. Multidimensional studies that incorporate analyses of and responses to biologically relevant natural sounds are necessary to understand acoustic processing and the evolution of acoustic communication in fishes.

Auditory Filters, Features, and Redundant Representations

Responses in auditory cortex tend to be weaker, more phasic, and noisier than those of auditory brainstem and midbrain nuclei. Is the activity in cortex therefore merely a "degraded echo" of lower-level neural representations? In this issue of Neuron, Chechik and colleagues show that, while cortical responses indeed convey less sensory information than auditory midbrain neurons, their responses are also much less redundant.

Novelty detector neurons in the mammalian auditory midbrain

Novel stimuli in all sensory modalities are highly effective in attracting and focusing attention. Stimulus-specific adaptation (SSA) and brain activity evoked by novel stimuli have been studied using population measures such as imaging and event-related potentials, but there have been few studies at the single-neuron level. In this study we compare SSA across different populations of neurons in the inferior colliculus (IC) of the rat and show that a subclass of neurons with rapid and pronounced SSA respond selectively to novel sounds. These neurons, located in the dorsal and external cortex of the IC, fail to respond to multiple repetitions of a sound but briefly recover their excitability when some stimulus parameter is changed. The finding of neurons that respond selectively to novel stimuli in the mammalian auditory midbrain suggests that they may contribute to a rapid subcortical pathway for directing attention and/or orienting responses to novel sounds.

Tuning for spectro-temporal modulations as a mechanism for auditory discrimination of natural sounds

Vocal communicators discriminate conspecific vocalizations from other sounds and recognize the vocalizations of individuals. To identify neural mechanisms for the discrimination of such natural sounds, we compared the linear spectro-temporal tuning properties of auditory midbrain and forebrain neurons in zebra finches with the statistics of natural sounds, including song. Here, we demonstrate that ensembles of auditory neurons are tuned to auditory features that enhance the acoustic differences between classes of natural sounds, and among the songs of individual birds. Tuning specifically avoids the spectro-temporal modulations that are redundant across natural sounds and therefore provide little information; rather, it overlaps with the temporal modulations that differ most across sounds. By comparing the real tuning and a less selective model of spectro-temporal tuning, we found that the real modulation tuning increases the neural discrimination of different sounds. Additionally, auditory neurons discriminate among zebra finch song segments better than among synthetic sound segments.

Processing of Modulated Sounds in the Zebra Finch Auditory Midbrain: Responses to Noise, Frequency Sweeps, and Sinusoidal Amplitude Modulations

The avian auditory midbrain nucleus, the mesencephalicus lateralis, dorsalis (MLd), is the first auditory processing stage in which multiple parallel inputs converge, and it provides the input to the auditory thalamus. We studied the responses of single MLd neurons to four types of modulated sounds: 1) white noise; 2) band-limited noise; 3) frequency modulated (FM) sweeps, and 4) sinusoidally amplitude-modulated tones (SAM) in adult male zebra finches. Responses were compared with the responses of the same neurons to pure tones in terms of temporal response patterns, thresholds, characteristic frequencies, frequency tuning bandwidths, tuning sharpness, and spike rate/intensity relationships. Most neurons responded well to noise. More than one-half of the neurons responded selectively to particular portions of the noise, suggesting that, unlike forebrain neurons, many MLd neurons can encode specific acoustic components of highly modulated sounds such as noise. Selectivity for FM sweep direction was found in only 13% of cells that responded to sweeps. Those cells also showed asymmetric tuning curves, suggesting that asymmetric inhibition plays a role in FM directional selectivity. Responses to SAM showed that MLd neurons code temporal modulation rates using both spike rate and synchronization. Nearly all cells showed low-pass or band-pass filtering properties for SAM. Best modulation frequencies matched the temporal modulations in zebra finch song. Results suggest that auditory midbrain neurons are well suited for encoding a wide range of complex sounds with a high degree of temporal accuracy rather than selectively responding to only some sounds.

Seasonal changes in frequency tuning and temporal processing in single neurons in the frog auditory midbrain

Frogs rely on acoustic signaling to detect, discriminate, and localize mates. In the temperate zone, reproduction occurs in the spring, when frogs emerge from hibernation and engage in acoustically guided behaviors. In response to the species mating call, males typically show evoked vocal responses or other territorial behaviors, and females show phonotactic responses. Because of their strong seasonal behavior, it is possible that the frog auditory system also displays seasonal variation, as evidenced in their vocal control system. This hypothesis was tested in male Northern leopard frogs by evaluating the response characteristics of single neurons in the torus semicircularis (TS; a homolog of the inferior colliculus) to a synthetic mating call at different times of the year. We found that TS neurons displayed a seasonal change in frequency tuning and temporal properties. Frequency tuning shifted from a predominance of TS units sensitive to intermediate frequencies (700-1200 Hz) in the winter, to low frequencies (100-600 Hz) in the summer. In winter and early spring, most TS neurons showed poor, or weak, time locking to the envelope of the amplitude-modulated synthetic call, whereas in late spring and early summer the majority of TS neurons showed robust time-locked responses. These seasonal differences indicate that neural coding by auditory midbrain neurons in the Northern leopard frog is subject to seasonal fluctuation.

Impact of the chorus environment on temporal processing of advertisement calls by gray treefrogs

Male gray treefrogs advertise for mates using calls that consist of a series of pulses. Pulse duration, interpulse interval, and pulse shape determine whether a call is recognized as a conspecific signal by females. Females use call rate and call pulse number to assess relative calling performance by males, and prefer males that display high calling efforts. However, within choruses call overlap among males and background noise can compromise the ability of females to detect and correctly interpret temporal information in calls. Phonotaxis tests using calls suffering from different patterns of overlap or with internal gaps were used to investigate specific consequences of interference and masking as well as mechanisms that might alleviate such problems. Our data indicate that females do not employ a process analogous to phonemic restoration to ‘‘fill in’’ missing call segments; however, if a sufficient percent of call elements fall within species-specific ranges, females may ignore call anomalies. Additional findings are generally consistent with those from a recent study on anuran auditory midbrain neurons that count and indicate that inappropriate pulse intervals can reset the pulse counting process. [Work supported by NSF and a Pace University Eugene M. Lang Research Fellowship.]

Naturalistic Auditory Contrast Improves Spectrotemporal Coding in the Cat Inferior Colliculus

Statistical analysis of natural sounds and speech reveals logarithmically distributed spectrotemporal modulations that can cover several orders of magnitude. By contrast, most artificial stimuli used to probe auditory function, including pure tones and white noise, have linearly distributed amplitude fluctuations with a limited average dynamic range. Here we explore whether the operating range of the auditory system is physically matched to the statistical structure of natural sounds. We recorded single-unit and multi-unit neuronal activity from the central nucleus of the cat inferior colliculus (ICC) in response to dynamic spectrotemporal sound sequences to determine whether ICC neurons respond preferentially to linear or logarithmic spectrotemporal amplitudes. We varied the intensity, dynamic range, and contrast statistics of these sounds to mimic those of natural and artificial stimuli. ICC neurons exhibited monotonic and nonmonotonic contrast dependencies with increasing dynamic range that were independent of the stimulus intensity. Midbrain neurons had higher firing rates and higher receptive field energies and showed a net improvement in spectrotemporal encoding ability for logarithmic stimuli, with an increase in the mutual information rate of approximately 50% over linear amplitude sounds. This efficient use of logarithmic spectrotemporal modulations by auditory midbrain neurons reflects a neural adaptation to structural regularities in natural sounds and likely underlies human perceptual abilities.

Computational model of modulation detection by the bullfrog

Bullfrog eighth-nerve fibers operate as envelope detectors, showing significant phase-locking to amplitude modulation (AM) rates as high as 800 Hz. A computational model that estimates stimulus period from all-order interval histograms (autocorrelation functions) aligned in time across frequency channels mimics fiber responses. The use of autocorrelation implies a mechanism based on delay lines or neural coincidence detection. The goal of this study was to determine the relevance of such a model in predicting responses of neurons in bullfrogs auditory midbrain (torus semicircularis) to AM stimuli. Modeled output of peripheral fibers was passed through a series of delay lines varying in latency, and then compared with actual midbrain data. There is a great diversity in representation of AM in the auditory midbrain, and this diversity is related to response latency and recording location. Neural responses from the cell sparse zone in the caudal midbrain were well-matched by a delay line mechanism, although the model was poorer in predicting response properties of other midbrain areas. [Work supported by NIH and the Brown University Brain Science Program.]

Spectro-temporal receptive fields of midbrain auditory neurons in the rat obtained with frequency modulated stimulation

Single unit responses at the auditory midbrain of the anesthetized rat were characterized in terms of spectro-temporal receptive field (STRF) using random frequency modulated (FM) tones and peri-spike averaging. STRFs were obtained from 121 FM-sensitive units covering a wide range of characteristic frequency (CF). Roughly half of the neurons showed clearly preferred stimulus time profiles that formed either a single, double or multiple bands. Neurons with a single-band STRF appeared to be sorted into positive or negative directional sensitivity for FM modulation on the basis of their CF either below or above 10 kHz. This directional selectivity is discussed in relation to the most sensitive part of the rat's audiogram.

Auditory temporal computation in fish

Fishes offer valuable opportunities for investigating auditory temporal computation. They use simple communication sounds. The ears and central auditory pathways are similar to those of other vertebrates, but the periphery is not specialized for frequency analysis as it is in mammals, and acoustic temporal analysis predominates. In the fish Pollimyrus, a small gas-filled bladder is coupled to each sacculus and translates acoustic pressure to motion of the hair cells. Behaviorally, these fish are sensitive to small differences in the temporal structure of sounds. Neurophysiological recordings from the auditory nerve show that sounds are faithfully encoded by the intervals between phase-locked spikes. This representation is transformed as it ascends the pathway, and is used in neural computations. In the auditory midbrain neurons are activated by particular temporal patterns. The selectivity of the auditory feature detectors results from neural computations that use synchronized trains of spikes as input. Computational modeling supports the hypothesis that a simple network, with three neurons and inhibitory gating, underlies the emergence of temporal tuning in the auditory midbrain. The slow kinetics of inhibition and postinhibitory rebound provide a basis for tuning to the long time intervals (10–50 ms) that are important in communication sounds. [Work supported by NIH Grant No. R01 DC01252.]

Neural population coding and auditory temporal pattern analysis

Over the 2 decades that have elapsed since Robert Erickson first published his pioneering work on across-fiber patterns in the gustatory system, the idea that information is represented by a population code has become almost universally accepted among neuroscientists. Although the concept of a population code is an implicit theoretical assumption underlying most of the work done in neuroscience today, the details of how population codes operate in specific systems remain unclear in many respects. This article reviews electrophysiological studies of the auditory system of echolocating bats that show that information about sound is initially represented across both space and time by relative amounts of activity in populations of excitatory and inhibitory neurons with different discharge patterns, different sensitivity functions, and different latencies. At the next level, each neuron in the auditory midbrain receives convergent input from a specific population of these lower brainstem neurons and acts as a “readout” of activity within this population. As a result, midbrain neurons become selectively tuned to stimulus features, for example, signal duration, to which neurons at lower levels respond indiscriminately. Intracellular recordings from auditory midbrain neurons show some of the mechanisms by which population input is processed. The known projection patterns of the midbrain “readout” neurons indicate that they, in turn, must become part of a new spatio-temporal population code that is transmitted to neurons at the thalamus, where additional forms of selectivity and patterns of output arise.

Interdependence of spatial and temporal coding in the auditory midbrain.

To date, most physiological studies that investigated binaural auditory processing have addressed the topic rather exclusively in the context of sound localization. However, there is strong psychophysical evidence that binaural processing serves more than only sound localization. This raises the question of how binaural processing of spatial cues interacts with cues important for feature detection. The temporal structure of a sound is one such feature important for sound recognition. As a first approach, we investigated the influence of binaural cues on temporal processing in the mammalian auditory system. Here, we present evidence that binaural cues, namely interaural intensity differences (IIDs), have profound effects on filter properties for stimulus periodicity of auditory midbrain neurons in the echolocating big brown bat, Eptesicus fuscus. Our data indicate that these effects are partially due to changes in strength and timing of binaural inhibitory inputs. We measured filter characteristics for the periodicity (modulation frequency) of sinusoidally frequency modulated sounds (SFM) under different binaural conditions. As criteria, we used 50% filter cutoff frequencies of modulation transfer functions based on discharge rate as well as synchronicity of discharge to the sound envelope. The binaural conditions were contralateral stimulation only, equal stimulation at both ears (IID = 0 dB), and more intense at the ipsilateral ear (IID = -20, -30 dB). In 32% of neurons, the range of modulation frequencies the neurons responded to changed considerably comparing monaural and binaural (IID =0) stimulation. Moreover, in approximately 50% of neurons the range of modulation frequencies was narrower when the ipsilateral ear was favored (IID = -20) compared with equal stimulation at both ears (IID = 0). In approximately 10% of the neurons synchronization differed when comparing different binaural cues. Blockade of the GABAergic or glycinergic inputs to the cells recorded from revealed that inhibitory inputs were at least partially responsible for the observed changes in SFM filtering. In 25% of the neurons, drug application abolished those changes. Experiments using electronically introduced interaural time differences showed that the strength of ipsilaterally evoked inhibition increased with increasing modulation frequencies in one third of the cells tested. Thus glycinergic and GABAergic inhibition is at least one source responsible for the observed interdependence of temporal structure of a sound and spatial cues.

Response of inferior colliculus neurons to electrical stimulation of the auditory nerve in neonatally deafened cats.

Response properties of neurons in the inferior colliculus (IC) were examined in control and profoundly deafened animals to electrical stimulation of the auditory nerve. Seven adult cats were used: two controls; four neonatally deafened (2 bilaterally, 2 unilaterally); and one long-term bilaterally deaf cat. All control cochleae were deafened immediately before recording to avoid electrophonic activation of hair cells. Histological analysis of neonatally deafened cochleae showed no evidence of hair cells and a moderate to severe spiral ganglion cell loss, whereas the long-term deaf animal had only 1-2% ganglion cell survival. Under barbiturate anesthesia, scala tympani electrodes were implanted bilaterally and the auditory nerve electrically stimulated using 100 micros/phase biphasic current pulses. Single-unit (n = 419) recordings were made through the lateral (LN) and central (ICC) nuclei of the IC; responses could be elicited readily in all animals. Approximately 80% of cells responded to contralateral stimulation, whereas nearly 75% showed an excitatory response to ipsilateral stimulation. Most units showed a monotonic increase in spike probability and reduction in latency and jitter with increasing current. Nonmonotonic activity was seen in 15% of units regardless of hearing status. Neurons in the LN exhibited longer latencies (10-25 ms) compared with those in the ICC (5-8 ms). There was a deafness-induced increase in latency, jitter, and dynamic range; the extent of these changes was related to duration of deafness. The ICC maintained a rudimentary cochleotopic organization in all neonatally deafened animals, suggesting that this organization is laid down during development in the absence of normal afferent input. Temporal resolution of IC neurons was reduced significantly in neonatal bilaterally deafened animals compared with acutely deafened controls, whereas neonatal unilaterally deafened animals showed no reduction. It would appear that monaural afferent input is sufficient to maintain normal levels of temporal resolution in auditory midbrain neurons. These experiments have shown that many of the basic response properties are similar across animals with a wide range of auditory experience. However, important differences were identified, including increased response latencies and temporal jitter, and reduced levels of temporal resolution.

Timing in the auditory system of the bat.

Echolocating bats use audition to guide much of their behavior. As in all vertebrates, their lower brainstem contains a number of parallel auditory pathways that provide excitatory or inhibitory outputs differing in their temporal discharge patterns and latencies. These pathways converge in the auditory midbrain, where many neurons are tuned to biologically important parameters of sound, including signal duration, frequency-modulated sweep direction, and the rate of periodic frequency or amplitude modulations. This tuning to biologically relevant temporal patterns of sound is created through the interplay of the time-delayed excitatory and inhibitory inputs to midbrain neurons. Because the tuning process requires integration over a relatively long time period, the rate at which midbrain auditory neurons respond corresponds to the cadence of sounds rather than their fine structure and may provide an output that is closely matched to the rate at which motor systems operate.