Auditory temporal processing: responses to sinusoidally amplitude-modulated tones in the inferior colliculus

Time-varying envelopes are a common feature of acoustic communication signals like human speech and induce a variety of percepts in human listeners. We studied the responses of 109 single neurons in the inferior colliculus (IC) of the anesthetized Mongolian gerbil to contralaterally presented sinusoidally amplitude-modulated (SAM) tones with a wide range of parameters. Modulation transfer functions (MTFs) based on average spike rate (rMTFs) showed regions of enhancement and suppression, where spike rates increased or decreased respectively as stimulus modulation depth increased. Specifically, almost all IC rMTFs could be described by some combination of a primary and a secondary region of enhancement and an intervening region of suppression, with these regions present to varying degrees in individual rMTFs. rMTF characteristics of most neurons were dependent on sound pressure level (SPL). rMTFs in most neurons with "onset" or "onset-sustained" peri-stimulus time histograms (PSTHs) in response to brief pure tones showed only a peaked primary region of enhancement. The region of suppression tended to occur in neurons with "sustained" or "pauser" PSTHs, and usually emerged at higher SPLs. The secondary region of enhancement was only found in eight neurons. The lowest modulation frequency at which the spike rate reached a clear peak ("best modulation frequency" or BMF) was measured. All but two mean BMFs lay between 0 and 100 Hz. Fifty percent of the 49 neurons tested over at least a 20-dB range of SPLs showed a BMF variation larger than 66% of their mean BMF. MTFs based on vector strength (tMTFs) showed a variety of patterns; although mostly similar to those reported from the cochlear nucleus, tMTFs of IC neurons showed higher maximum values, smaller dynamic range with depth, and a lower high-frequency limit for significant phase locking. Systematic and large increases in phase-lead commonly occurred as SPL increased. rMTFs measured at multiple carrier frequencies (F(c)s) showed that the suppressive region was not the result of sideband inhibition. There was no systematic relationship between BMF and F(c) of stimulation in the cells studied, even at low carrier frequencies. The results suggest various possible mechanisms that could create IC MTFs, and strongly support the idea that inhibitory inputs shape the rMTF by sharpening regions of enhancement and creating a suppressive region. The paucity of BMFs above 100 Hz argues against simple rate-coding schemes for pitch. Finally, any labeled line or topographic representation of modulation frequency is unlikely to be independent of SPL.     

Comparison of responses of neurons in the mouse inferior colliculus to current injections, tones of different durations, and sinusoidal amplitude-modulated tones

We made in vivo whole cell patch-clamp recordings from the inferior colliculus of young-adult, anesthetized C57/Bl6 mice to compare the responses to constant-current injections with the responses to tones of different duration or to sinusoidal amplitude-modulated (SAM) tones. We observed that voltage-dependent ion channels contributed in several ways to the response to tones. A sustained response to long tones was observed only in cells showing little accommodation during current injection. Cells showing burst-onset firing during current injection showed a small response to SAM tones, whereas burst-sustained cells showed a good response to SAM tones. The hyperpolarization-activated nonselective cation channel I(h) had a special role in shaping the responses: I(h) was associated with an increased excitability, with chopper and pauser responses, and with an afterhyperpolarization following tones. Synaptic properties were more important in determining the responses to tones of different durations. A short-latency inhibitory response appeared to contribute to the long-pass response in some cells and short-pass and band-pass neurons were characterized by their slow recovery from synaptic adaptation. Cells that recovered slowly from synaptic adaptation showed a relatively small response to SAM tones. Our results show an important role for both intrinsic membrane properties -- most notably the presence of I(h) and the extent of accommodation -- and synaptic adaptation in shaping the response to tones in the inferior colliculus.     

Phase-locked responses to pure tones in the inferior colliculus

In the auditory system, some ascending pathways preserve the precise timing information present in a temporal code of frequency. This can be measured by studying responses that are phase-locked to the stimulus waveform. At each stage along a pathway, there is a reduction in the upper frequency limit of the phase-locking and an increase in the steady-state latency. In the guinea pig, phase-locked responses to pure tones have been described at various levels from auditory nerve to neocortex but not in the inferior colliculus (IC). Therefore we made recordings from 161 single units in guinea pig IC. Of these single units, 68% (110/161) showed phase-locked responses. Cells that phase-locked were mainly located in the central nucleus but also occurred in the dorsal cortex and external nucleus. The upper limiting frequency of phase-locking varied greatly between units (80-1,034 Hz) and between anatomical divisions. The upper limits in the three divisions were central nucleus, >1,000 Hz; dorsal cortex, 700 Hz; external nucleus, 320 Hz. The mean latencies also varied and were central nucleus, 8.2 +/- 2.8 (SD) ms; dorsal cortex, 17.2 ms; external nucleus, 13.3 ms. We conclude that many cells in the central nucleus receive direct inputs from the brain stem, whereas cells in the external and dorsal divisions receive input from other structures that may include the forebrain.     

Neural correlates of the precedence effect in the inferior colliculus: effect of localization cues

The precedence effect (PE) is an auditory phenomenon involved in suppressing the perception of echoes in reverberant environments, and is thought to facilitate accurate localization of sound sources. We investigated physiological correlates of the PE in the inferior colliculus (IC) of anesthetized cats, with a focus on directional mechanisms for this phenomenon. We used a virtual space (VS) technique, where two clicks (a "lead" and a "lag") separated by a brief time delay were each filtered through head-related transfer functions (HRTFs). For nearly all neurons, the response to the lag was suppressed for short delays and recovered at long delays. In general, both the time course and the directional patterns of suppression resembled those reported in free-field studies in many respects, suggesting that our VS simulation contained the essential cues for studying PE phenomena. The relationship between the directionality of the response to the lead and that of its suppressive effect on the lag varied a great deal among IC neurons. For a majority of units, both excitation produced by the lead and suppression of the lag response were highly directional, and the two were similar to one another. For these neurons, the long-lasting inhibitory inputs thought to be responsible for suppression seem to have similar spatial tuning as the inputs that determine the excitatory response to the lead. Further, the behavior of these neurons is consistent with psychophysical observations that the PE is strongest when the lead and the lag originate from neighboring spatial locations. For other neurons, either there was no obvious relationship between the directionality of the excitatory lead response and the directionality of suppression, or the suppression was highly directional whereas the excitation was not, or vice versa. For these neurons, the excitation and the suppression produced by the lead seem to depend on different mechanisms. Manipulation of the directional cues (such as interaural time and level differences) contained in the lead revealed further dissociations between excitation and suppression. Specifically, for about one-third of the neurons, suppression depended on different directional cues than did the response to the lead, even though the directionality of suppression was similar to that of the lead response when all cues were present. This finding suggests that the inhibitory inputs causing suppression may originate in part from subcollicular auditory nuclei processing different directional cues than the inputs that determine the excitatory response to the lead. Neurons showing such dissociations may play an important role in the PE when the lead and the lag originate from very different directions.     

Over-representation of species-specific vocalizations in the awake mouse inferior colliculus

Social vocalizations are particularly important stimuli in an animal's auditory environment. Because of their importance, vocalizations should be strongly represented in auditory pathways. Mice commonly emit ultrasonic vocalizations with spectral content between 45 and 100 kHz. However, there is limited representation of these ultra-high frequencies (particularly those greater than 60 kHz) throughout the ascending auditory system. Here, we show that neurons in the inferior colliculus (IC) of mice respond strongly to conspecific vocalizations even though the energy in the vocalizations is above the neurons' frequency tuning curves. This results in an over-representation of species-specific vocalizations in the IC. In addition, neurons in mouse IC show selectivity among different vocalizations. Many vocalization-responsive neurons do not respond to the individual ultrasonic frequencies contained within the vocalizations, but they do respond to combinations of ultrasonic tones if the difference between the tones is within the excitatory frequency tuning curve. The combinations of tones that elicit responses are the quadratic and/or cubic intermodulation distortion components that are generated by the cochlea. Thus, the intermodulation distortions in the cochlea may provide a previously overlooked mechanism for auditory processing of complex stimuli such as vocalizations. The implication of these findings is that nonlinear interactions of frequencies, possibly caused by distortions in the system, may be used to enhance the sensitivity to behaviorally important stimuli.     

Glutamatergic and GABAergic regulation of neural responses in inferior colliculus to amplitude-modulated sounds

Recordings were made from single neurons in the rat inferior colliculus in response to sinusoidally amplitude-modulated sounds (10-s duration) presented to the contralateral ear. Neural responses were determined for different rates of modulation (0.5 Hz to 1 kHz) at a depth of 100%, and modulation transfer functions were generated based on firing rate (MTFFR) and vector strength (MTFVS). The effects of AMPA, NMDA, and GABAA receptor antagonists were examined by releasing drugs iontophoretically through a multibarrel pipette attached to a single-barrel recording pipette. Both the AMPA receptor antagonist, 1,2,3,4-tetrahydro-6-nitro-2,3-dioxo-benzo[f]quinoxaline-7-sulfonamide disodium (NBQX), and the NMDA receptor antagonist, (+/-)-3-(2-carboxypiperazin-4-yl)-propyl-1-phosphonic acid (CPP) resulted in a decrease in firing rate, and the GABAA receptor antagonist, bicuculline, produced an increase in the firing rate in most of the cells examined. In some cases, the shape of the MTFFR was modified slightly by receptor antagonists, but in most cases, the peak firing rate that determined a neuron's best modulation frequency remained the same. Also there were no changes during delivery of either excitatory or inhibitory antagonists in the maximum response synchrony at the peak of the MTFVS although some changes were noticed at off-peak modulation rates particularly with the AMPA receptor antagonist, NBQX.     

Prevalence of stereotypical responses to mistuned complex tones in the inferior colliculus

The human auditory system has an exceptional ability to separate competing sounds, but the neural mechanisms that underlie this ability are not understood. Responses of inferior colliculus (IC) neurons to "mistuned" complex tones were measured to investigate possible neural mechanisms for spectral segregation. A mistuned tone is a harmonic complex tone in which the frequency of one component has been changed; that component may be heard as a separate sound source, suggesting that the mistuned tone engages the same mechanisms that contribute to the segregation of natural sounds. In this study, the harmonic tone consisted of eight harmonics of 250 Hz; in the mistuned tone, the frequency of the fourth harmonic was increased by 12% (120 Hz). The mistuned tone elicited a stereotypical discharge pattern, consisting of peaks separated by about 8 ms and a response envelope modulated with a period of 100 ms, which bore little resemblance to the discharge pattern elicited by the harmonic tone or to the stimulus waveform. Similar discharge patterns were elicited from many neurons with a range of characteristic frequencies, especially from neurons that exhibited short-latency sustained responses to pure tones. In contrast, transient and long-latency neurons usually did not exhibit the stereotypical discharge pattern. The discharge pattern was generally stable when the stimulus level or component phase was varied; the major effect of these manipulations was to shift the phase of the response envelope. Simulation of IC responses with a computational model suggested that off-frequency inhibition could produce discharge patterns with these characteristics.     

Iso-frequency 2-DG contours in the inferior colliculus of the awake monkey

Summary Tone bursts produced bands of selective 2-[¹⁴C]-deoxyglucose labelling in the inferior colliculus (IC) of the awake monkey. Low tone frequencies produced labelling in dorsal regions and high tone frequencies produced labelling in ventral regions. The position of the bands coincided with the position of a single unit with a characteristic frequency, which was the same as the frequency producing the labelling. These findings indicate that the bands of labelling represent iso-frequency contours in IC. The iso-frequency contours extended across most of the nucleus and were oriented from dorsomedially to ventro-laterally at 20–30° from the horizontal and became more vertical anteriorly. The width of the contours was as narrow as 200 m, suggesting that the contours might represent 2 or 3 overlapping cellular laminae.Supported by research grants from the National Health and Medical Research Council of Australia and the Australian Research Grants Scheme     

Responses of inferior colliculus neurons to amplitude-modulated intracochlear electrical pulses in deaf cats

Current cochlear prostheses use amplitude-modulated pulse trains to encode acoustic signals. In this study we examined the responses of inferior colliculus (IC) neurons to sinusoidal amplitude-modulated pulses and compared the maximum unmodulated pulse rate (Fmax) to which they responded with the maximum modulation frequency (maxFm) that they followed. Consistent with previous results, responses to unmodulated pulses were all low-pass functions of pulse rate. Mean Fmax to unmodulated pulses was 104 pulses per second (pps) and modal Fmax was 60 pps. Above Fmax IC neurons ceased responding except for an onset burst at the beginning of the stimulus. However, IC neurons responded to much higher pulse rates when these pulses were amplitude modulated; 74% were relatively insensitive to carrier rate and responded to all modulated carriers including those exceeding 600 pps. In contrast, the responses of these neurons (70%) were low-pass functions of modulation frequency, and the remaining (30%) had band-pass functions with a maxFm of 42 and 34 Hz, respectively. Thus temporal resolution of IC neurons for modulated frequencies is significantly lower than that for unmodulated pulses. These two measures of temporal resolution (Fmax and maxFm) were uncorrelated (r(2) = 0.101). Several parameters influenced the amplitude and temporal structure of modulation responses including modulation depth, overall intensity and modulation-to-carrier rate ratio. We observed distortions in unit responses to amplitude-modulated signals when this ratio was 1/4 to 1/6. Since most current cochlear implant speech processors permit ratios that are significantly greater than this, severe distortion and signal degradation may occur frequently in these devices.     

Single unit responses in the inferior colliculus of the awake and performing rhesus monkey

1. The activity of single units in the inferior colliculus of unanesthetized monkeys was recorded during performance in an auditory reaction time task. Stimulus intensity and frequency were varied. 2. Spontaneous rate of unit discharge varied from 0 to 78.2 discharges per second, with a mean of 14.7 discharges/sec. 3. Both broadly and narrowly tuned units were encountered in the central nucleus of the inferior colliculus. The temporal discharge pattern of most units varied with changes in stimulus frequency; onset bursts and/or sustained discharge suppression dominated the unit discharge at the edges of receptive fields. 4. Half of the units examined at several intensity levels displayed nonmonotonic relationships between evoked discharge rate and stimulus intensity, with most nonmonotonic units showing a distinct "best intensity". The temporal response pattern of almost all units varied with changes in stimulus intensity, with onset bursts and discharge suppression increasing in occurrence with increasing intensity. 5. Units recorded in the external nucleus of the inferior colliculus displayed spontaneous rates which were similar to those of central nucleus units, and were affected by variation in stimulus intensity in the same fashion. However, the average initial latency of such units to intense stimuli was no longer than the latency of central nucleus units. 6. Variations in unit discharge with changes in stimulus frequency and intensity are consistent with an interaction of excitatory and inhibitory inputs with different initial latencies, dynamic ranges and receptive fields. In particular, our data suggest that inhibitory inputs have longer initial latencies and higher thresholds. Inhibition is stronger at the edges of a unit's receptive field, and dominates at high frequencies in units with low characteristic frequency. 7. Our data are not consistent with previous reports that single units in the unanesthetized animal display uniformly monotonic intensity functions and uniformly broad frequency responses.     

Neural mechanisms underlying selectivity for the rate and direction of frequency-modulated sweeps in the inferior colliculus of the pallid bat

This study describes mechanisms that underlie neuronal selectivity for the direction and rate of frequency-modulated sweeps in the central nucleus of the inferior colliculus (ICC) of the pallid bat (Antrozous pallidus). This ICC contains a high percentage of neurons (66%) that respond selectively to the downward sweep direction of the bat's echolocation pulse. Some (19%) are specialists that respond only to downward sweeps. Most neurons (83%) are also tuned to sweep rates. A two-tone inhibition paradigm was used to describe inhibitory mechanisms that shape selectivity for sweep direction and rate. Two different mechanisms can create similar rate tuning. The first is an early on-best frequency inhibition that shapes duration tuning, which in turn determines rate tuning. In most neurons that are not duration tuned, a delayed high-frequency inhibition creates rate tuning. These neurons respond to fast sweep rates, but are inhibited as rate slows, and delayed inhibition overlaps excitation. In these neurons, starting a downward sweep within the excitatory tuning curve eliminates rate tuning. However, if rate tuning is shaped by duration tuning, this manipulation has no effect. Selectivity for the downward sweep direction is created by an early low-frequency inhibition that prevents responses to upward sweeps. In addition to this asymmetry in arrival times of low- and high-frequency inhibitions, the bandwidth of the low-frequency sideband was broader. Bandwidth influences the arrival time of inhibition during an FM sweep because a broader sideband will be encountered sooner. These findings show that similar spectrotemporal filters can be created by different mechanisms.     

Timing of sound-evoked potentials and spike responses in the inferior colliculus of awake bats

Neurons in the inferior colliculus (IC), one of the major integrative centers of the auditory system, process acoustic information converging from almost all nuclei of the auditory brain stem. During this integration, excitatory and inhibitory inputs arrive to auditory neurons at different time delays. Result of this integration determines timing of IC neuron firing. In the mammalian IC, the range of the first spike latencies is very large (5-50 ms). At present, a contribution of excitatory and inhibitory inputs in controlling neurons' firing in the IC is still under debate. In the present study we assess the role of excitation and inhibition in determining first spike response latency in the IC. Postsynaptic responses were recorded to pure tones presented at neuron's characteristic frequency or to downward frequency modulated sweeps in awake bats. There are three main results emerging from the present study: (1) the most common response pattern in the IC is hyperpolarization followed by depolarization followed by hyperpolarization, (2) latencies of depolarizing or hyperpolarizing responses to tonal stimuli are short (3-7 ms) whereas the first spike latencies may vary to a great extent (4-26 ms) from one neuron to another, and (3) high threshold hyperpolarization preceded long latency spikes in IC neurons exhibiting paradoxical latency shift. Our data also show that the onset hyperpolarizing potentials in the IC have very small jitter (<100 mus) across repeated stimulus presentations. The results of this study suggest that inhibition, arriving earlier than excitation, may play a role as a mechanism for delaying the first spike latency in IC neurons.     

Discharge characteristics of neuronal pairs in the rabbit inferior colliculus

Summary Activity of neuronal pairs in the inferior colliculus of the rabbit was recorded with a single stainless-steel microelectrode. Seventy pairs were investigated with monaural and binaural tonal stimuli. The most common parameter of the response in neuronal pairs was the best frequency, which was similar in 100% of the pairs (n = 45). Q₁₀ values were indentical in 44% of pairs and threshold tuning curves in 27% of pairs. Units with a smaller spike amplitude usually had a shorter latency to both binaural and monaural stimuli, when measured 10–20 dB above the best frequency threshold. Most units discharged during the entire period of the 100 ms tone stimulation at their best frequency; large differences, however, were found in their firing pattern, when peristimulus histograms were compared. High correlation was found in pairs where both neurones exhibited the same type of binaural interaction. The following types of binaural interaction were found: binaural excitatory drive with occlusion, binaural excitatory drive with facilitation; monaural excitatory drive with inhibition from the other ear and pure monaural excitatory drive. In a significant number of neuronal pairs the influence of binaural stimulation was similar for both neurones. The results suggest that: (a) many adjacent neurones in the inferior colliculus convey parallel information concerning features of the auditory stimulus; (b) units with a similar type of binaural interaction may be organized in clusters within isofrequency layers.     

Intracellular recording reveals temporal integration in inferior colliculus neurons of awake bats

The central nucleus of the inferior colliculus (IC) is a major integrative center in the central auditory system. It receives information from both the ascending and descending auditory pathways. To determine how single IC neurons integrate information over a wide range of sound frequencies and sound levels, we examined their intracellular responses to frequency-modulated (FM) sounds in awake little brown bats (Myotis lucifugus). Postsynaptic potentials were recorded in response to downward FM sweeps of the range typical for little brown bats (80-20 kHz) and to three FM subcomponents (80-60, 60-40, and 40-20 kHz). The majority of recorded neurons responded to the 80- to 20-kHz downward FM sweep with a complex response. In this response an initial hyperpolarization was followed by depolarization with or without spike followed by hyperpolarization. Intracellular recordings in response to three FM subcomponents revealed that these neurons receive excitatory and inhibitory inputs from a wide range of sound frequencies. One third of IC neurons performed nearly linear temporal summation across a wide range of sound frequencies, whereas two thirds of IC neurons exhibited nonlinear summation with different degrees of nonlinearity. Some IC neurons showed different latencies of postsynaptic potentials in response to different FM subcomponents. Often responses to the later FM subcomponent occurred before responses to the earlier ones. This phenomenon may be responsible for response selectivity of IC neurons to FM sweeps.     

Sensitivity to binaural intensity and phase difference cues in kitten inferior colliculus.

1. Responses of single neurons to monaural or binaural CF tones delivered through a closed and calibrated sound delivery system were studied in the central nucleus of the inferior colliculus (ICC) in ketamine and barbiturate-anesthetized kittens 4-105 days old. 2. Neurons from young kittens had elevated thresholds, some greater than 100 dB in the youngest kittens tested. Average thresholds in the ICC matched those previously measured in the auditory nerve (AN), cochlear nuclei (CN), and auditory cortex (CTX), suggesting that the drop in threshold as a function of age is primarily determined by development at the periphery. 3. Minimal first-spike latencies were relatively long in the youngest kittens, approaching adult values by the end of the third postnatal week. Latencies were distributed between values previously determined for the CN and auditory cortex and can be attributed to the centripetal development of the auditory system. 4. The range of frequencies that were effective in exciting ICC neurons was restricted in young kittens. Neurons having characteristic frequencies (CFs) greater than 7 kHz were not recorded before postnatal day 10. CF distribution matched that obtained in previous experiments from AN, CN, and CTX, reflecting the development of the cochlea. 5. Both monotonic and nonomonotonic spike count-versus-intensity functions were found in the youngest kittens. There was a tendency for monotonic functions from the youngest kittens to be steeper than those from older kittens. No age-related changes in the shapes of non-monotonic functions were found. 6. Sensitivity to interaural intensity difference (IID), tested by holding the intensity to the excitatory ear at a suprathreshold level and increasing the intensity of the stimulus to the inhibitory ear, was exhibited as early as 8 days after birth. The majority of the cells exhibiting sensitivity to IID (89.5%) were classified as EI cells, and almost all IID sensitive cells had CFs between 3 and 25 kHz. Within our sample the shapes of IID functions, as well as the operating range of the IID functions, closely resembled those obtained from the adult cat. Thresholds of excitation and of inhibition were highly correlated, suggesting that the ipsilateral and contralateral inputs to the ICC develop as a matched set. 7. Sensitivity to interaural phase difference (IPD), tested either by shifting the onset phase of a CF tone to one ear relative to the other or by presenting tones of slightly different frequency to the two ears, was present as early as 12 days after birth.(ABSTRACT TRUNCATED AT 400 WORDS)     

Spatial tuning to sound-source azimuth in the inferior colliculus of unanesthetized rabbit

Despite decades of research devoted to the study of inferior colliculus (IC) neurons' tuning to sound-source azimuth, there remain many unanswered questions because no previous study has examined azimuth tuning over a full range of 360° azimuths at a wide range of stimulus levels in an unanesthetized preparation. Furthermore, a comparison of azimuth tuning to binaural and contralateral ear stimulation over ranges of full azimuths and widely varying stimulus levels has not previously been reported. To fill this void, we have conducted a study of azimuth tuning in the IC of the unanesthetized rabbit over a 300° range of azimuths at stimulus levels of 10-50 dB above neural threshold to both binaural and contralateral ear stimulation using virtual auditory space stimuli. This study provides systematic evidence for neural coding of azimuth. We found the following: 1) level-tolerant azimuth tuning was observed in the top 35% regarding vector strength and in the top 15% regarding vector angle of IC neurons; 2) preserved azimuth tuning to binaural stimulation at high stimulus levels was created as a consequence of binaural facilitation in the contralateral sound field and binaural suppression in the ipsilateral sound field; 3) the direction of azimuth tuning to binaural stimulation was primarily in the contralateral sound field, and its center shifted laterally toward -90° with increasing stimulus level; 4) at 10 dB, azimuth tuning to binaural and contralateral stimulation was similar, indicating that it was mediated by monaural mechanisms; and 5) at higher stimulus levels, azimuth tuning to contralateral ear stimulation was severely degraded. These findings form a foundation for understanding neural mechanisms of localizing sound-source azimuth.     

Neural correlates of the precedence effect in the inferior colliculus of behaving cats

Several auditory spatial illusions, collectively called the precedence effect (PE), occur when transient sounds are presented from two different spatial locations but separated in time by an interstimulus delay (ISD). For ISDs in the range of localization dominance (<10 ms), a single fused sound is typically located near the leading source location only, as if the location of the lagging source were suppressed. For longer ISDs, both the leading and lagging sources can be heard and localized, and the shortest ISD where this occurs is called the echo threshold. Previous physiological studies of the extracellular responses of single neurons in the inferior colliculus (IC) of anesthetized cats and unanesthetized rabbits with sounds known to elicit the PE have shown correlates of these phenomena though there were differences in the physiologically measured echo thresholds. Here we recorded in the IC of awake, behaving cats using stimuli that we have shown to evoke behavioral responses that are consistent with the precedence effect. For small ISDs, responses to the lag were reduced or eliminated consistent with psychophysical data showing that sound localization is based on the leading source. At longer ISDs, the responses to the lagging source recovered at ISDs comparable to psychophysically measured echo thresholds. Thus it appears that anesthesia, and not species differences, accounts for the discrepancies in the earlier studies.     

Neural responses to overlapping FM sounds in the inferior colliculus of echolocating bats

The big brown bat, Eptesicus fuscus, navigates and hunts prey with echolocation, a modality that uses the temporal and spectral differences between vocalizations and echoes from objects to build spatial images. Closely spaced surfaces ("glints") return overlapping echoes if two echoes return within the integration time of the cochlea ( approximately 300-400 micros). The overlap results in spectral interference that provides information about target structure or texture. Previous studies have shown that two acoustic events separated in time by less than approximately 500 micros evoke only a single response from neural elements in the auditory brain stem. How does the auditory system encode multiple echoes in time when only a single response is available? We presented paired FM stimuli with delay separations from 0 to 24 micros to big brown bats and recorded local field potentials (LFPs) and single-unit responses from the inferior colliculus (IC). These stimuli have one or two interference notches positioned in their spectrum as a function of two-glint separation. For the majority of single units, response counts decreased for two-glint separations when the resulting FM signal had a spectral notch positioned at the cell's best frequency (BF). The smallest two-glint separation that reliably evoked a decrease in spike count was 6 micros. In addition, first-spike latency increased for two-glint stimuli with notches positioned nearby BF. The N(4) potential of averaged LFPs showed a decrease in amplitude for two-glint separations that had a spectral notch near the BF of the recording site. Derived LFPs were computed by subtracting a common-mode signal from each LFP evoked by the two-glint FM stimuli. The derived LFP records show clear changes in both the amplitude and latency as a function of two-glint separation. These observations in relation with the single-unit data suggest that both response amplitude and latency can carry information about two-glint separation in the auditory system of E. fuscus.     

Neural sensitivity to periodicity in the inferior colliculus: evidence for the role of cochlear distortions

Responses of low characteristic-frequency (CF) neurons in the inferior colliculus were obtained to amplitude-modulated (AM) high-frequency tones in which the modulation rate was equal to the neuron's CF. Despite all spectral components lying outside the pure tone-evoked response areas, discharge rates were modulated by the AM signals. Introducing a low-frequency tone (CF - 1 Hz) to the same ear as the AM tones produced a 1-Hz beat in the neural response. Introducing a tone (CF - 1 Hz) to the opposite ear to the AM tone also produced a beat in the neural response, with the beat at the period of the interaural phase difference between the CF - 1 Hz tone in one ear, and the AM rate in the other ear. The monaural and interaural interactions of the AM signals with introduced pure tones suggest that AM tones generate combination tones, (inter-modulation distortion) on the basilar membrane. These interact with low-frequency tones presented to the same ear to produce monaural beats on the basilar membrane, modulating the responses of inferior colliculus (IC) neurons on the 1-Hz period of the monaural beats or interacting binaurally with neural input generated in response to stimulation of the opposite ear. The auditory midbrain appears to show a robust representation of cochlear distortions generated by amplitude-modulated sounds.