Processing of interaural time and intensity differences in the cat inferior colliculus

Summary 1. Binaural neurones were recorded in the central nucleus of the cat inferior colliculus and were stimulated with tone and noise bursts. Closed field sound systems were used to produce independent interaural time (ITD) and intensity (IID) differences. Particular attention was paid to high frequency (above 2 kHz) cells. 2. Three main types of binaural neurone were found: High frequency excitatory-inhibitory neurones (EI cells), excited by input from the contralateral ear and inhibited by ipsilateral input, high frequency excitatory-excitatory cells (EE cells), excited by inputs from either ear and low frequency cells sensitive to interaural phase differences (IPD cells). 3. The EI cells had characteristics similar to those of IE cells in the contralateral lateral superior olive. They were sensitive to envelope ITDs (most cells) and IIDs (all cells) favouring the contralateral ear. The response of these cells increased with increasing contra lead ITDs or contra loud IIDs up to values well outside the physiological range. 4. Low frequency binaural cells were sensitive to interaural phase differences (IPDs). The peak response was often in the contralateral physiological range and the response was unaffected by IIDs. 5. Many high frequency EE cells were sensitive to envelope ITDs. These units were relatively unaffected by IID. Although the ITD sensitivity of these cells was generally less than that of the IPD cells, the peak response of the ITD curve was also often in the contralateral physiological range. 6. Some of the high frequency EI and EE cells were sensitive to ongoing time differences (OTDs) in white noise signals, i.e. they showed ITD response curves to carrier only shifted noise bursts. 7. The EI cells often showed recovery from inhibition at large ipsilateral lead. This tendency was increased as the sound pressure level on the inhibitory side was lowered and by the use of click stimuli. Similarly, cycles of suppression could be seen to follow excitation in some EE cells. The time course of these effects was in the order of hundreds of s. 8. Binaural characteristics (degree of ITD, IID or OTD sensitivity) showed considerable interunit variation within each cell type. These variations were also affected by signal type (tone or noise bursts) and did not appear to be correlated with best frequency, nature of the tuning curve or PSTH type. We suggest that the time course of the inhibitory and excitatory effects at each unit (and its interaction with the signal type) determines the type of ITD response and that this time course varies from cell to cell.     

Neural sensitivity to interaural envelope delays in the inferior colliculus of the guinea pig

Interaural time differences (ITDs) are important cues for mammalian sound localization. At high frequencies, sensitivity to ITDs, which are conveyed only by the envelope of the waveforms, has been shown to be poorer than sensitivity to ITDs at low frequencies, which are conveyed primarily by the fine structure of the waveforms. Recently, human psychophysical experiments have demonstrated that sensitivity to envelope-based ITDs in high-frequency transposed tones can be equivalent to low-frequency fine-structure-based ITD sensitivity. Transposed tones are designed to provide high-frequency auditory nerve fibers (ANFs) with similar temporal information to that provided by low-frequency tones. We investigated neural sensitivity to ITDs in high-frequency transposed and sinusoidally amplitude modulated (SAM) tones, in the inferior colliculus of the guinea pig. Neural sensitivity to ITDs in transposed tones was found to be greater than that to ITDs in SAM tones; in response to transposed tones, neural firing rates were more modulated as a function of ITD and discrimination thresholds were found to be lower than those in response to SAM tones. Similar to psychophysical findings, ITD discrimination of single neurons in response to transposed tones for rates of modulation <250 Hz was comparable to neural discrimination of ITDs in low-frequency tones. This suggests that the neural mechanisms that mediate sensitivity to ITDs at high and low frequencies are functionally equivalent, provided that the stimuli result in appropriate temporal patterns of action potentials in ANFs.     

Development of responses to acoustic interaural intensity differences in the cat inferior colliculus

Summary Responses of single neurones in the inferior colliculus of anaesthetized adult cats and kittens were studied using best-frequency stimuli of varying interaural intensity difference (IID). Two broad classes of neurone, distinguished by the predominant type of input from each ear, were examined. One class of cells received predominantly excitatory input from each ear (EE cells). The other class were excited by monaural stimulation of the contralateral ear and showed no response to monaural stimulation of the ipsilateral ear, but inhibition of the excitatory response by simultaneous ipsilateral stimulation (EI cells). Fourteen of the 18 adult EI cells showed marked changes in discharge rate with variation in IID. Adult EI cells showed low response variability and were insensitive to changes in average binaural intensity. In all cases of IID sensitivity, the onset component of the response was less sensitive to IID than the sustained component. Eight out of ten EE cells were insensitive to IID over the range tested. Cells of high best-frequency in kittens younger than 28 days showed irregular changes in discharge rate with variation in IID and wide response variability. Some low-frequency EI cells in young kittens showed sensitivity to IID, but it is unlikely that these could be involved in sound localization as their frequency response was inappropriate. Many cells in kittens aged 31–40 days showed monotonic, adult-like IID functions, but the response variability of these cells remained higher than that of adult cat neurones. These data provide evidence for a developmental change of binaural interaction in the cat.     

Responses of low-frequency cells in the inferior colliculus to interaural time differences of clicks: excitatory and inhibitory components

1. We studied extracellular responses of low-frequency cells in the central nucleus of the inferior colliculus (ICC) to interaural time differences (ITDs) of clicks and compared their responses to ITDs of noise and tones. Most cells that displayed sensitivity to ITDs of clicks responded cyclically as a function of ITD with central peaks and troughs at the same ITDs as in response to noise. The positions of these peaks and troughs also matched those predicted from tonal ITD curves. Thus over the range of physiologically relevant ITDs, the binaural cells in the ICC showed similar sensitivity to ITDs of tones, noise, and clicks. 2. The transient nature of the response to a click allowed association of individual discharges with either the ipsilateral or contralateral stimulus when the binaural stimulus included a large ITD. We studied the influence of the click presented to one side on responses to the click presented to the other side. By examining responses to clicks with large ITDs, ranging from 2 to 3 up to 200 ms, we could identify both excitatory and inhibitory components in response to binaural clicks. 3. For many cells, there was evidence for a short-lasting excitation arising from one or both inputs of the binaural stimulus. Inhibitory interactions could also be demonstrated over a large range of ITDs. Long-lasting, late inhibitory components arose from both contralateral and ipsilateral inputs. In 87% of cells that were driven by the contralateral input, a late inhibitory component originating from the ipsilateral side was detected. In all cells that were driven by the ipsilateral side, a late inhibitory contralateral component was detected. This late inhibition of the excitatory response to one side by a leading stimulus to the other side could be evoked even when the leading stimulus was not effective in evoking an excitatory response. 4. Some cells also exhibited an early inhibitory component that preceded the excitation. An early contralateral inhibition was detected in 44% of cells that were driven by the ipsilateral input, whereas an early ipsilateral component was detected in 17% of cells driven by the contralateral input. 5. We confirmed hypotheses about the laterality and time course of the inhibitory and excitatory components by introducing interaural level differences (ILDs) into the binaural clicks and thus varying the strengths of the different components. 6. Inhibitory components may play a role in shaping the sensitivity of individual cells to ITDs of stimuli other than clicks; they were also apparent in responses to noise.(ABSTRACT TRUNCATED AT 400 WORDS)     

Role of GABAergic inhibition in the coding of interaural time differences of low-frequency sounds in the inferior colliculus

A major cue for the localization of sound in space is the interaural time difference (ITD). We examined the role of inhibition in the shaping of ITD responses in the inferior colliculus (IC) by iontophoretically ejecting gamma-aminobutyric acid (GABA) antagonists and GABA itself using a multibarrel pipette. The GABA antagonists block inhibition, whereas the applied GABA provides a constant level of inhibition. The effects on ITD responses were evaluated before, during and after the application of the drugs. If GABA-mediated inhibition is involved in shaping ITD tuning in IC neurons, then applying additional amounts of this inhibitory transmitter should alter ITD tuning. Indeed, for almost all neurons tested, applying GABA reduced the firing rate and consequently sharpened ITD tuning. Conversely, blocking GABA-mediated inhibition increased the activity of IC neurons, often reduced the signal-to-noise ratio and often broadened ITD tuning. Blocking GABA could also alter the shape of the ITD function and shift its peak suggesting that the role of inhibition is multifaceted. These effects indicate that GABAergic inhibition at the level of the IC is important for ITD coding.     

Response of auditory units in the barn owl's inferior colliculus to continuously varying interaural phase differences.

1. We studied the response of single units in the central nucleus of the inferior colliculus (ICc) of the barn owl (Tyto alba) to continuously varying interaural phase differences (IPDs) and static IPDs. Interaural phase was varied in two ways: continuously, by delivering tones to each ear that varied by a few hertz (binaural beat, Fig. 1), and discretely, by delaying in fixed steps the phase of sound delivered to one ear relative to the other (static phase). Static presentations were repeated at several IPDs to characterize interaural phase sensitivity. 2. Units sensitive to IPDs responded to the binaural beat stimulus over a broad range of delta f(Fig. 4). We selected a 3-Hz delta f for most of our comparative measurements on the basis of constraints imposed by our stimulus generation system and because it allowed us to reduce the influence of responses to stimulus onset and offset (Fig. 3A). 3. Characteristic interaural time or phase sensitivity obtained by the use of the binaural beat stimulus were comparable with those obtained by the use of the static technique (Fig. 5; r2 = 0.93, Fig. 6). 4. The binaural beat stimulus facilitated the measurement of characteristic delay (CD) and characteristic phase (CP) of auditory units. We demonstrated that units in the owl's inferior colliculus (IC) include those that are maximally excited by specific IPDs (CP = 0 or 1.0) as well as those that are maximally suppressed by specific IPDs (CP = 0.5; Figs. 7 and 8). 5. The selectivity of units sensitive to IPD or interaural time difference (ITD) were weakly influenced by interaural intensity difference (IID).(ABSTRACT TRUNCATED AT 250 WORDS)     

Binaural interaction in high-frequency neurons in inferior colliculus of the cat: effects of variations in sound pressure level on sensitivity to interaural intensity differences

1. Development of models of the manner in which interaural intensity differences (IIDs), the major binaural cue for the azimuthal location of high-frequency sounds, are coded by populations of neurons requires knowledge of the extent to which the IID sensitivity of individual neurons is invariant with changes in sound pressure level (SPL) and other stimulus parameters. To examine this tissue, recordings were obtained from a large sample (n = 458) of neurons with characteristic frequency (CF) greater than 3 kHz in the central nucleus of the inferior colliculus (ICC) of anesthetized cats. The sensitivity to IIDs and the effects of changes in SPL on this sensitivity were examined in neurons receiving excitatory contralateral input and inhibitory or mixed inhibitory/facilitatory ipsilateral input (EI neurons). 2. The form of an EI neuron's IID sensitivity and the effects of changes in SPL on that sensitivity were found to be determined in part by the characteristics of the neuron's rate-intensity function for monaural contralateral stimulation, and detailed rate-intensity functions were therefore obtained for 91 neurons. Many ICC neurons have nonmonotonic rate-intensity functions, the proportion so classified depending on the criterion of nonmonotonicity employed. 3. IID sensitivity functions for CF tonal stimuli were obtained at one or more intensities for 90 neurons, using a method of generating IIDs that kept the average binaural intensity (ABI) of the stimuli at the two ears constant. In the standard ABI range in which a function was obtained for each unit, the majority of EI neurons (72%) had monotonic (sigmoidal) or near-monotonic IID sensitivity functions. The remainder had nonmonotonic (peaked) IID sensitivity functions, which were attributable either to mixed inhibitory and facilitatory ipsilateral influences or to the fact that the effects of ipsilateral stimulation were superimposed on nonmonotonic effects of changes in intensity at the excitatory ear. 4. IID sensitivity was examined at two or more ABIs (3-5 in most cases) for 40 neurons classified as having monotonic or near-monotonic functions in the standard ABI range and for 7 neurons classified as nonmonotonic. For a small proportion of neurons with monotonic IID sensitivity functions, the form of the function was relatively invariant with changes in ABI. In those monotonic neurons in which the form of the IID sensitivity function varied with changes in ABI, the most common type of variation was that the position of the sloping portion of the function shifted systematically in the direction of larger IIDs favoring the ipsilateral ear as ABI increased.(ABSTRACT TRUNCATED AT 400 WORDS)     

Effects of amplitude modulation on the coding of interaural time differences of low-frequency sounds in the inferior colliculus. I. Response properties

Most sounds in the natural environment are amplitude-modulated (AM). To determine if AM alters the neuronal sensitivity to interaural time differences (ITDs) in low-frequency sounds, we tested neuronal responses to a binaural beat stimulus with and without modulation. We recorded from single units in the inferior colliculus of the unanesthetized rabbit. We primarily used low frequency ( approximately 25 Hz) modulation that was identical at both ears. We found that modulation could enhance, suppress, or not affect the discharge rate. In extreme cases, a neuron that showed no response to the unmodulated binaural beat did so when modulation was added to both ears. At the other extreme, a neuron that showed sensitivity to the unmodulated binaural beat ceased firing with modulation. Modulation could also affect the frequency range of ITD sensitivity, best ITD, and ITD tuning width. Despite these changes in individual neurons, averaging across all neurons, the peak and width of the population ITD function remained unchanged. Because ITD-sensitive neurons also time-locked to the modulation frequency, the location and sound attributes are processed simultaneously by these neurons.     

Effects of amplitude modulation on the coding of interaural time differences of low-frequency sounds in the inferior colliculus. II. Neural mechanisms

In our companion paper, we reported on interaural time difference (ITD)-sensitive neurons that enhanced, suppressed, or did not change their response when identical AM was added to both ears. Here, we first examined physical factors such as the difference in the interaural correlation, spectrum, or energy between the modulated and unmodulated signals. These were insufficient to explain the observed enhancement and suppression. We then examined neural mechanisms by selectively modulating the signal to each ear, varying modulation depth, and adding background noise to the unmodulated signal. These experiments implicated excitatory and inhibitory monaural inputs to the inferior colliculus (IC). These monaural inputs are postulated to adapt to an unmodulated signal and adapt less to a modulated signal. Thus enhancement or suppression is created by the convergence of these excitatory or inhibitory inputs with the inputs from the binaural comparators. Under modulation, the role of the monaural input is to shift the threshold of the IC neuron. Consistent with this role, background noise mimicked the effect of modulation. Functionally, enhancement and suppression may serve in detecting the degree of modulation in a sound source while preserving ITD information.     

Responses of neurons in the inferior colliculus to dynamic interaural phase cues: evidence for a mechanism of binaural adaptation

Responses to sound stimuli that humans perceive as moving were obtained for 89 neurons in the inferior colliculus (IC) of urethan-anesthetized guinea pigs. Triangular and sinusoidal interaural phase modulation (IPM), which produced dynamically varying interaural phase disparities (IPDs), was used to present stimuli with different depths, directions, centers, and rates of apparent motion. Many neurons appeared sensitive to dynamic IPDs, with responses at any given IPD depending strongly on the IPDs the stimulus had just passed through. However, it was the temporal pattern of the response, rather than the motion cues in the IPM, that determined sensitivity to features such as motion depth, direction, and center locus. IPM restricted only to the center of the IPD responsive area, evoked lower discharge rates than when the stimulus either moved through the IPD responsive area from outside, or up and down its flanks. When the stimulus was moved through the response area first in one direction and then back in the other, and the same IPDs evoked different responses, the response to the motion away from the center of the IPD responsive area was always lower than the response to the motion toward the center. When the IPD was closer at which the direction of motion reversed was to the center, the response to the following motion was lower. In no case did we find any evidence for neurons that under all conditions preferred one direction of motion to the other. We conclude that responses of IC neurons to IPM stimuli depend not on the history of stimulation, per se, but on the history of their response to stimulation, irrespective of the specific motion cues that evoke those responses. These data are consistent with the involvement of an adaptation mechanism that resides at or above the level of binaural integration. We conclude that our data provide no evidence for specialized motion detection involving dynamic IPD cues in the auditory midbrain of the mammal.     

Direct innervation of identified tectothalamic neurons in the inferior colliculus by axons from the cochlear nucleus.

The present study sought to identify tectothalamic neurons in the rat inferior colliculus that receive their innervation directly from the cochlear nuclei and to identify the axons that provide the innervation. A direct projection would bypass the binaural interactions of the superior olivary complex and provide the quickest route to the neocortex. Axons, primarily from the dorsal cochlear nucleus, were labeled with anterograde transport of dextran and terminated in the central nucleus of the inferior colliculus in a laminar pattern. Most labeled axons were thin and simply branched. Other axons were thicker, gnarly, less frequently observed and probably originated from the ventral cochlear nucleus. None had concentrated endbulbs or a nest of endings. Both types of axons terminated primarily in the central nucleus and layer 3 of the external cortex. This pattern suggests that the combination of these subdivisions in the rat are equivalent to the central nucleus as defined in other species. Tectothalamic neurons in the inferior colliculus in the same animals were identified by retrograde transport from the medial geniculate body and intracellular injection of Lucifer Yellow. A number of different cell types act as tectothalamic neurons and receive contacts from cochlear nucleus axons. These include flat cells (disc-shaped), less-flat cells and stellate cells. Two innervation patterns were seen: a combination of axosomatic and axodendritic contacts, and predominantly axodendritic contacts. Both patterns were seen in the central nucleus, but axosomatic contacts were seen less often in the other subdivisions. This is the first study to show direct connections between cochlear nuclear axons and identified tectothalamic neurons. The layers of axons from cochlear nuclei may provide convergent inputs to neurons in the inferior colliculus rather than the heavy inputs from single axons typical of lower auditory nuclei. Excitatory synapses made by axons from the cochlear nuclei on tectothalamic neurons may provide a substrate for rapid transmission of monaural information to the medial geniculate body.     

Multipolar cells in the ventral cochlear nucleus project to the dorsal cochlear nucleus and the inferior colliculus

When retrograde markers are placed in the dorsal cochlear nucleus two classes of labeled cells are found in the ventral cochlear nucleus. These are multipolar cells and granule cells. The structure and distribution of labeled multipolar cells greatly resemble those seen following injection of retrograde markers into the contralateral inferior colliculus. When one retrograde marker is placed in the dorsal cochlear nucleus and another simultaneously placed into the contralateral inferior colliculus, large numbers of multipolar cells containing both markers are found in the ventral cochlear nucleus. These findings show that all or most cells in the ventral cochlear nucleus that project to the inferior colliculus also send collaterals to the ipsilateral dorsal cochlear nucleus.     

Temporal properties of chronic cochlear electrical stimulation determine temporal resolution of neurons in cat inferior colliculus

As cochlear implants have become increasingly successful in the rehabilitation of adults with profound hearing impairment, the number of pediatric implant subjects has increased. We have developed an animal model of congenital deafness and investigated the effect of electrical stimulus frequency on the temporal resolution of central neurons in the developing auditory system of deaf cats. Maximum following frequencies (Fmax) and response latencies of isolated single neurons to intracochlear electrical pulse trains (charge balanced, constant current biphasic pulses) were recorded in the contralateral inferior colliculus (IC) of two groups of neonatally deafened, barbiturate-anesthetized cats: animals chronically stimulated with low-frequency signals (< or = 80 Hz) and animals receiving chronic high-frequency stimulation (> or = 300 pps). The results were compared with data from unstimulated, acutely deafened and implanted adult cats with previously normal hearing (controls). Characteristic differences were seen between the temporal response properties of neurons in the external nucleus (ICX; approximately 16% of the recordings) and neurons in the central nucleus (ICC; approximately 81% of all recordings) of the IC: 1) in all three experimental groups, neurons in the ICX had significantly lower Fmax and longer response latencies than those in the ICC. 2) Chronic electrical stimulation in neonatally deafened cats altered the temporal resolution of neurons exclusively in the ICC but not in the ICX. The magnitude of this effect was dependent on the frequency of the chronic stimulation. Specifically, low-frequency signals (30 pps, 80 pps) maintained the temporal resolution of ICC neurons, whereas higher-frequency stimuli significantly improved temporal resolution of ICC neurons (i.e., higher Fmax and shorter response latencies) compared with neurons in control cats. Furthermore, Fmax and latencies to electrical stimuli were not correlated with the tonotopic gradient of the ICC, and changes in temporal resolution following chronic electrical stimulation occurred uniformly throughout the entire ICC. In all three experimental groups, increasing Fmax was correlated with shorter response latencies. The results indicate that the temporal features of the chronically applied electrical signals critically influence temporal processing of neurons in the cochleotopically organized ICC. We suggest that such plastic changes in temporal processing of central auditory neurons may contribute to the intersubject variability and gradual improvements in speech recognition performance observed in clinical studies of deaf children using cochlear implants.