Effects of auditory stimulus context on the representation of frequency in the gerbil inferior colliculus.

Prior studies of dynamic conditioning have focused on modulation of binaural localization cues, revealing that the responses of inferior colliculus (IC) neurons to particular values of interaural phase and level disparities depend critically on the context in which they occur. Here we show that monaural frequency transitions, which do not simulate azimuthal motion, also condition the responses of IC neurons. We characterized single-unit responses to two frequency transition stimuli: a glide stimulus comprising two tones linked by a linear frequency sweep (origin-sweep-target) and a step stimulus consisting of one tone followed immediately by another (origin-target). Using sets of glide and step stimuli converging on a common target, we constructed conditioned response functions (RFs) depicting the variability in the response to an identical stimulus as a function of the preceding origin frequency. For nearly all cells, the response to the target depended on the origin frequency, even for origins outside the excitatory frequency response area of the cell. Results from conditioned RFs based on long (2-4 s) and short (200 ms) duration step stimuli indicate that conditioning effects can be induced in the absence of the dynamic sweep, and by stimuli of relatively short duration. Because IC neurons are tuned to frequency, changes in the origin frequency often change the "effective" stimulus duty cycle. In many cases, the enhancement of the target response appeared related to the decrease in the "effective" stimulus duty cycle rather than to the prior presentation of a particular origin frequency. Although this implies that nonselective adaptive mechanisms are responsible for conditioned responses, slightly more than half of IC neurons in each paradigm responded significantly differently to targets following origins that elicited statistically indistinguishable responses. The prevailing influence of stimulus context when discharge history is controlled demonstrates that not all the mechanisms governing conditioning depend on the discharge history of the recorded neuron. Selective adaptation among the neuron's variously tuned afferents may help engender stimulus-specific conditioning. The demonstration that conditioning effects reflect sensitivity to spectral as well as spatial stimulus contrast has broad implications for the processing of a wide range of dynamic acoustic signals and sound sequences.

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.

Conditioned enhancement and suppression in the developing auditory midbrain.

Neural responses in the adult central auditory system to binaural stimuli can be altered by preceding acoustic events, including auditory motion. To determine whether the juvenile auditory system also exhibits this feature, we have examined interaural level difference (ILD) processing in the developing gerbil. A long binaural stimulus was followed without interruption by modulation of the level difference (virtual acoustic motion), which in turn was followed smoothly by a new steady state ILD. Auditory responses of single neurons in the inferior colliculus (IC) were assessed for sensitivity to the final steady state ILD. The response of EI neurons (excited by contralateral stimulation and inhibited ipsilaterally) was examined at postnatal (P) days 17-18, P24-25, and in adult animals. In adult animals, a sudden reduction of the inhibitory stimulus level resulted in a long-lasting (median = 4.3 s) enhanced discharge rate (conditioned enhancement). In P17-18 animals, conditioned enhancement only lasted for 1.2 s. When the inhibitory stimulus level was suddenly increased, adult neurons often displayed a conditioned suppression of discharge rate (median = 4.5 s), whereas P17-18 neurons remained suppressed for a much briefer period (median = 1.2 s). Moreover, the difference between conditioned responses and control discharge rates was three-four times greater in adult neurons compared to those recorded in P17-25 animals. Because conditioned responses are sensitive to the relative balance of contralateral excitation and ipsilateral inhibition, we examined the relationship between excitatory and inhibitory thresholds. In adult animals, excitatory thresholds were an average of 12 dB lower than inhibitory thresholds, while at P17-25 excitatory and inhibitory thresholds were roughly the same. These results indicate that computational properties of juvenile and adult IC neurons differ quantitatively, and this may reflect an imbalance between excitation and inhibition. The developmental differences described herein may limit the ability of young animals to locate a sound source with the latency and accuracy of an adult.

Transformation of binaural response properties in the ascending auditory pathway: influence of time-varying interaural phase disparity.

Transformation of binaural response properties in the ascending auditory pathway: influence of time-varying interaural phase disparity. J. Neurophysiol. 80: 3062-3076, 1998. Previous studies demonstrated that tuning of inferior colliculus (IC) neurons to interaural phase disparity (IPD) is often profoundly influenced by temporal variation of IPD, which simulates the binaural cue produced by a moving sound source. To determine whether sensitivity to simulated motion arises in IC or at an earlier stage of binaural processing we compared responses in IC with those of two major IPD-sensitive neuronal classes in the superior olivary complex (SOC), neurons whose discharges were phase locked (PL) to tonal stimuli and those that were nonphase locked (NPL). Time-varying IPD stimuli consisted of binaural beats, generated by presenting tones of slightly different frequencies to the two ears, and interaural phase modulation (IPM), generated by presenting a pure tone to one ear and a phase modulated tone to the other. IC neurons and NPL-SOC neurons were more sharply tuned to time-varying than to static IPD, whereas PL-SOC neurons were essentially uninfluenced by the mode of stimulus presentation. Preferred IPD was generally similar in responses to static and time-varying IPD for all unit populations. A few IC neurons were highly influenced by the direction and rate of simulated motion, but the major effect for most IC neurons and all SOC neurons was a linear shift of preferred IPD at high rates-attributable to response latency. Most IC and NPL-SOC neurons were strongly influenced by IPM stimuli simulating motion through restricted ranges of azimuth; simulated motion through partially overlapping azimuthal ranges elicited discharge profiles that were highly discontiguous, indicating that the response associated with a particular IPD is dependent on preceding portions of the stimulus. In contrast, PL-SOC responses tracked instantaneous IPD throughout the trajectory of simulated motion, resulting in highly contiguous discharge profiles for overlapping stimuli. This finding indicates that responses of PL-SOC units to time-varying IPD reflect only instantaneous IPD with no additional influence of dynamic stimulus attributes. Thus the neuronal representation of auditory spatial information undergoes a major transformation as interaural delay is initially processed in the SOC and subsequently reprocessed in IC. The finding that motion sensitivity in IC emerges from motion-insensitive input suggests that information about change of position is crucial to spatial processing at higher levels of the auditory system.

Role of synaptic inhibition in processing of dynamic binaural level stimuli.

We have recently discovered a paradoxical aftereffect associated with inhibition in the gerbil auditory midbrain. Single neurons in the inferior colliculus (IC) were assessed for sensitivity to a virtual motion stimulus produced by modulating the interaural level difference (ILD), a major cue for sound localization. The class of neuron studied was predominantly excited by contralateral stimulation and inhibited by ipsilateral stimulation. Sound pressure level was modulated trapezoidally at the ipsilateral "inhibitory" ear, whereas the contralateral "excitatory" level remained constant. When the inhibitory stimulus was decreased within a range of sound levels that maintained suppression under static conditions, an unexpected discharge was often elicited, apparently because of an aftereffect of synaptic inhibition. In contrast, when the inhibitory stimulus was increased within a range of sound levels that produced only modest suppression under static conditions, neuronal discharge was often profoundly suppressed. In many cases the "conditioned enhancement" or "conditioned suppression" persisted for several seconds after the modulation of ILD, and such conditioned responses were influenced by the modulation depth and rate. To test the effect of inhibition in the IC directly, glycine and GABA were pulsed from a glass recording pipette during a constant monaural excitatory stimulus. The acoustically elicited discharge rate was potentiated markedly if preceded immediately by the brief (0.5-10 sec) application of inhibitory transmitter. Collectively, these results revealed unusually long-lasting effects of inhibition that may establish a new range of acoustic cues to which the neuron responds best. This may have broad implications for processing ensuing auditory stimuli.

Stimulus-induced spike bursts in two fields of cat auditory cortex.

The sound-evoked responses of extracellularly recorded cat primary auditory cortical neurons usually consist of a single spike or a short-term burst of 2-4 spikes, irrespective of the nature of the acoustic signal. In the cat's auditory cortex, the properties of such responses have to date been described only for cells in the primary field (AI). The purpose of the present study was to describe the properties of stimulus-evoked spike-burst responses seen in neurons of the posterior auditory field (P) and to compare those properties with those of a sample of AI neurons studied under similar conditions. The data come from 80 field P and 31 AI neurons studied with tonal and noise-burst stimuli in barbiturate-anesthetized cats, using calibrated, sealed stimulus delivery systems and conventional extracellular recording techniques. The mean inter-spike intervals (ISI) seen in the transient burst responses of posterior field cells were typically short (2-5 ms) and, where it was possible to test them, independent of the rise time of tonal signals, suggesting that they were also independent of the onset spectrum of the stimulus. The mean ISIs were often independent of the stimulus amplitude, even though the signal level had profound effects on the number of spikes evoked and the latency and regularity with which the responses were initiated. Each neuron was assigned a 'characteristic ISI', i.e., the mean ISI seen in the most vigorous responses. The distribution of characteristic ISIs for AI and P neurons overlapped, but were significantly different, with the characteristic ISIs of field P neurons being longer. In both AI and P populations, characteristic ISI was significantly correlated with minimal first-spike latency. The slopes of the regression lines of characteristic ISI on minimal latency for AI and for P cells were not significantly different from each other. Since the minimal latencies of AI neurons were usually shorter than those of field P neurons, the shorter characteristic ISIs of AI cells may thus be interpreted as secondary to their shorter latent periods. The general properties of stimulus-evoked spike bursts seen in field P neurons were thus very similar those previously described for AI cells. These data are consistent with the view that the majority of extracellular recordings in the cat's auditory cortex come from pyramidal neurons and are appropriate as a specialization for transfer of information to nonpyramidal, inhibitory interneurons.

Monaural inhibition in cat auditory cortex.

1. Several studies of auditory cortex have examined the competitive inhibition that can occur when appropriate sounds are presented to each ear. However, most cortical neurons also show both excitation and inhibition in response to presentation of stimuli at one ear alone. The extent of such inhibition has not been described. Forward masking, in which a variable masking stimulus was followed by a fixed probe stimulus (within the excitatory response area), was used to examine the extent of monaural inhibition for neurons in primary auditory cortex of anesthetized cats (barbiturate or barbiturate-ketamine). Both the masking and probe stimuli were 50-ms tone pips presented to the contralateral ear. Most cortical neurons showed significant forward masking at delays beyond which masking effects in the auditory nerve are relatively small compared with those seen in cortical neurons. Analysis was primarily concerned with such components. Standard rate-level functions were also obtained and were examined for nonmonotonicity, an indication of level-dependent monaural inhibition. 2. Consistent with previous reports, a wide range of frequency tuning properties (excitatory response area shapes) was found in cortical neurons. This was matched by a wide range of forward-masking-derived inhibitory response areas. At the most basic level of analysis, these were classified according to the presence of lateral inhibition, i.e., where a probe tone at a neuron's characteristic frequency was masked by tones outside the limits of the excitatory response area. Lateral inhibition was a property of 38% of the sampled neurons. Such neurons represented 77% of those with nonmonotonic rate-level functions, indicating a strong correlation between the two indexes of monaural inhibition; however, the shapes of forward masking inhibitory response areas did not usually correspond with those required to account for the "tuning" of a neuron. In addition, it was found that level-dependent inhibition was not added to by forward masking inhibition. 3. Analysis of the discharges to individual stimulus pair presentations, under conditions of partial masking, revealed that discharges to the probe occurred independently of discharges to the preceding masker. This indicates that even when the masker is within a neuron's excitatory response area, forward masking is not a postdischarge habituation phenomenon. However, for most neurons the degree of masking summed over multiple stimulus presentations appears determined by the same stimulus parameters that determine the probability of response to the masker.(ABSTRACT TRUNCATED AT 400 WORDS)

Neurons sensitive to interaural phase disparity in gerbil superior olive: diverse monaural and temporal response properties.

1. We assessed mechanisms of binaural interaction underlying detection of interaural phase disparity (IPD) by recording single-unit responses in the superior olivary complex (SOC) of the anesthetized gerbil (Meriones unguiculatus). Binaural responses were obtained from 58 IPD-sensitive single units, 44 of which were histologically localized. Monaural responses were also obtained for 52 of 58 IPD-sensitive units. Additionally, responses were recorded from 16 units (best frequency < 2.4 kHz) in lateral SOC that were excited by ipsilateral stimulation and inhibited by contralateral stimulation (EI), none of which was IPD sensitive. Our results are consistent with a mechanism of binaural interaction involving detection of coincident excitatory inputs from the two ears. There was no compelling evidence of binaural sensitivity arising from IPD-dependent interactions of phase-locked excitatory and inhibitory inputs from the two ears. Despite the uniformity of binaural interactions, considerable diversity of temporal and monaural response properties was observed. 2. Monaural and binaural responses of 35 of 58 IPD-sensitive units were phase locked to the period of low-frequency (< 2.5 kHz) tones. Most phase-locking units were bilaterally excitable and, consistent with the coincidence-detection model, their IPD selectivity could be predicted from the difference between the mean phases of the monaural responses. The remaining units (23 of 58) did not phase lock in response to monaural or binaural tones. Most non-phase-locking units failed to respond to monaural stimulation of one or both ears (monaurally unresponsive units). 3. Some IPD-sensitive units were inhibited by monaural stimulation of the ipsilateral ear or both ears. A few units responded only at the onset of monaural and binaural tones. Phase locking was present in responses of some, but not all, of these monaurally inhibited and onset units. 4. Most IPD-sensitive neurons were encountered at sites within or immediately adjacent to the cell column of the medial superior olive (MSO). IPD-sensitive units were also recorded in the lateral superior olive (LSO), in the superior paraolivary nucleus (SPN), and within a region forming a medial-dorsal cap around MSO. Bilaterally excitable unites were concentrated around MSO, but were also encountered in SPN, the medial-dorsal region, and LSO. Some monaurally unresponsive units were recorded in the vicinity of the MSO, but most were located in the medial-dorsal region. Monaurally inhibited units were localized to the medial border of the MSO cell column or to SPN. Onset units were localized to SPN and the medial-dorsal region. EI units were located exclusively in LSO.(ABSTRACT TRUNCATED AT 400 WORDS)

Development of ventral cochlear nucleus projections to the superior olivary complex in gerbil.

The postnatal development of the projection from the ventral cochlear nucleus to the principal nuclei in the superior olivary complex in gerbil (Meriones unguiculatus) was studied in an age-graded series of pups ranging from 0 to 18 days old. Small crystals of 1,1'-dioctadecyl-3,3,3',3'-tetramethylindocarbocyanine perchlorate (DiI) were inserted into the ventral cochlear nucleus of aldehyde-fixed brains, and the labeled projections were examined with epifluorescence microscopy. Selected sections were photooxidized in a solution of diaminobenzidine and subsequently processed for electron microscopy to examine the development of labeled synapses in the target nuclei. Horseradish peroxidase was injected into the ventral cochlear nucleus of adult gerbils to assess the form and persistence of projections observed in the neonatal animals. In addition, electrophysiological responses to acoustic stimuli of single units in the adult auditory brainstem were analyzed to confirm the functionality of the novel projection from the ventral cochlear nucleus to the contralateral lateral superior olive. By the day of birth (P0), developing axons from the ventral cochlear nucleus have already established highly ordered pathways to the three primary nuclei of the superior olivary complex: the ipsilateral lateral superior olive, the contralateral medial nucleus of the trapezoid body, and at the lateral and medial dendrites of the ipsilateral and contralateral medial superior olive, respectively. Developing axons from the ventral cochlear nucleus that innervated the contralateral medial nucleus of the trapezoid body lacked the terminal morphology characteristic of the calyx of Held, but began to adopt a more characteristic form on P5. The mature calyx appeared around P14-16. Exuberant developmental projections to topographically inappropriate areas of the superior olivary complex were not observed at the postnatal ages studied. In addition to the projections of the ventral cochlear nucleus to the superior olivary complex described in other species, we observed the development and maintenance of a major direct projection from the ventral cochlear nucleus to the contralateral lateral superior olive. On P0, ventral cochlear nucleus axons decussate in the dorsal trapezoid body, form a plexus at the dorsal edge of the contralateral medial superior olive, and enter the ventrolateral limb of the contralateral lateral superior olive. Over the next 2 weeks, fascicles of fibers form on the hilar and ventral aspects of the ventrolateral limb. Fibers arising from these fascicles form converging, but nonoverlapping, arborizations within the ventrolateral limb at right angles to the curvature of the nucleus. The medial region was devoid of labeled axons.(ABSTRACT TRUNCATED AT 400 WORDS)

Development of ectopic projections from the ventral cochlear nucleus to the superior olivary complex induced by neonatal ablation of the contralateral cochlea.

The ability of an animal to localize a sound in space requires the precise innervation of the superior olivary complex by the ventral cochlear nuclei on each side of the lower brainstem. This precise pattern of innervation could require an immutable recognition of appropriate targets by afferent processes arising from these nuclei. This possibility was investigated by destroying one cochlea of gerbil pups (Meriones unguiculatus) on the second postnatal day and assessing the projections from the ventral cochlear nucleus (VCN) on the unablated side to the superior olivary complex during the subsequent 2 weeks and after the animals had reached maturity. A crystal of 1,1'-dioctadecyl-3,3,3',3'-tetramethylindocarbocyanine perchlorate (DiI) was inserted into VCN on the unablated side in animals ranging in age from 3 to 14 days. To assess the permanence of any altered pattern of innervation, horseradish peroxidase was injected into VCN on the unablated side in adult, neonatally ablated animals. Finally, electrophysiological responses to acoustic stimuli delivered to the ear on the unablated side were recorded in the superior olivary complex of adult animals to assess whether altered innervation patterns were functional. Normative data were derived from our accompanying study of the development of VCN projections to the superior olivary complex in normal gerbils (Kil et al., this issue). Whereas VCN normally projects to the lateral aspect of the ipsilateral medial superior olive and to the medial aspect of the contralateral medial superior olive in control animals, in experimental animals VCN on the unablated side projects to both sides of these nuclei. Whereas in the gerbil, VCN normally projects only to the hilar area and to the ventrolateral limb of the contralateral lateral superior olive, in experimental animals VCN on the unablated side projects throughout this nucleus. This induced projection is specific in that the efferents to each limb of the contralateral nucleus are linked to the normal projection to the homotopic region of the ipsilateral nucleus. Whereas VCN innervates the contralateral medial nucleus of the trapezoid body in control animals, in experimental animals VCN on the unablated side provides calyces of Held in the ipsilateral nucleus as well. The induced projections to these three major subnuclei of the superior olivary complex first appear within 24 hours of the cochlear ablation and continue to develop over at least the subsequent 11 days. Thus, prior to the day when the cochlea becomes functional, VCN has established specific ectopic projections to loci normally innervated by VCN on the ablated side.(ABSTRACT TRUNCATED AT 400 WORDS)

Factors shaping the tone level sensitivity of single neurons in posterior field of cat auditory cortex.

1. The posterior field (field P) of the cat's auditory cortex contains a higher proportion of neurons whose response/level functions for characteristic frequency (CF) tones are nonmonotonic than does the primary field (AI). The general purpose of the present study is to assess whether the response/level functions of field P neurons are generated by the same mechanisms as those of cells in AI. All of the data came from single neurons in the cortices of barbiturate-anesthetized cats, to which we presented tonal stimuli through sealed, calibrated stimulating systems. 2. We obtained quantitative data from 123 neurons, of which 108 were located in field P. Of the 108 field P cells, 70% had nonmonotonic response/level functions for 5-ms rise time tones of CF. For cells of any given CF, both CF thresholds and best SPLs (i.e., SPLs associated with maximal responses) varied widely. A correlation analysis revealed that a linear relation between best SPL and CF threshold accounted for 73% of the data variance in the association between those response variables. An analysis of data from 83 nonmonotonic cells in AI revealed a similar relation. 3. Field P neurons whose response/level functions were non-monotonic for 5-ms rise time CF tones became even more narrowly tuned to SPL when the rise time of the tone bursts was reduced to 1 ms. Lengthening the rise time to 20 ms reduced or eliminated the SPL tuning in almost all of these neurons. The general form of monotonic tone response/level functions was commonly unaffected by variation in signal rise time. In a few instances, cells with monotonic response/level functions for 5- and 20-ms rise time tones developed nonmonotonic functions for 1-ms rise time tones. 4. Field P neurons with nonmonotonic response/level functions for CF tones usually failed to respond to wideband noise pulses, or, less commonly, responded to noise only at low SPLs. In contrast, field P cells with a monotonic response to CF tones usually responded monotonically to noise. 5. The minimal mean first-spike latencies of field P neurons were generally longer than those of AI cells studied under similar conditions. The precision of first-spike timing, measured using the SD of the mean first-spike latency, was commonly poorer than that of AI cells. 6. The properties of field P cells followed the same rules as those seen in AI.(ABSTRACT TRUNCATED AT 400 WORDS)

Level-dependent representation of stimulus frequency in cat primary auditory cortex.

The tonotopicity of the cat's primary auditory cortex (AI) is thought to provide the framework for frequency-specific processing in that field. This study was designed to assess this postulate by examining the spatial distribution of neurons within AI that are activated by a single tonal frequency delivered to the contralateral ear. Distributions obtained at each of several stimulus levels were then compared to assess the influence of stimulus amplitude on the spatial representation of a given stimulus frequency in AI. Data were obtained from 308 single units in AI of four adult, barbiturate-anesthetized cats, using extracellular recording methods. Stimuli were 40-ms tone pulses presented through calibrated, sealed stimulating systems. In each animal, the CF (stimulus frequency to which the unit is most sensitive), threshold at CF, response/level function at CF, and binaural interactions were determined for isolated neurons (usually one per track) in 60-90 electrode tracks. For each unit, regardless of its CF, responses to 40 repetitions of contralateral tones of a single frequency, presented at each of four or five sound pressure levels (SPLs) in the range from 10 to 80 dB were obtained. Different test frequencies were used in each of four cats (1.6, 8.0, 11.0, and 16.0 kHz). For tones of each SPL, we generated maps of the response rates across the cortical surface. These maps were then superimposed on the more traditional maps of threshold CF. All units whose CF was equal to the test frequency could be driven at some SPL, given an appropriate monaural or binaural configuration of the stimulus. There was a clear spatial segregation of neurons according to the shapes of their CF tone response/level functions. Patches of cortex, often occupying more than 2 mm2, seemed to contain only monotonic or only nonmonotonic units. In three cortices, a patch of nonmonotonic cells was bounded ventrally by a patch of monotonic cells, and in one of these cases, a second patch of monotonic cells was found dorsal to the nonmonotonic patch. Contralateral tones of any given SPL evoked excitatory responses in discontinuous cortical territories. At low SPLs (10, 20 dB), small foci of activity occurred along the isofrequency line representing the test frequency. Many of these cells had nonmonotonic response/level functions. (ABSTRACT TRUNCATED AT 400 WORDS)

Responses of inferior colliculus neurons to time-varying interaural phase disparity: effects of shifting the locus of virtual motion.

1. Motion of sound sources results in temporal variation of the binaural cues for sound localization. We evaluated the influence of virtual motion on neural tuning to one of these cues, interaural phase disparity (IPD). Responses to dichotic stimuli were recorded from single units in the inferior colliculus of the anesthetized cat and gerbil (Meriones unguiculatus). Static IPDs were generated by presenting dichotic tone pairs with a constant phase offset maintained for the duration of the stimulus. Time-varying IPDs were generated by simultaneously presenting a pure tone to one ear and a phase-modulated tone to the other ear. Sets of time-varying stimuli consisted of modulations through partially overlapping ranges of IPD, corresponding to movement of a sound source through partially overlapping arcs in the horizontal plane. 2. In agreement with previous results, neuronal discharge was typically a peaked function of static IPD resulting from both binaural facilitation at favorable IPDs and binaural suppression at unfavorable IPDs. Responses to time-varying IPD stimuli appeared to be shaped by the same facilitative and inhibitory mechanisms that underlie static IPD tuning. Modulation toward the peak of binaural facilitation increased the probability of discharge, and modulation toward the peak of binaural suppression decreased the probability of discharge. However, it was also clear that IPD tuning could be significantly altered by the temporal context of the stimulus. For the vast majority of units in response to modulation through partially overlapping ranges of IPD the discharge rate profiles were generally nonoverlapping. This shift in IPD tuning induced by the virtual motion reflects the fact that the binaural interaction associated with a given IPD depends on the recent history of stimulation. In addition, modulation in opposite directions through the same range of IPDs often elicited asymmetric responses. These nonlinearities imply that most inferior colliculus neurons do not unambiguously encode a specific IPD, but instead may encode small changes of IPD occurring virtually anywhere within their receptive fields. In a few cases modulation through overlapping ranges of IPD elicited contiguous response profiles, indicating that for these units responses were determined entirely by instantaneous IPD. 3. The nonlinearity of responses to time-varying IPD stimuli could not be attributed to monaural entrainment to the phase-modulated signals, did not depend on the phase modulation waveform, and occurred irrespective of which ear received the phase-modulated signal. Responses were similar in cats and gerbils, suggesting that the underlying mechanisms are common to binaural processing in diverse mammalian species.(ABSTRACT TRUNCATED AT 400 WORDS)

Binaural processing of sound pressure level in cat primary auditory cortex: evidence for a representation based on absolute levels rather than interaural level differences.

1. Single-neuron responses were recorded in high-frequency regions of primary auditory cortex (AI) of anesthetized cats. Best-frequency tone pips were presented to each ear independently via sealed stimulus delivery systems, and the sound pressure level (SPL) at each ear was independently manipulated. Each neuron was studied with many dichotic combinations of SPL, chosen to incorporate a broad range of the two synthetic interaural level variables, interaural level difference (ILD) and average binaural level (ABL). This paper illustrates the common forms of binaural SPL selectivity observed in a sample of 204 single neurons located in AI. 2. Most neurons (> 90%) were jointly influenced by ILD and ABL. A small proportion of bilaterally excitable (EE) neurons responded to ABL rather independently of ILD. Only one neuron was determined to respond to ILD independently of ABL. 3. Nonmonotonic selectivity for one or both of the binaural level cues was evident in > 60% of our sample. Within the most effective range of ILD values, response strength was usually related nonmonotonically to related both to ILD and ABL. We have described units exhibiting this kind of dual nonmonotonic selectivity for the two binaural variables as being influenced by a Two-Way Intensity Network (TWIN). 4. Each of the response forms identified in an earlier study of the gerbil inferior colliculus were found in this study of cat auditory cortex. However the classes were evident in markedly different proportions. In particular, TWIN responses alone accounted for 36.2% of the sample, nearly four times the proportion found in the inferior colliculus in a previous study. 5. Units with similar binaural responses do not necessarily have similar monaural properties. For example, the typically nonmonotonic relation between response strength and ABL was often observed in the absence of a monaurally demonstrable nonmonotonicity. There is no simple relation between a neuron's classification according to the sign of monaural influence and its response to ILD and ABL. In particular, EE neurons exhibited remarkably diverse binaural properties. 6. Since responses of nearly all AI neurons are influenced jointly by ABL and ILD, we contend that single neurons in primary auditory cortex are not specifically tuned to either cue. ILD and ABL are mathematical expressions relating the SPLs at the two ears to each other (as the difference and average, respectively) and any such combination is expressed most simply as a particular combination of SPL at each ear.(ABSTRACT TRUNCATED AT 400 WORDS)

Focal selectivity for binaural sound pressure level in cat primary auditory cortex: two-way intensity network tuning.

1. The influence of sound pressure level (SPL) at the two ears was studied in single-neuron responses recorded in high-frequency regions of primary auditory cortex (AI) of anesthetized cats. For each unit, many binaural combinations of SPL were tested by using best-frequency tone pips presented to each ear independently via sealed stimulus delivery systems. In the preceding paper, we illustrated the different forms of response observed in our sample of units. Here we explore in more detail the mechanisms underlying the properties of the largest single class of binaural response, characterized by joint nonmonotonic tuning to the SPLs at the two ears. We have described such units as being influenced by a Two-Way Intensity Network (TWIN). 2. Under binaural conditions, 62% of our sample of well documented neurons (81/130) exhibited a nonmonotonic relation between response magnitude and the SPL at one or the other ear. Of these units, 47 displayed clear bilateral nonmonotonicity (TWIN tuning), 17 units displayed only unilateral nonmonotonicity, and an additional 17 units showed intermediate (or transitional) characteristics between unilateral and bilateral nonmonotonicity. These characteristics can also be described in terms of average binaural level (ABL) and interaural level difference (ILD). Thus there is commonly a nonmonotonic relation between response magnitude and ABL and sometimes a TWIN tuning to ABL and ILD. The distribution of best frequencies for TWIN neurons is broad. 3. Under monaural conditions, TWIN neurons exhibit diverse properties. Some are responsive only under binaural conditions [i.e., predominantly binaural (PB)]. Some monaurally responsive TWINs are contralaterally excitable and ipsilaterally unresponsive (EO), some are ipsilaterally excitable and contralaterally unresponsive (OE), and a few are bilaterally excitable (EE). Monaural rate/level functions are monotonic for some of these neurons and nonmonotonic for others. Neurons of the PB class have previously been found to have nonmonotonic selectivity for ILDs near zero. In this study we have found that virtually all PB neurons are also nonmonotonically selective for ABL with different PB neurons having different best ABLs. 4. For TWIN neurons that respond monaurally, it is possible to demonstrate a mixed binaural influence. The optimal stimulus (or best binaural combination) for a TWIN neuron is associated with binaural facilitation. Flanking the most effective combination of ABL and ILD are less effective combinations that generate lower response magnitudes, either through threshold effects (at low SPLs) or through binaural suppression (at higher SPLs).(ABSTRACT TRUNCATED AT 400 WORDS)

Interaural phase coding in auditory midbrain: influence of dynamic stimulus features.

A laterally located sound source stimulates the two ears at slightly different times, generating interaural phase disparities (IPDs) that are used for sound localization. Under natural conditions, such interaural cues are likely to be constantly changing, or dynamic. In the inferior colliculus of gerbils and cats, the nonlinearities in the coding of dynamic interaural phase cues are demonstrated. Responses to ecologically realistic phase cues are more reflective of the change of IPD than of the absolute IPDs over which that change occurs. This observation is inconsistent with the established view that directional information is coded in terms of absolute IPD.

Binaural processing of sound pressure level in the inferior colliculus.

The central auditory system could encode information about the location of a high-frequency sound source by comparing the sound pressure levels at the ears. Two potential computations are the interaural intensity difference (IID) and the average binaural intensity (ABI). In this study of the central nucleus of the inferior colliculus (ICC) of the anesthetized gerbil, we demonstrate that responses of 85% of the 97 single units in our sample were jointly influenced by IID and ABI. For a given ABI, discharge rate of most units is a sigmoidal function of IID, and peak rates occur at IIDs favoring the contralateral ear. Most commonly, successive increments of ABI cause successive shifts of the IID functions toward IIDs favoring the ipsilateral ear. Neurons displaying this behavior include many that would conventionally be classified EI (receiving predominantly excitatory input arising from one ear and inhibitory input from the other), many that would be classified EE (receiving predominantly excitatory input arising from each ear), and all that are responsive only to contralateral stimulation. The IID sensitivity of a very few EI neurons is unaffected by ABI, except near threshold. Such units could provide directional information that is independent of source intensity. A few EE neurons are very sensitive to ABI, but are minimally sensitive to IID. Nevertheless, our data indicate that responses of most EE units in ICC are strongly dominated by excitation of contralateral origin. For some units, discharge rate is nonmonotonically related to IID and is maximal when the stimuli at the two ears are of comparable sound pressure. This preference for zero IID is common for all binaural levels. Many EI neurons respond nonmonotonically to ABI. Discharge rates are greater for IIDs representative of contralateral space and are maximal at a single best ABI. For a subset of these neurons, the influence arising from the ipsilateral ear is comprised of a mixture of excitation and inhibition. As a consequence, discharge rates are nonmonotonically related not only to ABI but also to IID. This dual nonmonotonicity creates a clear focus of peak response at a particular ABI/IID combination. Because of their mixed monaural influences, such units would be ascribed to different classes of the conventional (EE/EI) binaural classification scheme depending on the binaural level presented. Several response classes were identified in this study, and each might contribute differently to the encoding of spatial information.(ABSTRACT TRUNCATED AT 400 WORDS)

Single-unit responses in the inferior colliculus: different consequences of contralateral and ipsilateral auditory stimulation.

Monaural excitatory responses of 181 single units in the central nucleus of the inferior colliculus of 15 anesthetized gerbils (Meriones unguiculatus) were examined quantitatively. Pure-tone stimuli were presented monaurally through sealed, calibrated sound-delivery systems. Most units were excited only by contralateral stimulation (EO); 23% were bilaterally excitable (EE). The threshold frequency tuning curves for contralateral stimulation of EE units were significantly broader than those produced by ipsilateral stimulation of EE units and those produced by contralateral stimulation of EO units. The frequency at which threshold was lowest (best frequency), or BF) was very similar for ipsilateral and contralateral stimulation of individual EE units; however, ipsilateral BFs were slightly but significantly lower than contralateral BFs. For EE units, ipsilateral BF thresholds (mean: 29.2 dB SPL) were significantly higher than contralateral BF thresholds (mean: 14.9 dB SPL). Monotonic and nonmonotonic relationships between discharge rate and stimulus intensity at BF were observed in responses evoked both by contralateral and ipsilateral stimulation. Interestingly, for individual EE units it was not uncommon for the rate/intensity function for one monaural condition to be monotonic although the relationship for stimulation of the other ear was markedly nonmonotonic. There was no qualitative difference between rate/intensity functions evoked by contralateral stimulation in EO and EE units. Ipsilateral discharge rates were characteristically much lower than contralateral rates for a given stimulus intensity. For 50 BF tones of 100 ms duration, the median peak numbers of discharges for contralateral stimulation of EO and EE units were 361 and 339, respectively; the median for ipsilateral stimulation of EE units was 102. The dynamic range of each rate/intensity function was calculated by measuring the intensity range associated with an increase in spike count from 10 to 90% of the peak rate. No differences were detected between the distributions of dynamic range for contralateral stimulation in EO or EE units, or between contralateral and ipsilateral dynamic ranges within individual EE units. For all response types the distributions of dynamic range were approximately normal, with means near 20 dB. The minimum mean latency to the first spike at BF was generally longer for ipsilateral than for contralateral responses.(ABSTRACT TRUNCATED AT 400 WORDS)

Single-unit responses in the inferior colliculus: effects of neonatal unilateral cochlear ablation.

Monaural responses of single units isolated in the inferior colliculus of adult gerbils that have developed postnatally with one cochlea were compared with monaural responses recorded in animals that have developed with both cochleas. One cochlea of 2-day-old gerbils was ablated, and at approximately 6 mo of age, excitatory responses to stimulation of the nonoperated ear were recorded in the ipsilateral inferior colliculus. These responses were compared quantitatively with responses evoked by ipsilateral and contralateral monaural stimulation in normal gerbils. Responses to ipsilateral stimulation in adult gerbils subjected at 2 days of age to ablation of the contralateral cochlea are significantly different from ipsilateral responses in nonoperated gerbils. In several respects they are very similar to contralateral responses in nonoperated gerbils. (Differences between monaural contralateral and ipsilateral responses in control animals are documented in the companion paper, Ref. 24.) These conclusions are based on analyses of response threshold, peak discharge rate, response pattern, and minimum response latency. The mean dynamic range of ipsilateral rate/intensity functions obtained in neonatally ablated gerbils is significantly larger than the mean ipsilateral and contralateral dynamic ranges in control animals. Analyses of threshold tuning curves indicate that the frequency tuning of units in the inferior colliculus of neonatally ablated animals does not differ significantly from the tuning of units in control animals in response to either ipsilateral or contralateral stimulation. These data reveal that in normal gerbils responses of single units in the inferior colliculus to stimulation of the ipsilateral ear result in part from interactions during postnatal development between pathways that convey information from the contralateral ear. The results are discussed in terms of the known anatomic consequences of a neonatal cochlear ablation and the competition for available synaptic space in the development of the retinotectal system.