Correlation of neural response properties with auditory thalamus subdivisions in the awake marmoset

As the information bottleneck of nearly all auditory input that reaches the cortex, the auditory thalamus serves as the basis for establishing auditory cortical processing streams. The functional organization of the primary and nonprimary subdivisions of the auditory thalamus is not well characterized, particularly in awake primates. We have recorded from neurons in the auditory thalamus of awake marmoset monkeys and tested their responses to tones, band-pass noise, and temporally modulated stimuli. We analyzed the spectral and temporal response properties of recorded neurons and correlated those properties with their locations in the auditory thalamus, thereby forming the basis for parallel output channels. Three medial geniculate body (MGB) subdivisions were identified and studied physiologically and anatomically, although other medial subdivisions were also identified anatomically. Neurons in the ventral subdivision (MGV) were sharply tuned for frequency, preferred narrowband stimuli, and were able to synchronize to rapid temporal modulations. Anterodorsal subdivision (MGAD) neurons appeared well suited for temporal processing, responding similarly to tone or noise stimuli but able to synchronize to the highest modulation frequencies and with the highest temporal precision among MGB subdivisions. Posterodorsal subdivision (MGPD) neurons differed substantially from the other two subdivisions, with many neurons preferring broadband stimuli and signaling changes in modulation frequency with nonsynchronized changes in firing rate. Most neurons in all subdivisions responded to increases in tone sound level with nonmonotonic changes in firing rate. MGV and MGAD neurons exhibited responses consistent with provision of thalamocortical input to core regions, whereas MGPD neurons were consistent with provision of input to belt regions.     

Coding of amplitude modulation in primary auditory cortex

Conflicting results have led to different views about how temporal modulation is encoded in primary auditory cortex (A1). Some studies find a substantial population of neurons that change firing rate without synchronizing to temporal modulation, whereas other studies fail to see these nonsynchronized neurons. As a result, the role and scope of synchronized temporal and nonsynchronized rate codes in AM processing in A1 remains unresolved. We recorded A1 neurons' responses in awake macaques to sinusoidal AM noise. We find most (37-78%) neurons synchronize to at least one modulation frequency (MF) without exhibiting nonsynchronized responses. However, we find both exclusively nonsynchronized neurons (7-29%) and "mixed-mode" neurons (13-40%) that synchronize to at least one MF and fire nonsynchronously to at least one other. We introduce new measures for modulation encoding and temporal synchrony that can improve the analysis of how neurons encode temporal modulation. These include comparing AM responses to the responses to unmodulated sounds, and a vector strength measure that is suitable for single-trial analysis. Our data support a transformation from a temporally based population code of AM to a rate-based code as information ascends the auditory pathway. The number of mixed-mode neurons found in A1 indicates this transformation is not yet complete, and A1 neurons may carry multiplexed temporal and rate codes.     

Temporal and rate representations of time-varying signals in the auditory cortex of awake primates

Because auditory cortical neurons have limited stimulus-synchronized responses, cortical representations of more rapidly occurring but still perceivable stimuli remain unclear. Here we show that there are two largely distinct populations of neurons in the auditory cortex of awake primates: one with stimulus-synchronized discharges that, with a temporal code, explicitly represented slowly occurring sound sequences and the other with non-stimulus-synchronized discharges that, with a rate code, implicitly represented rapidly occurring events. Furthermore, neurons of both populations displayed selectivity in their discharge rates to temporal features within a short time-window. Our results suggest that the combination of temporal and rate codes in the auditory cortex provides a possible neural basis for the wide perceptual range of temporal information.     

Neural representations of sinusoidal amplitude and frequency modulations in the primary auditory cortex of awake primates

We investigated neural coding of sinusoidally modulated tones (sAM and sFM) in the primary auditory cortex (A1) of awake marmoset monkeys, demonstrating that there are systematic cortical representations of embedded temporal features that are based on both average discharge rate and stimulus-synchronized discharge patterns. The rate-representation appears to be coded alongside the stimulus-synchronized discharges, such that the auditory cortex has access to both rate and temporal representations of the stimulus at high and low frequencies, respectively. Furthermore, we showed that individual auditory cortical neurons, as well as populations of neurons, have common features in their responses to both sAM and sFM stimuli. These results may explain the similarities in the perception of sAM and sFM stimuli as well as the different perceptual qualities effected by different modulation frequencies. The main findings include the following. 1) Responses of cortical neurons to sAM and sFM stimuli in awake marmosets were generally much stronger than responses to unmodulated tones. Some neurons responded to sAM or sFM stimuli but not to pure tones. 2) The discharge rate-based modulation transfer function typically had a band-pass shape and was centered at a preferred modulation frequency (rBMF). Population-averaged mean firing rate peaked at 16- to 32-Hz modulation frequency, indicating that the A1 was maximally excited by this frequency range of temporal modulations. 3) Only approximately 60% of recorded units showed statistically significant discharge synchrony to the modulation waveform of sAM or sFM stimuli. The discharge synchrony-based best modulation frequency (tBMF) was typically lower than the rBMF measured from the same neuron. The distribution of rBMF over the population of neurons was approximately one octave higher than the distribution of tBMF. 4) There was a high degree of similarity between cortical responses to sAM and sFM stimuli that was reflected in both discharge rate- or synchrony-based response measures. 5) Inhibition appeared to be a contributing factor in limiting responses at modulation frequencies above the rBMF of a neuron. And 6) neurons with shorter response latencies tended to have higher tBMF and maximum discharge synchrony frequency than those with longer response latencies. rBMF was not significantly correlated with the minimum response latency.     

Information content of auditory cortical responses to time-varying acoustic stimuli

The present study explores the issue of cortical coding by spike count and timing using statistical and information theoretic methods. We have shown in previous studies that neurons in the auditory cortex of awake primates have an abundance of sustained discharges that could represent time-varying signals by temporal discharge patterns or mean firing rates. In particular, we found that a subpopulation of neurons can encode rapidly occurring sounds, such as a click train, with discharges that are not synchronized to individual stimulus events, suggesting a temporal-to-rate transformation. We investigated whether there were stimulus-specific temporal patterns embedded in these seemingly random spike times. Furthermore, we quantitatively analyzed the precision of spike timing at stimulus onset and during ongoing acoustic stimulation. The main findings are the following. 1) Temporal and rate codes may operate at separate stimulus domains or encode the same stimulus domain in parallel via different neuronal populations. 2) Spike timing was crucial to encode stimulus periodicity in "synchronized" neurons. 3) "Nonsynchronized" neurons showed little stimulus-specific spike timing information in their responses to time-varying signals. Such responses therefore represent processed (instead of preserved) information in the auditory cortex. And 4) spike timing on the occurrence of acoustic events was more precise at the first event than at successive ones and more precise with sparsely distributed events (longer time intervals between events) than with densely packed events. These results indicate that auditory cortical neurons mark sparse acoustic events (or onsets) with precise spike timing and transform rapidly occurring acoustic events into firing rate-based representations.     

Frequency organization and responses to complex sounds in the medial geniculate body of the mustached bat

The auditory cortex of the mustached bat (Pteronotus parnellii) displays some of the most highly developed physiological and organizational features described in mammalian auditory cortex. This study examines response properties and organization in the medial geniculate body (MGB) that may contribute to these features of auditory cortex. About 25% of 427 auditory responses had simple frequency tuning with single excitatory tuning curves. The remainder displayed more complex frequency tuning using two-tone or noise stimuli. Most of these were combination-sensitive, responsive to combinations of different frequency bands within sonar or social vocalizations. They included FM-FM neurons, responsive to different harmonic elements of the frequency modulated (FM) sweep in the sonar signal, and H1-CF neurons, responsive to combinations of the bat's first sonar harmonic (H1) and a higher harmonic of the constant frequency (CF) sonar signal. Most combination-sensitive neurons (86%) showed facilitatory interactions. Neurons tuned to frequencies outside the biosonar range also displayed combination-sensitive responses, perhaps related to analyses of social vocalizations. Complex spectral responses were distributed throughout dorsal and ventral divisions of the MGB, forming a major feature of this bat's analysis of complex sounds. The auditory sector of the thalamic reticular nucleus also was dominated by complex spectral responses to sounds. The ventral division was organized tonotopically, based on best frequencies of singly tuned neurons and higher best frequencies of combination-sensitive neurons. Best frequencies were lowest ventrolaterally, increasing dorsally and then ventromedially. However, representations of frequencies associated with higher harmonics of the FM sonar signal were reduced greatly. Frequency organization in the dorsal division was not tonotopic; within the middle one-third of MGB, combination-sensitive responses to second and third harmonic CF sonar signals (60-63 and 90-94 kHz) occurred in adjacent regions. In the rostral one-third, combination-sensitive responses to second, third, and fourth harmonic FM frequency bands predominated. These FM-FM neurons, thought to be selective for delay between an emitted pulse and echo, showed some organization of delay selectivity. The organization of frequency sensitivity in the MGB suggests a major rewiring of the output of the central nucleus of the inferior colliculus, by which collicular neurons tuned to the bat's FM sonar signals mostly project to the dorsal, not the ventral, division. Because physiological differences between collicular and MGB neurons are minor, a major role of the tecto-thalamic projection in the mustached bat may be the reorganization of responses to provide for cortical representations of sonar target features.     

Click train encoding in primary and non-primary auditory cortex of anesthetized macaque monkeys

We studied encoding of temporally modulated sounds in 28 multiunits in the primary auditory cortical field (AI) and in 35 multiunits in the secondary auditory cortical field (caudomedial auditory cortical field, CM) by presenting periodic click trains with click rates between 1 and 300 Hz lasting for 2-4 s. We found that all multiunits increased or decreased their firing rate during the steady state portion of the click train and that all except two multiunits synchronized their firing to individual clicks in the train. Rate increases and synchronized responses were most prevalent and strongest at low click rates, as expressed by best modulation frequency, limiting frequency, percentage of responsive multiunits, and average rate response and vector strength. Synchronized responses occurred up to 100 Hz; rate response occurred up to 300 Hz. Both auditory fields responded similarly to low click rates but differed at click rates above approximately 12 Hz at which more multiunits in AI than in CM exhibited synchronized responses and increased rate responses and more multiunits in CM exhibited decreased rate responses. These findings suggest that the auditory cortex of macaque monkeys encodes temporally modulated sounds similar to the auditory cortex of other mammals. Together with other observations presented in this and other reports, our findings also suggest that AI and CM have largely overlapping sensitivities for acoustic stimulus features but encode these features differently.     

Neural coding of temporal information in auditory thalamus and cortex

How the brain processes temporal information embedded in sounds is a core question in auditory research. This article synthesizes recent studies from our laboratory regarding neural representations of time-varying signals in auditory cortex and thalamus in awake marmoset monkeys. Findings from these studies show that 1) the primary auditory cortex (A1) uses a temporal representation to encode slowly varying acoustic signals and a firing rate-based representation to encode rapidly changing acoustic signals, 2) the dual temporal-rate representations in A1 represent a progressive transformation from the auditory thalamus, 3) firing rate-based representations in the form of monotonic rate-code are also found to encode slow temporal repetitions in the range of acoustic flutter in A1 and more prevalently in the cortical fields rostral to A1 in the core region of marmoset auditory cortex, suggesting further temporal-to-rate transformations in higher cortical areas. These findings indicate that the auditory cortex forms internal representations of temporal characteristics of sounds that are no longer faithful replicas of their acoustic structures. We suggest that such transformations are necessary for the auditory cortex to perform a wide range of functions including sound segmentation, object processing and multi-sensory integration.     

Corticofugal modulation on both ON and OFF responses in the nonlemniscal auditory thalamus of the guinea pig

Corticofugal modulation on both ON and OFF responses in various nuclei in the medial geniculate body (MGB) was examined by locally activating the auditory cortex and looking for effects on the neuronal responses to acoustic stimuli. In contrast with a major corticofugal facilitatory effect on the ON neurons in the lemniscal nucleus of the MGB of the guinea pigs, of 132 ON neurons tested in three conditions with cortical activation through each of three implanted electrodes, the majority of the tested conditions (319/396) that were sampled from the nonlemniscal nuclei of the MGB received inhibitory modulation from the activated cortex. This inhibitory effect was >50% for 99 cases while the auditory cortex was activated. Most of the OFF and ON-OFF MGB neurons (44/54) showed a facilitatory effect of 111.4 +/- 99.9%, and three showed a small inhibitory effect of 25.7 +/- 5.8% on their OFF responses. Thirty neurons in the border region between the lemniscal and nonlemniscal MGB showed mainly facilitatory corticofugal effects on both ON and OFF responses. Meanwhile, cortical stimulation induced almost exclusive inhibitory effects on the ON response and facilitatory effects on the OFF response in the MGcm. It is suggested that the OFF response is produced as a disinhibition from the inhibitory input of the auditory stimulus. The present results provide a possible explanation for selective gating of the auditory information through the lemniscal MGB while switching off other unwanted sensory signals and the interference from the limbic system, leaving the other auditory cortex prepared to process only the auditory signal.     

Neural coding of temporal information in auditory thalamus and cortex

How the brain processes temporal information embedded in sounds is a core question in auditory research. This article synthesizes recent studies from our laboratory regarding neural representations of time-varying signals in auditory cortex and thalamus in awake marmoset monkeys. Findings from these studies show that 1) the primary auditory cortex (A1) uses a temporal representation to encode slowly varying acoustic signals and a firing rate–based representation to encode rapidly changing acoustic signals, 2) the dual temporal-rate representations in A1 represent a progressive transformation from the auditory thalamus, 3) firing rate–based representations in the form of a monotonic rate-code are also found to encode slow temporal repetitions in the range of acoustic flutter in A1 and more prevalently in the cortical fields rostral to A1 in the core region of marmoset auditory cortex, suggesting further temporal-to-rate transformations in higher cortical areas. These findings indicate that the auditory cortex forms internal representations of temporal characteristics of sounds that are no longer faithful replicas of their acoustic structures. We suggest that such transformations are necessary for the auditory cortex to perform a wide range of functions including sound segmentation, object processing and multi-sensory integration.     

Cells in the rat auditory system have sensory-delay correlates during the performance of an auditory working memory task

Single unit activity was recorded from rat auditory cortex (AC), medial geniculate body (MGB), and inferior colliculus (IC) during performance of a continuous nonmatching-to-sample task. The rats made go and no-go responses to indicate whether the current tone was the same as (match) or different from (nonmatch) the preceding tone. Between 31% and 55% of the units from AC, MGB, and IC showed sensory correlates (differences in activity to the two types of tones), indicating an involvement in sensory discrimination. Twenty percent of the units from AC and MGB had delay correlates (sustained differential activity during the delay immediately after the tones), indicating an involvement in retention. Most of the units with delay correlates also had sensory correlates. These results suggest that the auditory system, especially AC and MGB, discriminates and retains auditory stimuli in an auditory working memory.     

Frequency-modulation encoding in the primary auditory cortex of the awake owl monkey

Many communication sounds, such as New World monkey twitter calls, contain frequency-modulated (FM) sweeps. To determine how this prominent vocalization element is represented in the auditory cortex we examined neural responses to logarithmic FM sweep stimuli in the primary auditory cortex (AI) of two awake owl monkeys. Using an implanted array of microelectrodes we quantitatively characterized neuronal responses to FM sweeps and to random tone-pip stimuli. Tone-pip responses were used to construct spectrotemporal receptive fields (STRFs). Classification of FM sweep responses revealed few neurons with high direction and speed selectivity. Most neurons responded to sweeps in both directions and over a broad range of sweep speeds. Characteristic frequency estimates from FM responses were highly correlated with estimates from STRFs, although spectral receptive field bandwidth was consistently underestimated by FM stimuli. Predictions of FM direction selectivity and best speed from STRFs were significantly correlated with observed FM responses, although some systematic discrepancies existed. Last, the population distributions of FM responses in the awake owl monkey were similar to, although of longer temporal duration than, those in the anesthetized squirrel monkeys.     

Neural representations of temporally asymmetric stimuli in the auditory cortex of awake primates

The representation of rapid acoustic transients by the auditory cortex is a fundamental issue that is still unresolved. Auditory cortical neurons have been shown to be limited in their stimulus-synchronized responses, yet the perceptual performances of humans and animals in discriminating temporal variations in complex sounds are better than what existing neurophysiological data would predict. This study investigated the neural representation of temporally asymmetric stimuli in the primary auditory cortex of awake marmoset monkeys. The stimuli, ramped and damped sinusoids, were systematically manipulated (by means of half-life of the exponential envelope) within a cortical neuron's presumed temporal integration window. The main findings of this study are as follows: 1) temporal asymmetry in ramped and damped sinusoids with a short period (25 ms) was clearly reflected by average discharge rate but not necessarily by temporal discharge patterns of auditory cortical neurons. There was considerable response specificity to these stimuli such that some neurons were strongly responsive to a ramped sinusoid but almost completely unresponsive to its damped counterpart or vice versa. Of 181 neurons studied, 140 (77%) showed significant response asymmetry in at least one of the tested half-life values of the exponential envelope. Forty-six neurons showed significant response asymmetry over all half-lives tested. Sustained firing, commonly observed under awake conditions, contributed to greater response asymmetry than that of onset responses in many neurons. 2) A greater proportion of the neurons (32/46) that exhibited significant overall response asymmetry showed stronger responses to the ramped sinusoids than to the damped sinusoids, possibly contributing to the difference in the perceived loudness between these two classes of sounds. 3) The asymmetry preference of a neuron to ramped or damped sinusoids did not appear to be correlated with its characteristic frequency or minimum response latency, suggesting that this is a general phenomenon that exists across populations of cortical neurons. Moreover, the intensity of the stimuli did not have significant effects on the measure of the asymmetry preference based on discharge rate. 4) A population measure of response preference, based on discharge rate, of cortical neurons to the temporally asymmetric stimuli was qualitatively similar to the performance of human listeners in discriminating ramped versus damped sinusoids at different half-life values. These findings suggest that rapid acoustic transients embedded in complex sounds can be represented by discharge rates of cortical neurons instead of or in the absence of stimulus-synchronized discharges.     

Distinct time scales in cortical discrimination of natural sounds in songbirds

Understanding how single cortical neurons discriminate between sensory stimuli is fundamental to providing a link between cortical neural responses and perception. The discrimination of sensory stimuli by cortical neurons has been intensively investigated in the visual and somatosensory systems. However, relatively little is known about discrimination of sounds by auditory cortical neurons. Auditory cortex plays a particularly important role in the discrimination of complex sounds, e.g., vocal communication sounds. The rich dynamic structure of such complex sounds on multiple time scales motivates two questions regarding cortical discrimination. How does discrimination depend on the temporal resolution of the cortical response? How does discrimination accuracy evolve over time? Here we investigate these questions in field L, the analogue of primary auditory cortex in zebra finches, analyzing temporal resolution and temporal integration in the discrimination of conspecific songs (songs of the bird's own species) for both anesthetized and awake subjects. We demonstrate the existence of distinct time scales for temporal resolution and temporal integration and explain how they arise from cortical neural responses to complex dynamic sounds.     

Anesthesia suppresses nonsynchronous responses to repetitive broadband stimuli

Although many aspects of sensory processing are qualitatively similar in awake and anesthetized subjects, important state-dependent differences are known to exist. To investigate the effects of anesthesia on temporal processing in rat auditory cortex, multi-unit neural responses to trains of broadband clicks were recorded prior to, 15 min following, and 5 h following the administration of a ketamine-based anesthetic. While responses to clicks in isolation were relatively stable between states, responses to subsequent clicks exhibited increases in latency, peak latency, response duration, and post-onset suppression under anesthesia. Ketamine anesthetic reduced the maximum rate at which multi-unit clusters entrained to repeated clicks. No multi-unit clusters entrained to stimulus presentation rates greater than 33 Hz under anesthesia, compared with 85% and 81% in the pre- and post-anesthetic condition, respectively. Anesthesia also induced oscillatory activity that was not present in awake subjects. Finally, ketamine anesthesia abolished all tonic excitatory and suppressive nonsynchronous responses to click trains. The results of this study suggest that ketamine-based anesthesia significantly alters neural coding of broadband click trains in auditory cortex.     

Multiple time scales of adaptation in the auditory system as revealed by human evoked potentials

Single neurons in the primary auditory cortex of the cat show faster adaptation time constants to short- than long-term stimulus history. This ability to encode the complex past auditory stimulation in multiple time scales would enable the auditory system to generate expectations of the incoming stimuli. Here, we tested whether large neural populations exhibit this ability as well, by recording human auditory evoked potentials (AEP) to pure tones in a sequence embedding short- and long-term aspects of stimulus history. Our results yielded dynamic amplitude modulations of the P2 AEP to stimulus repetition spanning from milliseconds to tens of seconds concurrently, as well as amplitude modulations of the mismatch negativity AEP to regularity violations. A simple linear model of expectancy accounting for both short- and long-term stimulus history described our results, paralleling the behavior of neurons in the primary auditory cortex.     

Sensitivity to temporal modulation rate and spectral bandwidth in the human auditory system: MEG evidence

Slow acoustic modulations below 20 Hz, of varying bandwidths, are dominant components of speech and many other natural sounds. The dynamic neural representations of these modulations are difficult to study through noninvasive neural-recording methods, however, because of the omnipresent background of slow neural oscillations throughout the brain. We recorded the auditory steady-state responses (aSSR) to slow amplitude modulations (AM) from 14 human subjects using magnetoencephalography. The responses to five AM rates (1.5, 3.5, 7.5, 15.5, and 31.5 Hz) and four types of carrier (pure tone and 1/3-, 2-, and 5-octave pink noise) were investigated. The phase-locked aSSR was detected reliably in all conditions. The response power generally decreases with increasing modulation rate, and the response latency is between 100 and 150 ms for all but the highest rates. Response properties depend only weakly on the bandwidth. Analysis of the complex-valued aSSR magnetic fields in the Fourier domain reveals several neural sources with different response phases. These neural sources of the aSSR, when approximated by a single equivalent current dipole (ECD), are distinct from and medial to the ECD location of the N1m response. These results demonstrate that the globally synchronized activity in the human auditory cortex is phase locked to slow temporal modulations below 30 Hz, and the neural sensitivity decreases with an increasing AM rate, with relative insensitivity to bandwidth.     

Environmental enrichment increases paired-pulse depression in rat auditory cortex

Temporal features are important for the identification of natural sounds. Earlier studies have shown that cortical processing of temporal information can be altered by long-term experience with modulated sounds. In a previous study, we observed that environmental enrichment dramatically increased the response of cortical neurons to single tone and noise burst stimuli in both awake and anesthetized rats. Here, we evaluate how enrichment influences temporal information processing in the auditory cortex. We recorded responses to repeated tones and noise bursts in awake rats using epidural evoked potentials and in anesthetized rats using microelectrodes. Enrichment increased the response of cortical neurons to stimuli presented at slow rates and decreased the response to stimuli presented at fast rates relative to controls. Our observation that enrichment substantially increased response strength and forward masking is consistent with earlier reports that long-term potentiation of cortical synapses is associated with increased paired-pulse depression. Enrichment also increased response synchronization at slow rates and decreased synchronization at fast rates. Paired-pulse depression increased within days of environmental enrichment and was restored to normal levels after return to standard housing conditions. These results are relevant to several clinical disorders characterized by abnormal gating of sensory information, including autism, schizophrenia, and dyslexia.     

Corticofugal projection inhibits the auditory thalamus through the thalamic reticular nucleus

Electrical stimulation of the auditory cortex (AC) causes both facilitatory and inhibitory effects on the medial geniculate body (MGB). The purpose of this study was to identify the corticofugal inhibitory pathway to the MGB. We assessed two potential circuits: 1) the cortico-colliculo-thalamic circuit and 2) cortico-reticulo-thalamic one. We compared intracellular responses of MGB neurons to electrical stimulation of the AC following bilateral ablation of the inferior colliculi (IC) or thalamic reticular nucleus (TRN) in anesthetized guinea pigs. Cortical stimulation with intact TRN could cause strong inhibitory effects on the MGB neurons. The corticofugal inhibition remained effective after bilateral IC ablation, but it was minimized after the TRN was lesioned with kainic acid. Synchronized TRN neuronal activity and MGB inhibitory postsynaptic potentials (IPSPs) were observed with multiple recordings. The results suggest that corticofugal inhibition traverses the corticoreticulothalamic pathway, indicating that the colliculi-geniculate inhibitory pathway is probably only for feedforward inhibition.     

Differential distribution of burst and single-spike responses in auditory thalamus

The medial geniculate body (MGB) of the auditory thalamus comprises lemniscal and nonlemniscal neurons that project to the primary auditory cortex and limbic structures, respectively. Here we show that in anesthetized guinea pigs, MGB responses to a noise-burst stimulus exhibit distinct and synaptic pathway-specific firing patterns. The majority of nonlemniscal MGB cells exhibited bursting responses, whereas lemniscal neurons discharged mainly single or spike doublets. The burst firing is delayed in nonlemniscal neurons and exhibited several features that are characteristics of those mediated by low-threshold Ca(2+) spikes. Such a synaptic pathway-specific allocation of bursting and single-spike firing patterns is consistent with the notion of parallel processing of auditory information in thalamocortical system.