Low Spontaneous Discharge Rates Research Articles

Development of spontaneous activity and response properties of primary lagenar neurons in the chick.

Here, we report for the first time developmental changes in spontaneous activity and in response properties of single nerve fibers from the macular chick lagena. Such aspects are important in order to get insight into the functional role of the lagena which remains undetermined. For this purpose, we used intracellular and extracellular single-unit recording techniques in an isolated inner ear preparation from the chicken at ages E15 and P1. At E15, afferent fibers displayed a low irregular spontaneous discharge rate (41 +/- 14 spikes/s, CV = 1.17 +/- 0.1), which was replaced by regular high frequency spontaneous activity at P1 (CV = 0.48 +/- 0.8, 89 +/- 27 spikes/s). During the developmental period including E15, the percentage of silent neurons was 60% while that of P1 was 40%. The synaptic activity was higher at E15 than at P1. The action potential waveform generated at E15 had small amplitude and derivative depolarization, and consequently, a large duration in correlation with respect to action potential waveform at P1 (respectively: 53 +/- 2 vs. 65 +/- 3 mV, 60 +/- 11 vs. 109 +/- 20 mV/ms, 3.6 +/- 0.4 vs. 1.1 +/- 0.12 ms). In addition, we recognized two response dynamics to the injection of current steps: phasic, or rapidly adapting neurons and tonic, or slowly adapting neurons. Our results indicate similar developmental processes for the lagena as described for the vestibular system in other species, in agreement with the known morphological characteristics of this otholitic end organ. The presence of more than one subtype of afferent neuron also correlates with previous reports on vestibular afferents with analogous electrophysiological properties, strongly suggesting the vestibular nature of the lagena.

Towards a unifying basis of auditory thresholds: Distributions of the first-spike latencies of auditory-nerve fibers

Detecting sounds in quiet is the simplest task performed by the auditory system, but the neural mechanisms underlying perceptual detection thresholds for sounds in quiet are still not understood. Heil and Neubauer [Heil, P., Neubauer, H., 2003. A unifying basis of auditory thresholds based on temporal summation. Proc. Natl. Acad. Sci. USA 100, 6151–6156] have provided evidence for a simple probabilistic model according to which the stimulus, at any point in time, has a certain probability of exceeding threshold and being detected. Consequently, as stimulus duration increases, the cumulative probability of detection events increases, performance improves, and threshold amplitude decreases. The origin of these processes was traced to the first synapse in the auditory system, between the inner hair cell and the afferent auditory-nerve fiber (ANF). Here we provide further support for this probabilistic “continuous-look” model. It is derived from analyses of the distributions of the latencies of the first spikes of cat ANFs with very low spontaneous discharge rates to tones of different amplitudes. The first spikes in these fibers can be considered detection events. We show that, as predicted, the distributions can be explained by the joint probability of the occurrence of three independent sub-events, where the probability of each of those occurring is proportional to the low-pass filtered stimulus amplitude. The “temporal integration” functions of individual ANFs, derived from their first-spike latencies, are remarkably similar in shape to “temporal integration” functions, which relate threshold sound pressure level at the perceptual level to stimulus duration. This further supports a close link between the mechanisms determining the timing of the first (and other) evoked spikes at the level of the auditory nerve and detection thresholds at the perceptual level. The possible origin and some functional consequences of the expansive power-law non-linearity are discussed.

Phase Locking of Auditory-Nerve Fibers to the Envelopes of High-Frequency Sounds: Implications for Sound Localization

Although listeners are sensitive to interaural time differences (ITDs) in the envelope of high-frequency sounds, both ITD discrimination performance and the extent of lateralization are poorer for high-frequency sinusoidally amplitude-modulated (SAM) tones than for low-frequency pure tones. Psychophysical studies have shown that ITD discrimination at high frequencies can be improved by using novel transposed-tone stimuli, formed by modulating a high-frequency carrier by a half-wave-rectified sinusoid. Transposed tones are designed to produce the same temporal discharge patterns in high-characteristic frequency (CF) neurons as occur in low-CF neurons for pure-tone stimuli. To directly test this hypothesis, we compared responses of auditory-nerve fibers in anesthetized cats to pure tones, SAM tones, and transposed tones. Phase locking was characterized using both the synchronization index and autocorrelograms. With both measures, phase locking was better for transposed tones than for SAM tones, consistent with the rationale for using transposed tones. However, phase locking to transposed tones and that to pure tones were comparable only when all three conditions were met: stimulus levels near thresholds, low modulation frequencies (<250 Hz), and low spontaneous discharge rates. In particular, phase locking to both SAM tones and transposed tones substantially degraded with increasing stimulus level, while remaining more stable for pure tones. These results suggest caution in assuming a close similarity between temporal patterns of peripheral activity produced by transposed tones and pure tones in both psychophysical studies and neurophysiological studies of central neurons.

Neural information transferred from the putamen to the globus pallidus during learned movement in the monkey.

1. We studied the physiology of the neuronal projection from the striatum to the external and internal segments of the globus pallidus (GPe and GPi, respectively) in macaque monkeys. The objective of the study was to answer the following specific questions. 1) Which classes of the electrophysiologically identified striate neurons project to GPe and GPi? 2) What kind of information is transferred from the striatum to GPe and GPi during learned movement? 3) What are the physiological actions of striate projection neurons on target neurons in GPe and GPi? 4) What is the spatial pattern of the striatopallidal projections? 2. Sequential arm and orofacial movements were used as behavioral tasks. Visual stimuli triggered a sequence of three flexions-extensions of the elbow joint across the target, and the click of a solenoid valve triggered repetitive licking movements. 3. Striatopallidal projection neurons were electrophysiologically identified by antidromic activation after focal stimulation of either GPe or GPi. Of two classes of striate neurons, tonically active neurons (TANs) with tonic spontaneous discharges (2-8 imp/s) and broad action potentials, and phasically active neurons (PANs) with a very low spontaneous discharge rate (< 0.5 imp/ s) and high-frequency discharges in relation to behavioral tasks, PANs were identified as the projection neurons to either GPe or GPi. In 325 TANs examined by stimulation of GPe or GPi, no neuron was activated antidromically, even in the case of TANs located in the close vicinity of PANs that were identified as striatopallidal projection neurons. 4. The physiologically identified projection neurons (52 cells) in the striatum exhibited either discharges related to movement (30 cells) or discharges related to preparation for movement (4 cells) during performance of learned motor tasks. The activities of the remaining 17 striatopallidal neurons either were not related to the behavioral tasks used or could not be characterized sufficiently in the tasks. However, all of the unidentified striatopallidal neurons were PANs, on the basis of the spontaneous discharge rate and the shape of the action potential. 5. PANs with movement-related activity and those with preparation for movement-related activity were antidromically activated from the globus pallidus (GP). Not only the PANs that show burst discharges specifically at the beginning of a sequence of movement but also PANs that show phasic discharges time-locked to each movement of a sequence were identified as putaminopallidal projection neurons. On the other hand, no neurons that showed responses to sensory stimulus were identified as putaminopallidal neurons. 6. The conduction velocities of the putaminopallidal axons were estimated at approximately 1 m/s on the basis of the latency of antidromic activation and conduction distance. The PANs with activity only at the beginning of a sequential movement were more frequently found to project to GPi than to GPe, whereas the PANs with burst activity at each movement were more frequently found to project to GPe than to GPi. Among the GPi-projecting PANs, neurons with initial activity only showed a tendency to have longer latencies of activation from GPi than neurons with activity time-locked to each movement. 7. The physiological action of the striatopallidal projection was examined by switching from recording to microstimulation after identification of striatopallidal projection neurons in the putamen while recording evoked field potentials or spike discharges of single GP neurons located where the electrical stimulation evoked antidromic activation of the striate neurons with the lowest threshold. A small majority of GP neurons that exhibited increase of discharges during motor tasks received facilitatory putaminopallidal influences, whereas the vast majority of GP neurons that exhibited decrease of discharges during motor tasks received suppressive putaminopallidal influences.

Morphological subclasses of lateral olivocochlear terminals? Ultrastructural analysis of inner spiral bundle in cat and guinea pig.

The lateral olivocochlear efferent pathway terminates in vesicle-filled swellings in the inner spiral bundles under inner hair cells (IHCs) and has been suggested to include at least two chemically distinct subclasses (see, e.g., Vetter et al. [1991] Synapse 7:21-43). In the present study, the ultrastructure and peripheral targets of vesicle-filled swellings in the IHC area of the cat and guinea pig cochleas were quantitatively analyzed to determine 1) whether morphological subclasses could be defined based on swelling size or on the density, size or shape of clear and dense-cored vesicles and 2) whether swellings with different postsynaptic targets differed morphologically. In both cat and guinea pig, all swellings contained large, round, clear vesicles and a variable number of dense-core vesicles. Although evidence of clear-cut subclasses was not compelling, the smallest swellings tended to be rich in dense-core and poor in clear vesicles and rarely formed synaptic contacts. Most of the larger swellings, which tended to contain few dense-core vesicles and a rich complement of clear round vesicles, formed synapses with radial afferent fibers. However, there were no morphological differences between swellings contacting afferents originating on the modiolar vs. pillar sides of the IHC (the source of afferents with low and high spontaneous discharge rates, respectively). We conclude that 1) if distinct gamma-amino butyric acid (GABA)ergic and cholinergic subclasses of lateral olivocochlear (LOC) fibers exist, then the vesicle morphology of their terminals does not differ as it does in the central nervous system and that 2) if peptide neurotransmitters, such as calcitonin gene-related peptide and enkephalins, are packaged in dense-core vesicles, then the LOC terminals synapsing with IHC afferent fibers are not particularly rich in these peptides.

Ultrastructural differences among afferent synapses on cochlear hair cells: Correlations with spontaneous discharge rate

The major class of cochlear afferent fibers, the type-I or radial-fiber (RF) population, has been subdivided into three functional groups according to spontaneous discharge rate (SR): those with low SR have the highest acoustic thresholds, high SR fibers have the lowest thresholds and medium SR fibers are of intermediate sensitivity (Liberman [1978] J. Acoust. Soc. Amer. 63:442–455). Existing evidence from intracellular labeling studies at the light microscopic level (Liberman [1982a] Science 216:1239–1241) suggests that a single cochlear inner hair cell makes synaptic contact with representatives of all three functional groups; however, low and medium SR fibers are spatially segregated from high SR fibers around the hair cell circumference, and low and medium SR fibers are smaller in caliber than those with high SR. The present study extends to the ultrastructural level the structure-function correlations available via intracellular labeling. Analysis is based on serial section reconstruction of the synaptic contacts between 11 radial fibers of known SR and their target hair cells. Results suggest systematic differences in synaptic ultrastructure among fibers of the three SR groups: with decreasing SR, the size and complexity of the synaptic body (a presynaptic specialization characteristic of the peripheral afferent synapses in all hair cell systems and some other peripheral receptors) tend to increase, as does the associated number of synaptic vesicles. The possible functional significance of these trends is discussed in the context of other known structural and functional differences among the three SR groups. © 1996 Wiley-Liss, Inc.

Discharge patterns of chicken cochlear ganglion neurons following kanamycin-induced hair cell loss and regeneration.

Hair cells in the basal, high frequency region (> 1100 Hz) of the chicken cochlea were destroyed with kanamycin (400 mg/kg/d x 10 d) and allowed to regenerate. Afterwards, single unit recordings were made from cochlear ganglion neurons at various times post-treatment. During the first few weeks post-treatment, only neurons with low characteristic frequencies (< 1100 Hz) responded to sound. Despite the fact that the low frequency region of the cochlea was not destroyed, neurons with low characteristic frequencies had elevated thresholds, abnormally broad U-shaped or W-shaped tuning curves and low spontaneous discharge rates. At 2 days post-treatment, the spontaneous discharge rates of some acoustically unresponsive units fluctuated in a rhythmical manner. As recovery time increased, thresholds decreased, tuning curves narrowed and developed a symmetrical V-shape, spontaneous rate increased and neurons with higher characteristic frequencies began to respond to sound. In addition, the proportion of interspike interval histograms with regularly spaced peaks increased. These improvements progressed along a low-to-high characteristic frequency gradient. By 10-20 weeks post-treatment, the thresholds and tuning curves of neurons with characteristic frequencies below 2000 Hz were within normal limits; however, the spontaneous discharge rates of the neurons were still significantly lower than those from normal animals.

Behavioral modulation of sensory responses of primate putamen neurons

Sensory response properties of putamen neurons were investigated in 4 awake macaque monkeys while the animals performed GO/NO-GO tasks guided by sensory stimuli. In the GO condition, visual stimuli served as a trigger for a sequence of repetitive elbow flexion-extensions and auditory stimuli served as a trigger for orofacial movements, while the identical sensory stimuli required the animals to withhold movements in the NO-GO condition. Short latency responses to visual and/or auditory stimuli were observed in 206 type I cells with tonic discharges at about 2–7 Hz, with a characteristic discharge rhythm and in 57 type II cells with low spontaneous discharge rates, usually less than 0.5 Hz, which showed burst discharges during the tasks. Most of these cells (163/206 type I cells, 52/57 type II cells) responded differentially to identical sensory stimuli presented in the GO and NO-GO conditions. The responses to sensory stimuli presented in the GO condition were much larger in 67% of type I cells and 58% of type II cells than the responses to identical stimuli presented in the NO-GO condition. On the other hand, 12% of type I and 33% of type II cells showed larger responses in the NO-GO than in the GO condition. It is suggested that the strong behavioral modulation of striatal sensory responses serves as a mechanism to start the neural processes for preparation and/or initiation or withholding of particular movements associated with learned sensory stimuli.

Synaptic connections of the auditory nerve in cats: Relationship between endbulbs of held and spherical bushy cells

This report focuses on a class of large synaptic endings, the endbulbs of Held. These endings are located in the anteroventral cochlear nucleus and arise from the axons of type I spiral ganglion neurons. Axons were stained with horseradish peroxidase (HRP) using intracellular injections of single fibers or extracellular injections into the auditory nerve. Individual endbulbs or pairs of endbulbs that converged onto the same spherical bushy cell were examined with the aid of a light microscope and subjected to morphometric analyses. Endbulbs of fibers having low spontaneous discharge rates (SR, less than or equal to 18 spikes/sec) have a more complex shape than those of high SR fibers (greater than 18 s/s), a feature represented by systematic differences in endbulb silhouette perimeter without differences in endbulb silhouette area. Consequently, the ratio, silhouette area divided by silhouette perimeter, yields a "form factor" separating endbulbs of high SR from those of low SR. High SR fibers had ratios greater than 0.52 (mean = 0.63 +/- 0.09), whereas low SR fibers had ratios less than 0.52 (mean = 0.45 +/- 0.06). Pairs of endbulbs with unknown physiological properties had similar form factor values, despite the wide range of values observed in the endbulb population. These data imply that endbulbs converging upon the cell body of a spherical bushy cell arise from fibers of the same SR group. Electron microscopic examination was conducted on the endbulb of one physiologically characterized and intracellularly stained auditory nerve fiber (CF = 1.4 kHz; SR = 55 s/s) and its unstained endbulb mate with the aid of serial ultrathin sections. In addition to the well-known axosomatic synapses, these endbulbs formed axodendritic synapses: 11.7% for the HRP-labeled endbulb and 13.3% for the unlabeled endbulb. The axodendritic synapses appear to occur on dendrites of nearby spherical bushy cells and may represent a mechanism whereby single endbulbs can disperse activity to multiple neurons in the cochlear nucleus. We propose that axosomatic synapses preserve fiber SR groupings, whereas axodendritic synapses may not.

Physiological properties of projection neurons in the monkey striatum to the globus pallidus

In order to study neuronal information transfer from the striatum to the globus pallidus (GP) during voluntary movement, we recorded activity of electrophysiologically identified projection neurons in the putamen to the GP while the monkey was performing learned movement tasks. Two categories of putamen neurons were recorded: one with tonic spontaneous discharges at about 2-7 impulses/s responded to external sensory stimuli (type I); the other with very low spontaneous discharge rates less than 0.5 impulses/s showed phasic burst discharges which were time-locked to limb or orofacial movements (type II). All of the putamen neurons identified as projecting to the GP (external and/or internal segment) by an antidromic activation from electrical stimulation of the GP were type II cells. It was concluded that the movement-related activity of type II putamen neurons is transferred to GP and/or SN during voluntary movement but tonically active type I cells do not project to the GP.

Behaviorally contingent property of movement-related activity of the primate putamen

1. In this study, the movement-related activity of putamen neurons was investigated in behaving monkeys. The objective of the study was to examine whether the activity occurring in phase with body movements is directly related to the movement per se by encoding movement parameters or whether it is dependent on the circumstances in which the movement is performed. 2. Sensorially triggered arm movements were used as a behavioral task. A sequence of three visually triggered repetitive flexion-extensions of the elbow joint across the target were followed by the delivery of a juice reward. 3. There are two classes of putamen cells: type I, with tonic spontaneous discharges (2-7 Hz) and broad extracellularly recorded action potentials, and type II, with very low spontaneous discharge rate (less than 1 Hz). The movement-related phasic discharges occur exclusively in type II cells. 4. The movement-related activity of type II cells is classified into two contrasting types of cells: type IIa that exhibit burst discharges preceding the first movement of a sequence of repetitive arm or orofacial movements but that are almost inactive during succeeding movements, and type IIb that show movement-locked burst discharges with one-to-one correspondence. The somatotopic location of the cells was identified by microstimulation and/or sensory responses to passive somatosensory manipulation of the periphery. 5. The activities of type IIa cells occur with a short and fairly constant latency after the visual trigger stimulus and cease as soon as the sequence of the learned movements is initiated. In the condition in which the monkey attended to the visual trigger stimulus without initiating learned movements and waited for the delivery of juice reward at a fixed time after the stimulus, type IIa cells exhibited slight but consistent phasic discharges after the visual stimulus with short latency. This indicates that the type IIa cells have a visuomovement property. The type IIb cells, on the other hand, have a longer latency of activity after the visual trigger than type IIa cells and do not have the visuomovement property. 6. The type IIa cells change their activity pattern depending on whether the direction of initial movement is predictable before the trigger stimulus or not. 7. The activities of type IIa cells in the arm area of the putamen precede the electromyogram (EMG) of prime mover muscles by greater than 100 ms on average, whereas most type IIb cells are activated after the EMG during a learned arm-movement task.(ABSTRACT TRUNCATED AT 400 WORDS)

Diversity of characteristic frequency rate-intensity functions in guinea pig auditory nerve fibres

Rate-intensity functions at characteristic frequency (CF) were recorded from single fibres in the auditory nerve of anaesthetised guinea pigs. Within the same animal, CF rate-intensity functions, although probably forming a continuum, could be conveniently divided into three groups; (1) Saturating; reach maximum discharge rate within 30 dB of threshold, (2) Sloping-saturation; initially rapid growth in discharge rate leading to a slower growth in discharge rate but not saturating and (3) Straight; approximately constant increase in firing rate per decibel increase in sound pressure up to the maximum sound pressures used. Thresholds for individual fibres were plotted relative to compound action potential thresholds at the appropriate frequency. Fibres with straight CF rate-intensity functions had the highest thresholds. Fibres of the saturating CF rate-intensity type had the lowest thresholds, and the sloping-saturation CF rate-intensity type had thresholds intermediate between saturating and straight. There was a close relationship between the type of CF rate-intensity function exhibited by a fibre and its spontaneous discharge rate. Fibres with saturating CF rate-intensity functions generally had high spontaneous discharge rates (greater than 18/s), whereas those with straight CF rate-intensity functions generally had low spontaneous discharge rates (less than 0.5/s). The majority of fibres with sloping-saturation CF rate-intensity functions had spontaneous rates between 0.5/s and 18/s. There was a negative correlation (r = −0.59) between the logarithm of the spontaneous discharge rate and relative threshold at CF with the lowest spontaneous rate fibres having the highest thresholds and vice-versa. This diversity of CF rate-intensity functions has functional implications for both frequency and intensity coding at high sound pressures in the mammalian auditory system.

Neural coding in the chick cochlear nucleus

Physiological recordings were made from single units in the two divisions of the chick cochlear nucleus-nucleus angularis (NA) and nucleus magnocellularis (NM). Sound evoked responses were obtained in an effort to quantify functional differences between the two nuclei. In particular, it was of interest to determine if nucleus angularis and magnocellularis code for separate features of sound stimuli, such as temporal and intensity information. The principal findings are: 1. Spontaneous activity patterns in the two nuclei are very different. Neurons in nucleus angularis tend to have low spontaneous discharge rates while magnocellular units have high levels of spontaneous firing. 2. Frequency tuning curves recorded in both nuclei are similar in form, although the best thresholds of NA units are about 10 dB more sensitive than their NM counterparts across the entire frequency range. A wide spread of neural thresholds is evident in both NA and NM. 3. Large driven increases in discharge rate are seen in both NA and NM. Rate intensity functions from NM units are all monotonic, while a substantial percentage (22%) of NA units respond to increased sound level in a nonmonotonic fashion. 4. Most NA units with characteristic frequencies (CF) above 1000 Hz respond to sound stimuli at CF as 'choppers', while units with CF's below 1000 Hz are 'primary-like'. Several 'onset' units are also seen in NA. In contrast, all NM units show 'primary-like' response. 5. Units in both nuclei with CF's below 1000 Hz show strong neural phase-locking to stimuli at their CF. Above 1000 Hz, few NA units are phase-locked, while phase-locking in NM extends to 2000 Hz. 6. These results are discussed with reference to the hypothesis that NM initiates a neural pathway which codes temporal information while NA is involved primarily with intensity coding, similar in principle to the segregation of function seen in the cochlear nucleus of the barn owl (Sullivan and Konishi 1984).

The central projections of intracellularly labeled auditory nerve fibers in cats: an analysis of terminal morphology.

The axons of physiologically characterized spiral ganglion neurons (type I) were stained throughout their arborizations in the cochlear nucleus by the intracellular injection of horseradish peroxidase (HRP). The tips of the axonal branches were marked by distinct swellings, ranging in size and shape from small boutons to large perisomatic ramifications. Electron microscopic analysis of such swellings revealed ultrastructural features characteristic of primary auditory synapses, consistent with the hypothesis that terminal swellings identifiable in the light microscope represent presynaptic endings. On the basis of light microscopic differences in size, these endings were organized into three categories. Endings of relatively small size (terminal boutons, free endings, boutons with filopodia, string endings, and small complex endings) composed 94% of all terminal endings. Within this category of small endings, there were predictable variations in relative size and regional distribution that related to the spontaneous discharge rate (SR) of the fiber. The endings of low and medium SR fibers (SR less than or equal to 18 spikes/second) were smaller on average than those of high SR fibers (SR greater than 18 spikes/second). Furthermore, there were more endings arising from the ascending branch than from the descending branch when comparing fibers of the low and medium SR group with those of the high SR group. There were not, however, obvious morphological features of this ending category that correlated with the characteristic frequency (CF, the pure tone frequency to which the neuron is most sensitive). A second category contained medium-sized complex endings, most of which formed axosomatic contacts. This category composed 4% of the population and was found in close proximity to the perikarya of globular, octopus, and spherical cells. The endings from low and medium SR fibers were smaller on average than those from high SR fibers. These endings did not vary in their parent branch distribution with respect to fiber SR, nor did they exhibit morphological features that correlated with fiber CF. The third category contained large complex endings (endbulbs of Held) and composed 2% of the ending population. Within the anteroventral cochlear nucleus, these large, complex endings made axosomatic contact with spherical cells in the anterior division and with globular cells in the posterior division. There were no systematic variations in ending size or branch distribution that correlated with fiber SR. There was, however, a relationship between ending size and fiber CF such that fibers having CFs below 4 kHz gave rise to the largest endbulbs.

Coding of spectral fine structure in the auditory nerve. I. Fourier analysis of period and interspike interval histograms.

The temporal fine structure of discharge patterns of single auditory-nerve fibers in adult cats was analyzed in response to signals consisting of a variable number of equal-intensity, in-phase harmonics of a common low-frequency fundamental. Two analytic methods were employed. The first method considered Fourier spectra of period histograms based on the period of the fundamental, and the second method considered Fourier spectra of interspike interval histograms (ISIH's). Both analyses provide information about fiber tuning properties, but Fourier spectra of ISIH's also allow estimates to be made of the degree of resolution of individual stimulus components. At low intensities (within 20-40 dB of threshold), indices of synchronization to individual components of complex tones were similar to those obtained for pure tones. This was true even when fibers were capable of responding to several signal components simultaneously. Response spectra obtained at low intensities resembled fibers' tuning curves, and fibers with low spontaneous discharge rates tended to provide better resolution of stimulus components than fibers with high spontaneous rates. Strongly nonlinear behavior existed at higher stimulus intensities. In this, information was transmitted about progressively fewer signal components and about frequencies not present in the acoustic stimulus, and the component eliciting the largest response shifted away from the fiber's characteristic frequency and toward the edges of the stimulus spectrum. This high-intensity "edge enhancement" can result from the combined effects of a compressive input-output nonlinearity, suppression, and the fortuitous addition of internally generated combination tones. The data indicate that sufficient information exists for the auditory system to determine the frequencies of narrowly spaced stimulus components from the temporal fine structure of nerve fiber's responses.

The central projections of intracellularly labeled auditory nerve fibers in cats.

The central projections of physiologically characterized auditory nerve fibers were studied in the cochlear nuclei of adult cats after intracellular staining with horseradish peroxidase (HRP). This technique consistently labels only the type I spiral ganglion neurons which contact inner hair cells in the cochlea (Liberman and Oliver, '84). The central axon of each type I neuron bifurcates in the cochlear nucleus to form an ascending branch and a descending branch. The characteristic frequency (CF) of a fiber corresponds to the dorsoventral position of these major branches and their collateral ramifications within the nucleus. Fibers of low CFs are distributed ventrally, and fibers of increasing CF are distributed progressively more dorsally. In some cases, the collateral branches deviate from this tonotopic arrangement, particularly in (1) the octopus cell region of the posteroventral cochlear nucleus, (2) the zone of bifurcations of the auditory nerve fibers, and (3) the anterior, dorsal, and lateral margins of the ventral cochlear nucleus. Spontaneous discharge rate (SR) is related to the complexity of the axon arbor, especially along the ascending branch. Fibers of low and medium SR exhibit more axonal branch points and longer collateral lengths than do those with high SR. Six of 37 labeled fibers fail to innervate the dorsal cochlear nucleus, a feature apparently unrelated to CF or SR.

Tone‐on‐tone masking in auditory nerve fibers with medium spontaneous rates

Auditory nerve fibers can be categorized by their spontaneous discharge rates (SRs). Although the significance of these categories is not known, it has been suggested that the low and medium SR fibers may contribute to frequency analysis at signal levels at which the more sensitive high SR fibers are saturated. Data obtained from chinchilla auditory nerve fibers in response to two‐tone stimuli are consistent with that possibility. The stimuli were presented in a tone‐on‐tone masking paradigm analogous to that used by Long and Miller [Hear. Res. 4, 279–285 (1981)] for psychophysical measurements in chinchillas, and average discharge rate data from fibers with medium and high SRs were analyzed separately. Good agreement between the “masked thresholds” of medium SR fibers and the behavioral masked thresholds was observed. Masked thresholds of medium SR fibers were sometimes lower than the masked thresholds of high SR fibers, even though their quiet thresholds tend to be higher. This difference was greatest (10–15 dB) for masker‐probe tone pairs with the smallest frequency separations. High SR fibers were often driven to saturation by the masker, so that no masked threshold could be estimated; however, probe tones nearly always produced rate changes in medium SR fibers. [Supported by NIH.]

Intensity coding in the auditory periphery of the cat: responses of cochlear nerve and cochlear nucleus neurons to signals in the presence of bandstop masking noise.

The dynamic range over which fine intensity discrimination is possible has been reported to be largely unaffected by limitation of the spread of neuronal activity to neighbouring frequency regions by bandstop noise masking. We have therefore examined the responses of cochlear nerve and nucleus neurons to tone and noise signals in the presence of a bandstop masking noise designed to be comparable to that employed in the psychophysical experiments. Under these conditions, the vast majority of cochlear nerve fibres were saturated by sound levels at which some 50% of our sample of cochlear nucleus neurons still responded to signal level differences. The extended dynamic ranges of these cochlear nucleus neurons was shown to be a result of activation, by the masking noise, of the lateral inhibitory side-bands 'biassing' the neuron's discharge. A small proportion of cochlear fibres, having low spontaneous discharge rates and showing strong two-tone suppression effects, demonstrated analogous but not so pronounced effects. It is unclear in what form information on the level of stimuli under these conditions is transmitted by the majority of apparently saturated cochlear nerve fibres, but several possible mechanisms are discussed.

Relationship between the dynamic range of cochlear nerve fibres and their spontaneous activity

The dynamic ranges of cochlear nerve fibres in cats were determined automatically and were related to the fibres' rates of spontaneous activity, in both pooled data and data from individual cochlear nerves. The dynamic range represents the range of levels of a tone at the characteristic frequency of the fibre evoking mean discharge rates between spontaneous and saturated activity. In common with the findings of other investigators, the distribution of spontaneous discharge rates was bimodal. The total population could be divided into two sub-populations with spontaneous discharge rates above and below 15 spikes/s, respectively. The mean dynamic range of fibres having spontaneous discharge rates in excess of 15 spikes/s, was 41 dB (+/- 0.65 S.E.); that for fibres with rates below 15 spikes/s was 50 dB (+/- 1.2 S.E.). While the distributions of dynamic ranges of the two populations overlapped, they were significantly different, and dynamic ranges in excess of 60 dB were only found in substantial numbers (23%) in the population having low spontaneous discharge rates. Some of these were not saturated at the highest stimulus levels used.

Cochlear fibre rate-intensity functions: No evidence for basilar membrane nonlinearities

The presence of inflexions in the slopes of the rate-intensity functions of single cochlear fibres has been cited as evidence for nonlinearities, in the motion of the basilar membrane, of the type described by Rhode. We have carried out a detailed study of these inflexions in the anaesthetized cat. The inflexions were found to be related more to the threshold of the individual fibre than to occur at a common sound pressure level, for fibres of similar and differing characteristic frequency. Likewise, contrary to the earlier evidence, no strong inverse relationship was found to exist between the magnitude of the slope of the rate-intensity function and the threshold of a fibre. What relationship did exist depended upon the presence of fibres having low spontaneous discharge rate activity. The data therefore do not support the concept of a common input (i.e. basilar membrane) nonlinearity; rather, they suggest that the shape and slope of the rate-intensity functions are more related to the properties of individual neural channels.