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Octopus cells in the ventral cochlear nucleus (VCN) have been difficult to study because of the very features that distinguish them from other VCN neurons. We performed in vivo recordings in cats on well-isolated units, some of which were intracellularly labeled and histologically reconstructed. We found that responses to low-frequency tones with frequencies

Much of what is known about how the cochlear nuclei participate in mammalian hearing comes from studies of non-primate mammalian species. To determine to what extent the cochlear nuclei of primates resemble those of other mammalian orders, we have recorded responses to sound in three primate species: marmosets, cynomolgus macaques, and squirrel monkeys. These recordings show that the same types of temporal firing patterns are found in primates that have been described in other mammals. Responses to tones of neurons in the ventral cochlear nucleus have similar tuning, latencies, post-stimulus time and interspike interval histograms as those recorded in non-primate cochlear nucleus neurons. In the dorsal cochlear nucleus, too, responses were similar. From these results it is evident that insights gained from non-primate studies can be applied to the peripheral auditory system of primates.

The mammalian cochlear nucleus (CN) consists of a diverse set of neurons both physiologically and morphologically that are involved in processing different aspects of the sound signal. One class of CN neurons that is located near the entrance of the auditory nerve (AN) to the CN has an oval soma with an eccentric nucleus and a short-bushy dendritic tree and is called a globular/bushy cell (GBC). They contact the principal cells of the medial nucleus of the trapezoid body (MNTB) with the very large calyx of Held that is one of the most secure synapses in the brain. Because MNTB cells provide an inhibitory input to the lateral superior olive (LSO), a structure purported to play a role in lateralizing high frequency sounds, GBC physiology is of great interest. Results were obtained with intracellular recording and subsequent labeling with neurobiotin of 32 GBCs along with a number of cells characterized extracellularly as likely GBCs in the cochlear nucleus (CN) of cat. Their poststimulus discharge response pattern to repeated tones varies from a primarylike pattern, i.e. similar to the AN, to a primarylike pattern with a 0.5–2 ms notch after the initial spike, to an onset pattern with a low-sustained rate. They can represent low frequency tones and amplitude modulated signals exceptionally well with a temporal code.

Amplitude modulated (AM) signals have often been used as precisely defined partial analogs of speech sounds. This study considers the response to an AM complex with 200% sinusoidal modulation, that is, the amplitudes of the three AM components are equal. By varying the carrier frequency across the entire frequency range of unit response, it is shown that units in the cochlear nucleus of cat are relatively insensitive to variation in the carrier frequency, which is to say that population response to an AM signal at a fixed locus will be widespread. These stimuli and procedures result in the presentation of both harmonic and inharmonic complexes, and thus permit assessment of neural responses for the information needed to make spectral or time-domain pitch matches. It is shown that the reciprocals of the modes (favored intervals) in the interspike interval histogram reflect the first effect of pitch shift, which is defined psychophysically as a proportional shift in pitch to the change in carrier frequency. In particular, interspike intervals of units with a widespread spectral response provide a basis to explain phase and dominant component pitch behavior that early narrow-band pitch theories found problematical. The amplitude of phase locking to individual AM components varies systematically though there are some unexplained variations across the frequency-intensity plane that could be due to combination tones. The unit response to a quasifrequency modulated (QFM) stimulus shows that if pitch is based on interspike intervals, it would remain the smae as pitch for an AM signal. The magnitude of the synchrony response to QFM stimuli is less than to AM stimuli for the majority of cochlear nucleus units; however, there are exceptions.

A software routine to reconstruct individual spike trains from multi-neuron, single-channel extracellular recordings was designed. Using a neural network algorithm that automatically clusters and sorts the spikes, the only user input needed is the threshold level for spike detection and the number of unit types present in the recording. Adaptive features are included in the algorithm to allow for tracking of spike trains during periods of amplitude variation and also to identify noise spikes. The routine will operate on-line during extracellular studies of the cochlear nucleus in cats.

1. Amplitude modulation (AM) is a pervasive property of acoustic communication systems. In the present study we investigate neural temporal mechanisms in the auditory nerve and cochlear nuclei of the pentobarbital sodium-anesthesized cat associated with the neural coding of 100% AM tones, both in quiet and in the presence of wideband, quasi-flat-spectrum noise. The AM carrier frequency was set to the neuron's characteristic frequency (CF) and the sound pressure level (SPL) of acoustic stimuli was varied over a wide dynamic range of intensities (< or = 40 dB). The temporal AM-encoding capability of auditory neurons was measured by computing the synchronization coefficient (SC) of the neural response to the signal's modulation and carrier frequency. The temporal modulation transfer function (tMTF) of a neuron was then computed by measuring the SC of the response to signals of variable fmod (50-2550 Hz). 2. Neurons in the cochlear nuclei synchronize on average more highly to the modulation frequency than fibers of comparable CF, threshold, and spontaneous rate in the auditory nerve. The disparity in performance is greatest at high SPLs and low signal-to-noise ratios. However, there is a significant degree of diversity in AM-encoding capability among neurons in both the cochlear nuclei and auditory nerve. Among auditory nerve fibers (ANFs), low- and medium-spontaneous-rate (SR) units (SR < 18 spike/s) phase-lock with greater precision than comparable high-SR units at any given frequency, particularly at moderate to high SPLs, consistent with previous studies. 3. The phase-locking capabilities of neurons in the cochlear nucleus are considerably more variable than in the auditory nerve. Moreover, the variability itself depends on two distinct measures of phase-locking performance. Most ANFs are capable of phase-locking to frequencies as high as 3–4 kHz. In the cochlear nucleus many unit types do not phase-lock to modulation frequencies > 1 kHz. As a result, phase-locking performance is measured on the basis of two parameters, maximum synchronization, irrespective of stimulus frequency, and the upper frequency limit for significant phase-locking. 4. Cochlear nucleus neurons may be divided into three distinct groups on the basis of maximum synchronization capability. In group 1 are the primary-like (PL) units of the anteroventral division, whose phase-locking capabilities are comparable with those of high-SR ANFs.(ABSTRACT TRUNCATED AT 400 WORDS)

Two-tone suppression and two-tone distortion were investigated at the level of the basilar membrane in the hook region of cat and guinea pig cochleae using a displacement-sensitive laser interferometric measurement system. The system allowed measurements to be performed at physiological stimulus levels in the cochlear region tuned to 30-35 kHz in cat and 29 kHz in guinea pig. The amplitude of vibration of the basilar membrane due to a probe tone at the characteristic frequency (CF) was attenuated during the presentation of a simultaneous suppressor tone either above or below CF. The amount of suppression depended on the intensities of both probe and suppressor, and the relationship of the suppressor frequency to the CF. Suppressors at frequencies more than an octave below the CF attenuated the responses to the CF probe at a rate of up to 1 dB/dB, with little variation based on suppressor frequency. As the suppressor frequency was increased above CF the rate of suppression decreased rapidly. The lowest suppressor intensity at which attenuation of the probe response was observed did not vary in direct proportion to the probe intensity. This suppression threshold often varied only a few dB SPL when the probe was varied over a 20 dB SPL range. In a few instances the rate of attenuation was as much as a factor of two greater at the lowest probe intensities than at higher intensities. It is noteworthy that suppression was found when the frequency of the suppressor was either above or below CF in the same preparation. Low frequency suppressor tones suppress basilar membrane motion at the CF when the basilar membrane undergoes displacement toward either scala. The maximum suppression occurs around 100 microseconds after the peak excursions caused by the low frequency biasing tone. Two-tone distortion products were often observed even at stimulus levels below those causing two-tone suppression at the site studied. The cubic difference tone (CDT) was the most prominent of the distortion products. The level of the CDT component varied nonmonotonically with the level of either of the primary tones. Responses at the difference frequency between the two primaries were usually below the noise floor of the recording system. The existence of both two-tone distortion and two-tone suppression was dependent on the presence of a cochlear nonlinearity.

A heterodyne laser interferometer was used to observe the movements of small (approximately 20 microns) stainless-steel beads placed on the basilar membrane in the hook region of cat and guinea-pig cochleae. In several preparations, the displacement patterns observed exhibited sharp nonlinear tuning; in one cat this tuning was comparable to that commonly observed in single auditory-nerve fibers. The most sensitive frequencies of the preparations ranged from 31-40 kHz in the cat, and 28-32 kHz in the guinea-pig. The sharp tuning and nonlinearity of the basilar membrane responses was not apparent in surgically or acoustically traumatized preparations. The response nonlinearities were susceptible to temporary threshold shifts and disappeared within a few minutes post-mortem. Stimulus-related shifts in the baseline position of the basilar membrane were not apparent at low stimulus levels. Such shifts were occasionally observed at higher stimulus levels (e.g., > 90 dB SPL), but never approached the fundamental (oscillatory) component of basilar membrane vibration in magnitude. These findings are discussed in relation to previous observations by other workers.

Middle-ear to basilar membrane (BM) velocity transfer functions are reported for seven locations in the hook region of a single cat cochlea. These transfer functions were recorded at high sound pressure levels in a linearized, or passive cochlea, and resemble those reported previously by Wilson and Evans (1983). They demonstrate longitudinal tonotopicity with a gradient of approximately 3.6 mm/octave. When allowances are made for the nonlinear mechanisms previously demonstrated in active hook region preparations (Cooper and Rhode, 1992), the data are also consistent with the tonotopic map derived from the intracellular dye-filling studies of Liberman (1982).

A composite model of the auditory periphery, based upon a unique analysis technique for deriving filter response characteristics from cat auditory-nerve fibers, is presented. The model is distinctive in its ability to capture a significant broadening of auditory-nerve fiber frequency selectivity as a function of increasing sound-pressure level within a computationally tractable time-invariant structure. The output of the model shows the tonotopic distribution of synchrony activity of single fibers in response to the steady-state vowel [e] presented over a 40-dB range of sound-pressure levels and is compared with the population-response data of Young and Sachs (1979). The model, while limited by its time invariance, accurately captures most of the place-synchrony response patterns reported by the Johns Hopkins group. In both the physiology and in the model, auditory-nerve fibers spanning a broad tonotopic range synchronize to the first formant (F1), with the proportion of units phase-locked to F1 increasing appreciably at moderate to high sound-pressure levels. A smaller proportion of fibers maintain phase locking to the second and third formants across the same intensity range. At sound-pressure levels of 60 dB and above, the vast majority of fibers with characteristic frequencies greater than 3 kHz synchronize to F1 (512 Hz), rather than to frequencies in the most sensitive portion of their response range. On the basis of these response patterns it is suggested that neural synchrony is the dominant auditory-nerve representation of formant information under "normal" listening conditions in which speech signals occur across a wide range of intensities and against a background of unpredictable and frequently intense acoustic interference.

At a time when little was known about processing in the auditory system, Aage Moller undertook an extensive investigation of the response properties of cochlear nucleus (CN) neurons. With an excellent background in physiological acoustics and a command of computational techniques he systematically explored neural tuning, rate-level functions, and receptive fields of CN neurons using microelectrode recordings. He chose to employ more natural stimuli than just pure tones and employed a variety of stimuli consisting of tones, clicks, noise, amplitude- and frequency-modulated signals to document both intensity and temporal response characteristics. The response to noise stimuli was quantified using linear systems analysis which was very innovative at that time. By choosing to perform the studies in the white rat rather than cat, he provided important comparative data on this first center of the central auditory system. Over a span of ten years he provided a significant body of observations of CN units properties that has rarely been equaled.

The dorsal cochlear nucleus receives input from the auditory nerve and relays acoustic information to the inferior colliculus. Its principal cells receive two systems of inputs. One system through the molecular layer carries multimodal information that is processed through a neuronal circuit that resembles the cerebellum. A second system through the deep layer carries primary auditory nerve input, some of which is relayed through interneurons. The present study reveals the morphology of individual interneurons and their local axonal arbors and how these inhibitory interneurons respond to sound. Vertical cells lie beneath the fusiform cell layer. Their dendritic and axonal arbors are limited to an isofrequency lamina. They give rise to pericellular nests around the base of fusiform cells and their proximal basal dendrites. These cells exhibit an onset-graded response to short tones and have response features defined as type II. They have tuning curves that are closed contours (0 shaped), thresholds approximately 27 dB SPL, spontaneous firing rates of approximately 0 spikes/s, and they respond weakly or not at all to broadband noise, as described for type II units. Their responses are nonmonotonic functions of intensity with peak responses between 30 and 60 dB SPL. They also show a preference for the high-to-low direction of a frequency sweep. It has been suggested that these circuits may be involved in the processing of spectral cues for the localization of sound sources.

1. The ability of cells in the cochlear nucleus (CN) to encode frequency information in the presence of background noise on the basis of "place/rate" information was investigated by measuring the threshold, magnitude, and extent of lateral suppression in the ventral and dorsal CN of the anesthesized cat. The suppression regions were delineated through the use of "masked" response areas (MRAs). The MRA is a family of isointensity curves derived from the average discharge rate in response to a tone of variable frequency and sound pressure level in the presence of a concurrently presented broadband, quasi-flat-spectrum noise. Tonal stimuli of sufficient intensity are often effective in significantly reducing the average discharge rate of CN neurons over a wide frequency range. 2. Most units in the CN exhibit prominent lateral suppressive sidebands, but the variability in threshold, magnitude, and extent of suppression is large. Primary-like and onset units of the ventral CN manifest the least suppression and have the highest suppression thresholds. Pauser/buildup units in the dorsal division and choppers distributed throughout the CN show the largest amount of suppression and have the lowest suppression thresholds. 3. Auditory nerve fibers manifest some degree of lateral suppression, particularly fibers of low and medium spontaneous rate. However, in few instances are the threshold, magnitude, and extent comparable with that observed among the majority of chopper and pauser/buildup units. For this reason the lateral suppression observed among the latter unit types is unlikely to originate entirely from cochlear processes, but rather is likely to reflect largely neural mechanisms intrinsic to the CN. In contrast, the MRAs of most primary-like and onset units suggest that the suppression behavior of most of these cells originates mostly, if not entirely, in the cochlea and auditory nerve. 4. A primary consequence of lateral suppression is to preserve the sharp frequency selectivity of CN neurons at moderate to high sound pressure levels, particularly in background noise. In this fashion lateral suppressive mechanisms potentially enhance the representation of spectral information on the basis of place/rate information relative to that in the auditory nerve under noisy background conditions. 5. Lateral suppressive mechanisms probably underlie the dynamic range shift seen in the presence of a simultaneously presented noise. This mechanism may be crucial for preserving the ability to perceive signals in a noisy background.

We report on the anatomical and physiological features of globular bushy cells in the posterior division of the anteroventral cochlear nucleus based on the characteristics of 20 cells from this population. Each of these cells was recorded from and characterized intracellularly and/or extracellularly, injected with horseradish peroxidase, and studied at the light and/or electron microscopic level. Intracellular records from the vicinity of the globular bushy cell body displayed large, fast synaptic potentials, and in some instances a larger presumed action potential both in silence and during short tone stimulation. Intraaxonal recordings displayed large action potentials in addition to small, fast potentials, which evidence indicates may be the decrementally conducted subthreshold synaptic potentials. Both recording situations indicated that these auditory nerve inputs need not be suprathreshold. Bushy cells with high characteristic frequencies (CFs greater than 3 kHz) typically showed primary-like-with-notch responses to short tones at CF or on-type L responses if the sustained level of discharge after the notch was not as robust. Low-CF bushy cells phase-locked after a well-timed onset spike. Light microscopic anatomy revealed a typically oval cell body giving rise to one or two primary dendrites that branched profusely and an axon that gave off no collaterals within the cochlear nucleus before entering the trapezoid body. Electron microscopic analysis showed a high concentration of large, round, vesicle-containing terminals on the cell body and primary dendrite while the population of terminals on the initial segment and sparsely covered distal dendrites was made up mostly of flat and pleomorphic vesicle-containing terminals.

The physiology and morphology of fusiform cells in the dorsal cochlear nucleus were studied using extracellular and intracellular recording and intracellular injection of horseradish peroxidase. Fusiform cells displayed a variety of responses to tone pips presented at the characteristic frequency; most often these cells exhibited the pauser/buildup pattern defined in earlier studies. The response pattern of each neuron was dependent on frequency and sound-pressure level. Tone pips evoked short-lasting depolarizations of about 10 mV and long-lasting hyperpolarizations of about 10 mV in cells whose resting potentials were -50 to -65 mV. The time courses of both the excitation and the inhibition depended on frequency and sound-pressure level. Generally the depolarization was sustained for the duration of the tone pip, whereas the hyperpolarization could last as long as 600 ms after the end of the tone pip. Often a neuron exhibited a sustained chopper pattern after microelectrode impalement. This was probably a result of a decrease in membrane potential which altered the relative effectiveness of the excitatory and inhibitory inputs. The large, bitufted fusiform cells had many apical dendrites, which branched one to five times and were covered with spines, and fewer basal dendrites, which exhibited little branching and had few appendages. The morphology of fusiform cells varied systematically as a function of location within the dorsal cochlear nucleus. Response patterns for tone pips were not exclusive to individual cell types as two nonfusiform cells were found to exhibit a buildup pattern. Axons of injected neurons left the nucleus via the dorsal acoustic stria and 14 of 15 had collaterals within the dorsal cochlear nucleus.

We report on the anatomy and physiology of three fusiform cells in the dorsal cochlear nucleus (DCN) of the cat. The extra- and intracellular responses of these cells to pure tones showed features typical of the cell type. Peristimulus time histograms (PSTHs) were usually of the pauser or buildup configuration with chopping behavior noted in certain instances. Intracellular records during stimulus presentations revealed sustained depolarizations for the duration of the tone followed by a prolonged after-hyperpolarization (AHP). On rare occasions, a hyperpolarization corresponding to the pause region of the PSTH was noted. Occasionally, a stimulus-induced depolarization would be maintained after stimulus offset. Rebound excitation was also observed after the AHP. Morphologically, all three cells showed the standard fusiform cell features at the light microscopic level. The cell body gave rise to apical and basal dendritic trees. The apical tree branched frequently and displayed numerous spines distally. The basal tree had fewer branches and fewer, more irregular appendages. The axon originated from the cell body and gave rise to one or more collaterals before leaving the nucleus via the dorsal acoustic stria (DAS). At the electron microscopic (EM) level, the axon collaterals may terminate on a variety of cell types in the DCN, including fusiform cells. Their vesicles are round and the terminals closely resemble many unlabeled terminals seen on the cell body and apical and basal dendrites of our labeled fusiform cells. Terminals containing round vesicles, believed to be eighth nerve terminals, were found, with one exception, only on the basal dendrites. The spine-laden, distal apical dendrites received primarily terminals containing round vesicles, presumed to originate from the unmyelinated axons of granule cells. The cell body and unmyelinated initial segment received mostly terminals containing pleomorphic and flat vesicles, which also made up a large percentage of the dendritic input. Some relevant correlations, between the distribution of synaptic terminals and the observed physiology, may be possible.

Recent measurements obtained with a variety of techniques have extended von Békésy's observations of cochlear-partition mechanics including the traveling-wave pattern and the frequency-place relation. Whereas the cochlear fiber has been shown to be sharper than expected, on the basis of Békésy's results, it apparently is not sharp enough to account for the frequency selectivity observed in auditory nerve fibers. The main remaining question is whether the vibration of the basilar membrane is linear or not. Steady-state nonlinearities that disappear rapidly upon death, transient nonlinear response, and two-tone suppression have been observed in the mid-frequency range in one animal species. Whether the linearity-nonlinearity controversy arises from a species difference or a frequency-place difference remains to be resolved.

The responses of single auditory nerve (AN) fibers in the cat were recorded in response to 25 ms tone pips. Peristimulus time histograms (PSTH) of discharge patterns recorded from fibers with high spontaneous rates (high SRs), show that the discharge rate rapidly adapts to a much lower steady-state level over a 15 ms period with shorter times for units with best frequencies (CFs) greater than 5 kHz. The PSTHs of auditory nerve fibers with low SRs do not show this pattern of rapid adaptation. Differences between the high and low SR populations include higher thresholds, better tuning, and longer latency in the low SR population. The peak-to-steady-state discharge ratio is an increasing function of SR and CF; it varies from 1.0 for fibers with SR = 0 to over 8 for fibers with high SRs and CFs near 10 kHz. This ratio increases with increasing stimulus intensity and stimulus recovery time. The high SR population shows a number of responses to transients which are weak or absent in the low SR population. Increasing the recovery time shortened the latency of both high and low SR AN fibers by as much as 1 ms. A number of other response properties of AN fibers are also reported that are important when interpreting the responses of cochlear nucleus neurons to tone pips.

A quantitative model of the relative motion between the tectorial membrane and reticular lamina of the mammalian cochlea is presented. The model is proposed for the stapes side of the region of maximum deflection during sinusoidal excitation. Based on familiar concepts, the model assumes that basilar membrane deflection causes a sliding motion between the tectorial membrane and the reticular lamina. Equations for the motion between opposing points on these two structures are derived in terms of various cochlear dimensions and of the basilar‐membrane displacement. Average values of these dimensions, obtained from eight cat ears, were used to achieve numerical answers.