Donal G. Sinex

Acute spiral ganglion lesions change the tuning and tonotopic organization of cat inferior colliculus neurons

Many studies have reported plastic changes in central auditory frequency organization after chronic cochlear lesions. These studies employed mechanical, acoustic or drug-induced disruptions of restricted regions of the organ of Corti that permanently alter its tuning and sensitivity and require an extended recovery period before central effects can be measured. In this study, mechanical lesions were made to 1 mm sectors of the spiral ganglion (SG). These lesions remove a restricted portion of the cochlear output, but leave the organ of Corti and basilar membrane intact. Multiunit mapping assessed the pre- and post-lesion tonotopic organization of the inferior colliculus (IC). Immediately after SG lesions, IC neurons previously tuned to the lesion frequencies became less sensitive to those frequencies but more sensitive to lesion edge frequencies, resulting in a shift in their characteristic frequencies (CFs). Notches in the excitatory response areas at frequencies corresponding to the lesion frequencies and expansion of spatial tuning curves were also observed. CFs of neurons tuned to unlesioned frequencies were unchanged. These results suggest that plastic changes similar to those observed after long survival times in previous studies require little or no experience and occur within minutes to hours following the lesion.

Responses of inferior colliculus neurons to harmonic and mistuned complex tones

Responses of inferior colliculus neurons to simplified stimuli that may engage mechanisms that contribute to auditory scene analysis were obtained. The stimuli were harmonic complex tones, which are heard by human listeners as single sounds, and the same tones with one component mistuned, which are heard as two separate sounds. The temporal discharge pattern elicited by a harmonic complex tone usually resembled the same neurons response to a pure tone. In contrast, tones with a mistuned component elicited responses with distinctive, stereotypical temporal patterns that were not obviously related to the stimulus waveform. For a particular stimulus configuration, the discharge pattern was similar across neurons with different pure-tone frequency selectivity. A computational model that compared response envelopes across multiple narrow bands successfully reproduced the stereotypical response patterns elicited by different stimulus configurations. The results suggest that mistuning created a temporally synchronous distributed representation of the mistuned component that could be identified by higher auditory centers in the presence of the ongoing response produced by the remaining components; this kind of representation might facilitate the identification of individual sound sources in complex acoustic environments.

Frequency organization and cellular lamination in the medial geniculate body of the rabbit

Cellular laminae within the tonotopically organized ventral division of the medial geniculate body (MGV) of the cat have been proposed as the anatomical substrate for physiologically defined isofrequency contours. In most species, the laminae are not visible with routine Nissl stains, but are defined by the dendritic fields of principal cells and the terminal arbors of afferents arising from the inferior colliculus. In the present study, we have used the rabbit to directly examine the relationship between the laminar and tonotopic organization of the MGV. Best frequency maps of the MGV in anesthetized adult New Zealand white rabbits were generated from cluster responses recorded at 30-100 microm intervals to randomly presented tone bursts. Parallel vertical penetrations, roughly perpendicular to the laminae, revealed a low-to-high frequency gradient within the MGV. Non-laminated regions of the ventral division, generally found at the rostral or caudal poles, did not demonstrate a systematic frequency gradient. In contrast to a predicted smooth gradient, best frequencies shifted in discrete steps across the axis of the laminae. A similar step-wise frequency gradient has been shown in the central nucleus of the inferior colliculus of the cat. It is proposed that the central laminated core of the MGV represents an efficient architecture for creating narrow frequency filters involved in fine spectral analysis.

Responses of auditory nerve fibers to harmonic and mistuned complex tones

Responses of auditory nerve fibers were obtained to harmonic complex tones in which single components could be mistuned. Human listeners hear the harmonic tones as single sounds, but the same tones with one component mistuned are heard as two separate sounds. Fourier analysis of the temporal discharge patterns indicated that auditory nerve fibers typically responded to one or two stimulus components near the fibers characteristic frequencies. At low stimulus levels, the discharge patterns could also exhibit low-frequency modulation that was produced by beating of two higher-frequency components. The same components were observed in the response spectra, whether those components were part of the original harmonic series or had been mistuned. The discharge patterns and response spectra were consistent with expectations based on previous studies of auditory nerve fibers with harmonic tones and other complex sounds. However, the discharge patterns differed dramatically from the discharge patterns elicited from inferior colliculus neurons by comparable stimuli.

Cell types and response properties of neurons in the ventral division of the medial geniculate body of the rabbit

Although there is evidence for multiple classes of thalamic relay neurons in the auditory thalamus, correlative anatomical and physiological studies are lacking. We have used the juxtacellular labeling technique, in conjunction with Nissl, Golgi, and immunocytochemical methods, to study the morphology and response properties of cells in the ventral division of the medial geniculate body of the rabbit. Single units in the ventral division of the medial geniculate body (MGV) were characterized extracellularly with monaural and binaural tone and noise bursts (100‐ to 250‐msec duration). Characterized units were filled with biocytin and visualized with an antibody enhanced diaminobenzidine reaction. A total of 31 neurons were physiologically characterized and labeled with the juxtacellular technique. Labeled neurons were fully reconstructed from serial sections by using a computer microscope system. Three subregions of the rabbit MGV were identified, each characterized by differences in Nissl architecture, calcium‐binding protein expression, and by the dendritic orientation of tufted relay neurons. In general, the dendritic fields of relay neurons were closely aligned with the cellular laminae. Qualitative and quantitative analyses revealed two types of presumptive relay neurons within the MGV. Type I cells had thick dendrites with a greater total volume and morphologically diverse appendages compared with the Type II cells whose dendrites were thin with a moderate number of small spines. Both classes were acoustically responsive and exhibited a variety of response patterns, including onset, offset, and sustained responses. In terms of binaural characteristics, most (ca. 53%) labeled neurons were of the EE type, with the remaining cells classified as EO (27%) or EI (20%) response types. Two types of presumptive interneurons were also seen: bipolar neurons with large dendritic fields and a small neurogliaform variety. Cell types and dendritic orientation within the MGV are discussed in terms of the physiological organization of the rabbit auditory thalamus. J. Comp. Neurol. 445:78–96, 2002.

Electrophysiological responses of cochlear root neurons.

Cochlear root neurons (CRNs) are second-order neurons interspersed among the fibers of the cochlear nerve in certain rodents. They project, among other nuclei, mainly to the pontine reticular nucleus, and participate in the acoustic startle response (ASR), a short-latency motor reflex initiated by sudden intense sounds. The sound-evoked activity of CRNs has not previously been described. Here we describe extracellular responses of CRNs located in the infranuclear portion of the cochlear nerve root. CRNs exhibited secure responses to tone bursts, with first-spike latencies of approximately 2.2 ms. The characteristic frequencies of the recorded CRNs were about 30 kHz, and the best-characterized CRN had a threshold of 10 dB sound pressure level and sharpness of tuning similar to that of cochlear nerve fibers. The peristimulus time histograms were primary-like with notch. The observed response properties were consistent with the suggestion that CRNs provide the short-latency acoustic input to the reticular formation that leads to an ASR.

Responses of chinchilla inferior colliculus neurons to amplitude-modulated tones with different envelopes.

Responses of single neurons in the inferior colliculus of the chinchilla to amplitude-modulated tones were obtained. In one condition, the modulating waveform was a low-frequency sinusoid (SAM tone). In the other, the modulator was a trapezoid with fixed parameters, used to create trains of brief tone bursts presented at various repetition rates (TRAM tone). Modulation frequency (or repetition rate) was varied over the range from 10 to 200 Hz. Many individual neurons exhibited strong selectivity for modulator type. Neurons with pauser discharge patterns to steady-state tones usually exhibited greater responsiveness to SAM tones than to TRAM. In contrast, neurons that responded transiently to steady-state tones usually exhibited greater responsiveness to TRAM tones than to SAM. Neurons with sustained responses to steady-state tones responded strongly to both types of modulated tones. The selectivity for modulator type suggests that transient neurons may play a different functional role in the representation of envelopes than do other types of neurons.

Responses of inferior colliculus neurons to SAM tones located in inhibitory response areas

In order to examine the effect of inhibition on processing auditory temporal information, responses of single neurons in the inferior colliculus of the chinchilla to sinusoidally amplitude-modulated (SAM) tones alone and the presence of a steady-state tone were obtained. The carrier frequency of the SAM tone was either the characteristic frequency (CF) or a frequency in the inhibitory response area of a studied neuron. When the carrier frequency was set to the neurons CF, neurons responded in synchrony to the SAM-tone envelope, as expected. When the carrier frequency was set to a frequency at which pure tones produced inhibition, SAM tones elicited little or no response, also as expected. However, when the same SAM tone was paired with a pure tone whose frequency was set to the neurons CF, responses synchronized to the SAM tone envelope were obtained. These modulated responses were typically one-half cycle out-of-phase with the response to the SAM tone at CF, suggesting that they arose from cyclic inhibition and release from inhibition by the SAM tone. The results demonstrate that the representation of temporal information by inferior colliculus neurons is influenced by temporally-patterned inhibition arising from locations remote from CF.

Effects of interaural time differences on the responses of chinchilla inferior colliculus neurons to consonant-vowel syllables

The responses of 100 inferior colliculus neurons to syllables differing in voice onset time (VOT) presented binaurally were studied. As in a previous study of monaural responses (Chen et al., 1996), the responses consisted of 1-3 response components, referred to as release responses, VOT responses or vowel responses. The discharge rate of all response components could vary cyclically with the interaural time difference (ITD). The maximal rate often occurred at an ITD around +0.2 ms (contralateral ear leading). Response frequencies (RF) based on the periodicity of the delay curves varied with the characteristic frequency (CF) and VOT. RF also varied across response components. Overall, RF was correlated with the most effective frequency, the spectral component with the highest amplitude, relative to the tuning curve. VOT response latency for a given syllable could change by a few ms with ITD, but those changes were small, relative to the range of latencies observed over the entire range of VOTs. Changes in ITD produced large changes in the overall shape of the peristimulus time histogram. There was no relation between the histogram shape and perceptual consonant categories.

Anatomical localization of electrophysiological recording sites by co-ordinate transformation

A method for estimating the anatomical locations of the units recorded in electrophysiological mapping experiments is described. A total of three locations must be marked by dye injections or electrolytic lesions and identified in tissue sections. From those locations, equations are derived to translate, scale, and rotate the three-dimensional co-ordinates of the recording sites, so that they are correct for a second, three-dimensional co-ordinate system based on the anatomy of the mapped structure. There is no limit to the number of recording sites that can be localized. This differs from methods that require a dye injection or lesion to be made at the exact location at which a particular unit was recorded. The accuracy of the transformed co-ordinates is limited by the accuracy with which the co-ordinates can be measured: in test measurements and in the experiments for which this algorithm was developed, the computed co-ordinates were typically accurate to within 100 microns or less.