Binaural Response Properties of Low-Frequency Neurons in the Gerbil Dorsal Nucleus of the Lateral Lemniscus

2006 ◽  
Vol 96 (3) ◽  
pp. 1425-1440 ◽  
Author(s):  
Ida Siveke ◽  
Michael Pecka ◽  
Armin H. Seidl ◽  
Sylvie Baudoux ◽  
Benedikt Grothe
Keyword(s):  
Low Frequency ◽  
Superior Olivary Complex ◽  
Suitable Model ◽  
Medial Superior Olive ◽  
Lateral Lemniscus ◽  
Auditory Midbrain ◽  
Response Properties ◽  
Superior Olive ◽  
Dorsal Nucleus ◽  
Anatomical Evidence

Differences in intensity and arrival time of sounds at the two ears, interaural intensity and time differences (IID, ITD), are the chief cues for sound localization. Both cues are initially processed in the superior olivary complex (SOC), which projects to the dorsal nucleus of the lateral lemniscus (DNLL) and the auditory midbrain. Here we present basic response properties of low-frequency (<2 kHz) DNLL neurons and their binaural sensitivity to ITDs and IIDs in the anesthetized gerbil. We found many neurons showing binaural properties similar to those reported for SOC neurons. IID-properties were similar to that of the contralateral lateral superior olive (LSO). A majority of cells had an ITD sensitivity resembling that of either the ipsilateral medial superior olive (MSO) or the contralateral LSO. A smaller number of cells displayed intermediate types of ITD sensitivity. In neurons with MSO-like response ITDs that evoked maximal discharges were mostly outside of the range of ITDs the gerbil naturally experiences. The maxima of the first derivative of their ITD-functions (steepest slope), however, were well within the physiological range of ITDs. This finding is consistent with the concept of a population rather than a place code for ITDs. Moreover, we describe several other binaural properties as well as physiological and anatomical evidence for a small but significant input from the contralateral MSO. The large number of ITD-sensitive low-frequency neurons implicates a substantial role for the DNLL in ITD processing and promotes this nucleus as a suitable model for further studies on ITD-coding.

Response properties of single units in the dorsal nucleus of the lateral lemniscus and paralemniscal zone of an echolocating bat

1993 ◽  
Vol 69 (3) ◽  
pp. 842-859 ◽  
Author(s):  
E. Covey
Keyword(s):  
Sound Level ◽  
Single Units ◽  
Superior Olivary Complex ◽  
Inhibitory Input ◽  
Gamma Aminobutyric Acid ◽  
Lateral Lemniscus ◽  
Response Properties ◽  
Binaural Interaction ◽  
Dorsal Nucleus ◽  
Interaural Level Differences

1. Connectional evidence suggests that the dorsal nucleus of the lateral lemniscus (DNLL) and the paralemniscal zone (PL) function as centers for binaural analysis interposed between the superior olivary complex and the midbrain. In addition, the DNLL is known to be a major source of inhibitory input to the midbrain. The aim of this study was to characterize the response properties of neurons in DNLL and PL of the echolocating bat Eptesicus fuscus, a species that utilizes high-frequency hearing and that might be expected to have a large proportion of neurons responsive to interaural differences in sound level. 2. Auditory stimuli were presented monaurally or binaurally to awake animals, and responses of single units were recorded extra-cellularly with the use of glass micropipettes. 3. Below the ventrolateral border of the inferior colliculus is a region that contains large gamma-aminobutyric acid-positive neurons. On the basis of its immunohistochemical reactivity, this entire region could be considered as DNLL. However, within the area, there was an uneven distribution of binaural responses. Caudally, binaural neurons made up 84% (41/49) of those tested, but rostrally only 29% (6/21). For this reason the rostral area is considered as a separate functional subdivision and referred to as the dorsal paralemniscal zone (DPL). PL is located ventral to DPL and medial to the intermediate and ventral nuclei of the lateral lemniscus; in PL 88% (14/16) of neurons were binaural. 4. Most neurons responded only to a contralateral stimulus when sounds were presented monaurally. Out of 49 neurons in DNLL, 42 responded only to a contralateral sound, 1 responded only to an ipsilateral sound, and 6 responded to sound at either ear. In the DPL, all of the 21 neurons tested responded to a contralateral sound and none to an ipsilateral sound. Out of 16 neurons in the PL, 11 responded only to a contralateral sound, 1 responded only to an ipsilateral sound, and 4 responded to sound at either ear. 5. When sounds were presented at both ears simultaneously, several different patterns of binaural interaction occurred. The most common pattern was suppression of the response to sound at one ear by sound at the other ear. In DNLL, 57% (28/49) of neurons showed this type of binaural interaction. Another 10% (5/49) showed facilitation at some interaural level differences and suppression at others, and another 10% (5/49) showed facilitation at some interaural level differences but no suppression.(ABSTRACT TRUNCATED AT 400 WORDS)

Spectral Composition of Concurrent Noise Affects Neuronal Sensitivity to Interaural Time Differences of Tones in the Dorsal Nucleus of the Lateral Lemniscus

2007 ◽  
Vol 98 (5) ◽  
pp. 2705-2715 ◽  
Author(s):  
Ida Siveke ◽  
Christian Leibold ◽  
Benedikt Grothe
Keyword(s):  
White Noise ◽  
Response Rate ◽  
Spectral Composition ◽  
Low Frequency ◽  
Maximal Response ◽  
Lateral Lemniscus ◽  
Interaural Time Differences ◽  
Binaural Cues ◽  
Dorsal Nucleus ◽  
Monaural Stimulation

We are regularly exposed to several concurrent sounds, producing a mixture of binaural cues. The neuronal mechanisms underlying the localization of concurrent sounds are not well understood. The major binaural cues for localizing low-frequency sounds in the horizontal plane are interaural time differences (ITDs). Auditory brain stem neurons encode ITDs by firing maximally in response to “favorable” ITDs and weakly or not at all in response to “unfavorable” ITDs. We recorded from ITD-sensitive neurons in the dorsal nucleus of the lateral lemniscus (DNLL) while presenting pure tones at different ITDs embedded in noise. We found that increasing levels of concurrent white noise suppressed the maximal response rate to tones with favorable ITDs and slightly enhanced the response rate to tones with unfavorable ITDs. Nevertheless, most of the neurons maintained ITD sensitivity to tones even for noise intensities equal to that of the tone. Using concurrent noise with a spectral composition in which the neuron's excitatory frequencies are omitted reduced the maximal response similar to that obtained with concurrent white noise. This finding indicates that the decrease of the maximal rate is mediated by suppressive cross-frequency interactions, which we also observed during monaural stimulation with additional white noise. In contrast, the enhancement of the firing rate to tones at unfavorable ITD might be due to early binaural interactions (e.g., at the level of the superior olive). A simple simulation corroborates this interpretation. Taken together, these findings suggest that the spectral composition of a concurrent sound strongly influences the spatial processing of ITD-sensitive DNLL neurons.

Differential Response Properties to Amplitude Modulated Signals in the Dorsal Nucleus of the Lateral Lemniscus of the Mustache Bat and the Roles of GABAergic Inhibition

1997 ◽  
Vol 77 (1) ◽  
pp. 324-340 ◽  
Author(s):  
Lichuan Yang ◽  
George D. Pollak
Keyword(s):  
Phase Locking ◽  
Modulation Frequency ◽  
Tone Burst ◽  
Differential Response ◽  
Gabaergic Inhibition ◽  
Lateral Lemniscus ◽  
Response Properties ◽  
Dorsal Nucleus ◽  
Modulated Signals ◽  
Onset Response

Yang, Lichuan and George D. Pollak. Differential response properties to amplitude modulated signals in the dorsal nucleus of the lateral lemniscus of the mustache bat and the roles of GABAergic inhibition. J. Neurophysiol. 77: 324–340, 1997. We studied the phase-locking of 89 neurons in the dorsal nucleus of the lateral lemniscus (DNLL) of the mustache bat to sinusoidally amplitude modulated (SAM) signals and the influence that GABAergic inhibition had on their response properties. Response properties were determined with tone bursts at each neuron's best frequency and then with a series of SAM signals that had modulation frequencies ranging from 50–100 to 800 Hz in 100-Hz steps. DNLL neurons were divided into two principal types: sustained neurons (55%), which responded throughout the duration of the tone burst, and onset neurons (45%), which responded only at the beginning of the tone burst. Sustained and onset neurons responded differently to SAM signals. Sustained neurons responded with phase-locked discharges to modulation frequencies ≤400–800 Hz. In contrast, 70% of the onset neurons phase-locked only to low modulation frequencies of 100–300 Hz, whereas 30% of the onset neurons did not phase-lock to any modulation frequency. Signal intensity differentially affected the phase-locking of sustained and onset neurons. Sustained neurons exhibited tight phase-locking only at low intensities, 10–30 dB above threshold. Onset neurons, in contrast, maintained strong phase-locking even at relatively high intensities. Blocking GABAergic inhibition with bicuculline had different effects on the phase-locking of sustained and onset neurons. In sustained neurons, there was an overall decline in phase-locking at all modulation frequencies. In contrast, 70% of the onset neurons phase-locked to much higher modulation frequencies than they did when inhibition was intact. The other 30% of onset neurons phase-locked to SAM signals, although they fired only with an onset response to the same signals before inhibition was blocked. In both cases, blocking GABAergic inhibition transformed their responses to SAM signals into patterns that were more like those of sustained neurons. We also propose mechanisms that could explain the differential effects of GABAergic inhibition on onset neurons that locked to low modulation frequencies and on onset neurons that did not lock to any SAM signals before inhibition was blocked. The key features of the proposed mechanisms are the absolute latencies and temporal synchrony of the excitatory and inhibitory inputs.

scholarly journals Differing Roles of Inhibition in Hierarchical Processing of Species-Specific Calls in Auditory Brainstem Nuclei

2005 ◽  
Vol 94 (6) ◽  
pp. 4019-4037 ◽  
Author(s):  
Ruili Xie ◽  
John Meitzen ◽  
George D. Pollak
Keyword(s):  
Auditory Brainstem ◽  
Lateral Lemniscus ◽  
Response Properties ◽  
Hierarchical Processing ◽  
Tuning Curves ◽  
Neuronal Populations ◽  
Dorsal Nucleus ◽  
Brainstem Nuclei ◽  
Communication Calls ◽  
Species Specific

Here we report on response properties and the roles of inhibition in three brain stem nuclei of Mexican-free tailed bats: the inferior colliculus (IC), the dorsal nucleus of the lateral lemniscus (DNLL) and the intermediate nucleus of the lateral lemniscus (INLL). In each nucleus, we documented the response properties evoked by both tonal and species-specific signals and evaluated the same features when inhibition was blocked. There are three main findings. First, DNLL cells have little or no surround inhibition and are unselective for communication calls, in that they responded to ∼97% of the calls that were presented. Second, most INLL neurons are characterized by wide tuning curves and are unselective for species-specific calls. The third finding is that the IC population is strikingly different from the neuronal populations in the INLL and DNLL. Where DNLL and INLL neurons are unselective and respond to most or all of the calls in the suite we presented, most IC cells are selective for calls and, on average, responded to ∼50% of the calls we presented. Additionally, the selectivity for calls in the majority of IC cells, as well as their tuning and other response properties, are strongly shaped by inhibitory innervation. Thus we show that inhibition plays only limited roles in the DNLL and INLL but dominates in the IC, where the various patterns of inhibition sculpt a wide variety of emergent response properties from the backdrop of more expansive and far less specific excitatory innervation.

Interaural time sensitivity in medial superior olive of cat

1990 ◽  
Vol 64 (2) ◽  
pp. 465-488 ◽  
Author(s):  
T. C. Yin ◽  
J. C. Chan
Keyword(s):  
Broad Band ◽  
Low Frequency ◽  
Sound Field ◽  
Phase Changes ◽  
Medial Superior Olive ◽  
Superior Olive ◽  
Band Noise ◽  
Interaural Phase ◽  
Combining Data ◽  
Monaural Stimulation

1. We studied the sensitivity of cells in the medial superior olive (MSO) of the anesthetized cat to variations in interaural phase differences (IPDs) of low-frequency tones and in interaural time differences (ITDs) of tones and broad-band noise signals. Our sample consisted of 39 cells histologically localized to the MSO. 2. All but one of the cells had characteristic frequencies less than 3 kHz, and 79% were sensitive to ITDs and IPDs. More than one-half (56%) of the cells responded to monaural stimulation of either ear, and both the binaural and monaural responses were highly phase locked. All of the cells that were sensitive to IPDs and monaurally driven by either ear responded in accord with that predicted by the coincidence model of Jeffress, as judged by comparisons of the phases at which the monaural and binaural responses occurred. The optimal IPDs were tightly clustered between 0.0 and 0.2 cycles. Most cells exhibited facilitation of the response at favorable ITDs and inhibition at unfavorable ITDs compared with the monaural responses. 3. Cells in the MSO exhibited characteristic delay, as judged by a linear relationship between the mean interaural phase and stimulating frequency. Characteristic phases were clustered near 0 indicating the most cells responded maximally when the two input tones were in phase. With the use of the binaural beat stimulus we found no differential selectivity for either the direction or speed of interaural phase changes. 4. The cells were also sensitive to ITDs of broad-band noise signals. The ITD curve in response to broad-band noise was similar to that predicted by the composite curve, which was calculated by linearly summating the tonal responses over the frequencies in the response area of the cell. Most (93%) of the peaks of the composite curves were between 0 and +400 microseconds, corresponding to locations in the contralateral sound field. Moreover, computer cross correlations of the monaural spike trains were similar to the ITD curve generated binaurally for both correlated and uncorrelated noise signals to the two ears. Thus our data suggest that the cells in the MSO behave much like cross-correlators. 5. By combining data from different animals and lcoating each cell on a standard MSO, we found evidence for a spatial map of ITDs across the anterior-posterior (A-P) axis of the MSO.(ABSTRACT TRUNCATED AT 400 WORDS)

Frequency-dependent interaural delays in the medial superior olive: implications for interaural cochlear delays

2011 ◽  
Vol 106 (4) ◽  
pp. 1985-1999 ◽  
Author(s):  
Mitchell L. Day ◽  
Malcolm N. Semple
Keyword(s):  
Interaural Time Difference ◽  
Superior Olivary Complex ◽  
Medial Superior Olive ◽  
Biophysical Parameters ◽  
Tone Frequency ◽  
Frequency Dependent ◽  
Superior Olive ◽  
Interaural Phase ◽  
Cochlear Delays ◽  
Delay Component

Neurons in the medial superior olive (MSO) are tuned to the interaural time difference (ITD) of sound arriving at the two ears. MSO neurons evoke a strongest response at their best delay (BD), at which the internal delay between bilateral inputs to MSO matches the external ITD. We performed extracellular recordings in the superior olivary complex of the anesthetized gerbil and found a majority of single units localized to the MSO to exhibit BDs that shifted with tone frequency. The relation of best interaural phase difference to tone frequency revealed nonlinearities in some MSO units and others with linear relations with characteristic phase between 0.4 and 0.6 cycles. The latter is usually associated with the interaction of ipsilateral excitation and contralateral inhibition, as in the lateral superior olive, yet all MSO units exhibited evidence of bilateral excitation. Interaural cochlear delays and phase-locked contralateral inhibition are two mechanisms of internal delay that have been suggested to create frequency-dependent delays. Best interaural phase-frequency relations were compared with a cross-correlation model of MSO that incorporated interaural cochlear delays and an additional frequency-independent delay component. The model with interaural cochlear delay fit phase-frequency relations exhibiting frequency-dependent delays with precision. Another model of MSO incorporating inhibition based on realistic biophysical parameters could not reproduce observed frequency-dependent delays.

scholarly journals Physiological and anatomical investigation of the auditory brainstem in the Fat-tailed Dunnart (Sminthopsis crassicaudata)

2019 ◽  
Author(s):  
Andrew Garrett ◽  
Virginia Lannigan ◽  
Nathanael Yates ◽  
Jennifer Rodger ◽  
Wilhelmina Mulders
Keyword(s):  
Auditory System ◽  
Mammalian Species ◽  
Auditory Brainstem ◽  
Auditory Brainstem Responses ◽  
Superior Olivary Complex ◽  
Medial Superior Olive ◽  
Superior Olive ◽  
Medial Nucleus ◽  
Sminthopsis Crassicaudata ◽  
Nissl Stain

The fat-tailed Dunnart (Sminthopsis crassicaudata) is a small (10-20g) native marsupial endemic to the south west of Western Australia. Currently little is known about the auditory capabilities of the dunnart, and of marsupials in general. Consequently, this study sought to investigate several electrophysiological and anatomical properties of the dunnart auditory system. Auditory brainstem responses (ABR) were recorded to brief (5ms) tone pips at a range of frequencies (4-47.5 kHz) and intensities to determine auditory brainstem thresholds. The dunnart ABR displayed multiple distinct peaks at all test frequencies, similar to other mammalian species. ABR showed the dunnart is most sensitive to higher frequencies increasing up to 47.5 kHz. Morphological observations (Nissl stain) revealed that the auditory structures thought to contribute to the first peaks of the ABR were all distinguishable in the dunnart. Structures identified include the dorsal and ventral subdivisions of the cochlear nucleus, including a cochlear nerve root nucleus as well as several distinct nuclei in the superior olivary complex, such as the medial nucleus of the trapezoid body, lateral superior olive and medial superior olive. This study is the first to show functional and anatomical aspects of the lower part of the auditory system in the Fat-tailed Dunnart.

Interaural time and intensity coding in superior olivary complex and inferior colliculus of the echolocating bat Molossus ater

1985 ◽  
Vol 53 (1) ◽  
pp. 89-109 ◽  
Author(s):  
G. Harnischfeger ◽  
G. Neuweiler ◽  
P. Schlegel
Keyword(s):  
Inferior Colliculus ◽  
Stimulus Frequency ◽  
Stimulus Onset ◽  
Time Difference ◽  
Superior Olivary Complex ◽  
Inhibitory Input ◽  
Medial Superior Olive ◽  
Transient Time ◽  
Interaural Time Differences ◽  
Superior Olive

Single-unit responses to tonal stimulation with interaural disparities were recorded in the nuclei of the superior olivary complex (SOC) and the central nucleus of the inferior colliculus (ICC) of the echolocating bat, Molossus ater. Seventy-six units were recorded from the ICC and 74 from the SOC; of the SOC units, 31 were histologically verified in the medial superior olive (MSO), 10 in the lateral superior olive (LSO), and 33 in unidentified areas of the SOC. Best frequencies (BFs) of the units ranged from 10.3 to 89.6 kHz, and Q10 dB values ranged from 2 to 70 dB. Most ICC neurons responded phasically to stimulus onset and were either inhibitory/excitatory [I/E; (53)] or excitatory/excitatory [E/E; (21)] units. In the MSO, 23 units responded tonically and 7 phasically on, 18 were E/E or E/OF (facilitatory for other input) units, and 11 were I/E neurons. All LSO neurons responded in a "chopper" fashion, and the binaural neurons were E/I units. In E/E units the excitatory response to binaural stimulation was frequently larger than the sum of the monaurally evoked responses. Many neurons with E/I or I/E inputs had very steep binaural impulse-count functions and were sensitive to small interaural intensity differences. Twenty-eight units (24%) responded with a change in firing rate of at least 20% to interaural time differences of +/- 500 microseconds. Within this sample, 11 units (8 from ICC, 2 from MSO, and 1 from SOC) were sensitive to interaural time differences of only +/- 50 microseconds. Of these 11 units, 10 were I/E units responding phasically only to stimulus onset and were also sensitive to intensity differences (delta I), being suppressed completely by the inhibitory input over a delta I range of 20 dB or less. Of 117 units tested in the ICC and SOC nuclei, 86 units (76%) were not sensitive to interaural time disparities within +/- 500 microseconds. Because the BFs of these units sensitive to interaural transient time differences (delta t) ranged between 18 and 90 kHz, responses were elicited by pure tones, and responses did not change periodically with the period equal to that of the stimulus frequency, we conclude that the neurons reacted to interaural differences of stimulus-onset time (transient time difference) but not to phase differences (ongoing time difference). Sensitivity to interaural time differences was also correlated with interaural intensity differences.(ABSTRACT TRUNCATED AT 400 WORDS)

Functional organization of lateral cell groups of cat superior olivary complex

1977 ◽  
Vol 40 (2) ◽  
pp. 296-318 ◽  
Author(s):  
C. Tsuchitani
Keyword(s):  
Superior Olivary Complex ◽  
Maximum Output ◽  
Medial Superior Olive ◽  
Superior Olive ◽  
Response Characteristics ◽  
Cell Groups ◽  
Discharge Patterns ◽  
Intensity Functions ◽  
Contralateral Stimulus ◽  
Stimulation Of

1. Single-unit discharges to auditory stimuli were recorded extracellularly from superior olivary complex (SOC) units located lateral to the medial superior olive. Stimuli consisted of monaurally or binaurally presented tone bursts. The response measures obtained were effective ear, nature of effect, stimulus-frequency representation, maximum output, latency of response, and temporal pattern of tone burst-elicited discharges. Electrolytic marks were made at the unit studied or at the end of the electrode tract and in the medial superior olive. Following each experiment the locations of the units studied were determined histologically. An atlas of the laterally located SOC cell groups was developed to permit classification of units on the basis of localization within cell groups. Units were also classified according to the effects of stimulating the two ears. 2. All SOC units located lateral to the medial superior olive were excited by stimulation of the ipsilateral ear. Stimulation of the contralateral ear either excited, inhibited, had no effect, or had a potentiating effect on the discharges elicited by stimulating the ipsilateral ear. 3. Most lateral superior olivary (LSO) units were inhibited by contralateral stimulation, were narrowly tuned, produced low to high levels of maximum output, had short latencies, and produced regular discharge patterns characterized by chopper PST histograms with narrow initial peaks. 4. Most units within the caudal margins of the LSO (pLSO) were not affected or were inhibited by a contralateral stimulus; many were broadly tuned and exhibited intensity functions with large dynamic range and low slope. These units also had long latencies and produced chopper PST histograms with wide initial peaks. 5. Most units located dorsal to the LSO (DPO and DLPO) were not affected by the contralateral stimulus, were narrowly tuned, produced moderate levels of maximum discharge, had long latencies, and produced chopper PST histograms with wide initial peaks. 6. Units located ventral to the LSO appeared to have response characteristics related to unit location. Most units below the ventral hilum of the LSO (VLPO) were inhibited by the contralateral stimulus and many were broadly tuned VLPO units produced wide or poorly defined narrow-chopper discharge patterns and intensity functions with high maximum output. Most units located ventral to the lateral loop of the LSO (LNTB) were not affected by the contralateral stimulus and had response characteristics that may be related to the rostrocaudal location of the unit. 7. The cell groups located dorsal and ventral to the LSO were tonotopically organized with low-frequency-sensitive units located laterally and high-frequency-sensitive units located medially. The units located along the caudal margins of the LSO had a tonotopic organization similar to that of the LSO.

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