Low-frequency neurons in the lateral superior olive exhibit phase-sensitive binaural inhibition

1991 ◽  
Vol 65 (3) ◽  
pp. 598-605 ◽  
Author(s):  
P. G. Finlayson ◽  
D. M. Caspary
Keyword(s):  
Discharge Rate ◽  
Low Frequency ◽  
Lateral Superior Olive ◽  
Superior Olive ◽  
Total Inhibition ◽  
Interaural Phase ◽  
Phase Sensitive ◽  
Evoked Activity ◽  
Discharge Patterns ◽  
Contralateral Stimulus

1. Responses of low characteristic frequency (CF) neurons in the lateral limb of the lateral superior olive (LSO) of chinchilla and rat to binaural stimuli at various interaural phase and intensity differences were examined and compared to responses from previous studies of high CF neurons. 2. Ninety-six LSO neurons from chinchillas and 10 LSO neurons from rats with CFs less than 1,200 Hz were characterized. The majority of these neurons displayed phase-locked tone-evoked temporal discharge patterns to ipsilateral CF stimuli. 3. Similar to high-CF LSO neurons, low-CF LSO neurons were excited by ipsilateral stimuli and inhibited by contralateral stimuli, with discharge rate sensitive to interaural intensity differences (IID). Discharge rate increased as ipsilateral intensity was increased and decreased as contralateral stimulus intensity was increased. 4. Binaural inhibition, inhibition of ipsilaterally evoked activity by contralateral stimuli, was dependent on interaural phase differences (IPD) in the majority of low-CF LSO neurons. Responses of phase-sensitive neurons to binaural stimuli often varied with 90 or 180 degrees changes in IPD from total inhibition to a facilitated response when compared to responses to control ipsilateral stimuli alone. 5. In summary, like high-CF LSO neurons, LSO neurons with low CFs (less than 1,200 Hz) were ipsilaterally excited and contralaterally inhibited (EI) and were sensitive to IID. Unlike most high-CF EI LSO neurons, which are not responsive when the azimuth of the stimulus is directly in front of or directly behind the animal, many low-CF LSO neurons are responsive to these stimuli.(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals Discharge patterns in the lateral superior olive of decerebrate cats

2012 ◽  
Vol 108 (7) ◽  
pp. 1942-1953 ◽  
Author(s):  
Nathaniel T. Greene ◽  
Kevin A. Davis
Keyword(s):  
Discharge Rate ◽  
Full Range ◽  
Stimulus Onset ◽  
Lateral Superior Olive ◽  
Superior Olive ◽  
Shape Adaptation ◽  
Discharge Patterns ◽  
Decerebrate Cats ◽  
Sustained Discharge ◽  
Initial Peak

Anatomical and pharmacological studies have shown that the lateral superior olive (LSO) receives inputs from a number of sources and that LSO cells can alter the balance of their own excitatory and inhibitory drive. It is thus likely that the ongoing sound-evoked responses of LSO cells reflect a complex interplay of excitatory and inhibitory events, which may be affected by anesthesia. The goal of this study was to characterize the temporal discharge patterns of single units in the LSO of unanesthetized, decerebrate cats in response to long-duration ipsilateral best-frequency tone bursts. A decision tree is presented to partition LSO units on the basis of poststimulus time histogram shape, adaptation of instantaneous firing rate as a function of time, and sustained discharge rate. The results suggest that LSO discharge patterns form a continuum with four archetypes: sustained choppers that show two or more peaks of activity at stimulus onset and little adaptation of rate throughout the response, transient choppers that undergo a decrease in rate that eventually stabilizes with time, primary-like units that display an initial peak of activity followed by a monotonic decline in rate to a steady-state value, and onset-sustained units that exhibit an initial peak of activity at stimulus onset followed by a low sustained activity. Compared with the chopper units, the nonchopper units tend to show longer first-spike latencies, lower peak firing rates, and more irregular sustained discharge patterns. Modeling studies show that the full range of LSO response types can be obtained from an underlying sustained chopper by varying the strength and latency of a sound-driven ipsilateral inhibition relative to that of excitation. Together, these results suggest that inhibition plays a major role in shaping the temporal discharge patterns of units in unanesthetized preparations.

Envelope coding in the lateral superior olive. II. Characteristic delays and comparison with responses in the medial superior olive

1996 ◽  
Vol 76 (4) ◽  
pp. 2137-2156 ◽  
Author(s):  
P. X. Joris
Keyword(s):  
Modulation Frequency ◽  
Small Sample ◽  
Spike Rate ◽  
Common Mechanism ◽  
Half Cycle ◽  
Medial Superior Olive ◽  
Lateral Superior Olive ◽  
Superior Olive ◽  
Binaural Interaction ◽  
Interaural Phase

1. Spike rates of cells in the cat's lateral superior olive (LSO) depend on interaural level differences (ILDs) and envelope interaural time differences (ITDs) of amplitude-modulated tones presented to both ears. We previously proposed that these sensitivities arise from a common mechanism, which is the IE binaural interaction (Inhibited by the contralateral and Excited by the ipsilateral ear). As a further test of that proposal and to gain a better understanding of the importance of this ITD-sensitivity, responses to monaural and binaural modulation are compared here over a range of modulation frequencies. 2. At low modulation frequencies, LSO-IE cells respond maximally when the envelopes of the amplitude-modulated stimuli at the two ears are out-of-phase by a half-cycle. This phase difference changes in a systematic way, which varies from cell to cell, when modulation frequency is increased. Mean interaural phase, measured over a range of modulation frequencies, was subjected to a characteristic delay analysis. Two measures were extracted: characteristic delay, which reflects differences in conduction delay between ipsi- and contralateral pathways, and characteristic phase, which reflects their sign of interaction. Most characteristic delays were within the physiological range of ITDs. There was a small bias toward positive delays, indicating a longer conduction time for the contralateral pathway. Characteristic phases were tightly distributed approximately 0.5 cycles, consistent with the proposed IE mechanism for ITD-sensitivity. 3. Increases in the modulation frequency of binaural stimuli beyond approximately 300 Hz consistently caused a profound decrease in average spike rate, as well as a decrease in the modulation of spike rate by ITD. The upper limit of ITD-sensitivity was 800 Hz. Sensitivity to envelope ITDs therefore is limited to a much lower range of frequencies than sensitivity to ITDs in fine-structure, e.g., as found in the medial superior olive (MSO), which operates up to several kilo Hertz. 4. A small sample of high-frequency EE cells (excited by both ears) in MSO also was tested with binaural amplitude-modulated stimuli. MSO-EE cells showed weak envelope ITD-sensitivity over a limited range of modulation frequencies. Consistent with the EE interaction, characteristic phases clustered approximately 0 cycles. 5. Mean interaural phase was compared with the phase of responses to monaural modulation. The difference between the ipsilateral and contralateral phases correlated well with the phase measured binaurally, both for LSO and MSO cells. 6. Many features of LSO-IE responses were mimicked by the simplest possible computer model, consisting of subtraction and rectification of low-pass filtered envelope waveforms. Differences between model and physiological results are suggestive of a temporal limitation in the binaural interaction that creates the ITD-sensitivity. 7. These results provide additional evidence for LSO ITD-sensitivity paralleling human psychophysical results. The stimulus boundaries within which ITD-sensitivity occurs suggest that it has a limited role in free-field conditions. It is traditionally thought that, to contribute to the perceived change in spatial location of a sound source, the LSO needs to show a change in overall firing rate summed across cells. This is achieved with small ILDs, but requires large ITDs, because the latter cue is less potent in single cells and has varied effects across cells by virtue of differences in characteristic delay.

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)

Comparative posthearing development of inhibitory inputs to the lateral superior olive in gerbils and mice

2011 ◽  
Vol 106 (3) ◽  
pp. 1443-1453 ◽  
Author(s):  
Jan Walcher ◽  
Benjamin Hassfurth ◽  
Benedikt Grothe ◽  
Ursula Koch
Keyword(s):  
Excitatory Input ◽  
Membrane Properties ◽  
Inhibitory Input ◽  
Synaptic Currents ◽  
Lateral Superior Olive ◽  
Superior Olive ◽  
Medial Nucleus ◽  
Whole Cell Patch Clamp ◽  
Auditory Experience ◽  
Evoked Activity

Interaural intensity differences are analyzed in neurons of the lateral superior olive (LSO) by integration of an inhibitory input from the medial nucleus of the trapezoid body (MNTB), activated by sound from the contralateral ear, with an excitatory input from the ipsilateral cochlear nucleus. The early postnatal refinement of this inhibitory MNTB-LSO projection along the tonotopic axis of the LSO has been extensively studied. However, little is known to what extent physiological changes at these inputs also occur after the onset of sound-evoked activity. Using whole-cell patch-clamp recordings of LSO neurons in acute brain stem slices, we analyzed the developmental changes of inhibitory synaptic currents evoked by MNTB fiber stimulation occurring after hearing onset. We compared these results in gerbils and mice, two species frequently used in auditory research. Our data show that neither the number of presumed input fibers nor the conductance of single fibers significantly changed after hearing onset. Also the amplitude of miniature inhibitory currents remained constant during this developmental period. In contrast, the kinetics of inhibitory synaptic currents greatly accelerated after hearing onset. We conclude that tonotopic refinement of inhibitory projections to the LSO is largely completed before the onset of hearing, whereas acceleration of synaptic kinetics occurs to a large part after hearing onset and might thus be dependent on proper auditory experience. Surprisingly, inhibitory input characteristics, as well as basic membrane properties of LSO neurons, were rather similar in gerbils and mice.

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.

Effects of interaural time delays of noise stimuli on low-frequency cells in the cat's inferior colliculus. I. Responses to wideband noise

1986 ◽  
Vol 55 (2) ◽  
pp. 280-300 ◽  
Author(s):  
T. C. Yin ◽  
J. C. Chan ◽  
D. R. Irvine
Keyword(s):  
Inferior Colliculus ◽  
Discharge Rate ◽  
Low Frequency ◽  
Central Peak ◽  
Stimulus Level ◽  
Central Nucleus ◽  
Interaural Phase ◽  
Wideband Noise ◽  
Pure Tones ◽  
Phase Differences

We examined the responses of low-frequency neurons in the central nucleus of the inferior colliculus (ICC) of the cat to interaurally delayed, wideband noise stimuli. The stimuli were pseudorandom noise signals that were generated digitally with a nominal bandwidth of 60-4,000 Hz. We also compared the responses to noise with those obtained from interaural phase differences of pure tones. We studied 144 neurons with characteristic frequencies below 2.5 kHz. Eighty-five percent (85%) of these were sensitive to changes in both interaural time differences (ITDs) of noise and interaural phase differences of pure tones, only 2% were sensitive to one stimulus but not the other, and the remainder were insensitive to both stimuli. For most cells the discharge rate was modulated in an approximately cyclic fashion by changes in ITDs of the wideband noise stimuli. The maximal spike counts often occurred near zero ITD, and there was considerable variability in the nature of the cycling, though it usually disappeared for ITDs greater than +/- 4,000 microseconds. The position of the central peak was usually (65%) within the physiologically relevant range of +/- 400 microseconds, and most (80%) occurred at positive ITDs, which corresponded to delays to the ipsilateral stimulus. In general, the shapes of the responses were not affected by changes in stimulus level above threshold. As long as identical noises were delivered to both ears, the responses were not sensitive to the particular noise stimulus used. When uncorrelated noises were delivered to the two ears, there was no sensitivity to ITDs. Composite curves were computed by linear summation of the responses to ITDs of pure tones at frequencies spaced at equal intervals throughout each cell's response area. The shapes of composite curves were similar to the responses of the same cell to ITDs of wideband noise stimuli. The positions of the central peaks of these two functions were highly correlated (r = 0.91, slope = 0.97). The values of characteristic delay and characteristic phase computed from the tonal responses were found to be good indicators of the shapes of the noise delay curves. Characteristic phases (CPs) near zero were associated with noise delay curves symmetric about the central peak, CPs near 0.5 cycles with those symmetric about the trough, while CPs between 0 and 0.5 or between 0.5 and 1.0 had noise delay curves that were asymmetric with a prominent trough to the left or right, respectively, of the central peak.(ABSTRACT TRUNCATED AT 400 WORDS)

Envelope coding in the lateral superior olive. I. Sensitivity to interaural time differences

1995 ◽  
Vol 73 (3) ◽  
pp. 1043-1062 ◽  
Author(s):  
P. X. Joris ◽  
T. C. Yin
Keyword(s):  
High Frequency ◽  
Response Rate ◽  
Discharge Rate ◽  
Modulation Frequency ◽  
Good Correspondence ◽  
Afferent Pathways ◽  
Lateral Superior Olive ◽  
Interaural Time Differences ◽  
Superior Olive ◽  
Naturally Occurring

1. Interaural level differences (ILDs), created by the head and pinna, have long been known to be the dominant acoustic cue for azimuthal localization of high-frequency tones. However, psychophysical experiments have demonstrated that human subjects can also lateralize complex high-frequency sounds on the basis of interaural time differences (ITDs) of the signal envelope. The lateral superior olive (LSO) is one of two pairs of binaural nuclei where the primary extraction of binaural cues for sound source location occurs. "IE" cells in LSO are inhibited by stimuli to the contralateral and excited by stimuli to the ipsilateral ear, and their response rate is therefore dependent on ILD. Anatomic specializations in the afferent pathways to the LSO suggest that this circuit also has a function in the detection of timing cues. We hypothesized that, besides ILD sensitivity, the IE property also conveys a sensitivity to ITDs of amplitude-modulated (AM) tones and could provide the physiological substrate for the psychophysical effect mentioned above. 2. In extracellular recordings from binaural LSO cells in barbiturate-anesthetized cats, response rate was a periodic function of ITDs of AM stimuli, i.e., all cells displayed ITD sensitivity. Binaural responses were smaller than responses to stimulation of the ipsilateral ear alone and were minimal when the envelopes in both ears were in-phase or nearly so. There was good correspondence between responses to ITDs and to dynamic interaural phase differences (IPDs), created by a difference in the envelope frequency to the two ears. Qualitatively, the responses were consistent with the outcome of an IE operation on temporally structured inputs. 3. To compare the relative importance of ILD and ITD, responses to combinations of the two cues were obtained. Despite robust ITD sensitivity in all binaural LSO cells encountered, the changes in response rate that would occur in response to naturally occurring ITDs were small in comparison with the changes expected for naturally occurring ILDs. The main limitation on ITD sensitivity was a steep decline in average discharge rate as the modulation frequency exceeded several hundred Hertz. 4. ITD sensitivity was also present to broadband stimuli, again with minimal rates occurring near 0 ITD. The sensitivity depended in a predictable fashion on the passband of filtered noise and was absent to binaurally uncorrelated noise bands. In response to clicks, ILDs interacted with ITD in a complicated fashion involving amplitude and latency effects. 5. Three low-characteristic frequency (CF) LSO cells were encountered that were IE and showed ITD sensitivity to the fine structure of low-frequency stimuli.(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals Interaction of excitation and inhibition in processing of pure tone and amplitude-modulated stimuli in the medial superior olive of the mustached bat

1994 ◽  
Vol 71 (2) ◽  
pp. 706-721 ◽  
Author(s):  
B. Grothe
Keyword(s):  
Discharge Rate ◽  
Stimulus Frequency ◽  
Spontaneous Discharge ◽  
Band Pass Filter ◽  
Response Patterns ◽  
Medial Superior Olive ◽  
Pass Filter ◽  
Superior Olive ◽  
Mustached Bat ◽  
Discharge Patterns

1. In mammals with good low-frequency hearing, the medial superior olive (MSO) processes interaural time or phase differences that are important cues for sound localization. Its cells receive excitatory projections from both cochlear nuclei and are thought to function as coincidence detectors. The response patterns of MSO neurons in most mammals are predominantly sustained. In contrast, the MSO in the mustached bat is a monaural nucleus containing neurons with phasic discharge patterns. These neurons receive projections from the contralateral anteroventral cochlear nucleus (AVCN) and the ipsilateral medial nucleus of the trapezoid body (MNTB). 2. To further investigate the role of the MSO in the bat, the responses of 252 single units in the MSO to pure tones and sinusoidal amplitude-modulated (SAM) stimuli were recorded. The results confirmed that the MSO in the mustached bat is tonotopically organized, with low frequencies in the dorsal part and high frequencies in the ventral part. The 61-kHz region is overrepresented. Most neurons tested (88%) were monaural and discharged only in response to contralateral stimuli. Their response could not be influenced by stimulation of the ipsilateral ear. 3. Only 11% of all MSO neurons were spontaneously active. In these neurons the spontaneous discharge rate was suppressed during the stimulus presentation. 4. The majority of cells (85%) responded with a phasic discharge pattern. About one-half (51%) responded with a level-independent phasic ON response. Other phasic response patterns included phasic OFF or phasic ON-OFF, depending on the stimulus frequency. Neurons with ON-OFF discharge patterns were most common in the 61-kHz region and absent in the high-frequency region. 5. Double tone experiments showed that at short intertone intervals the ON response to the second stimulus or the OFF response to the first stimulus was inhibited. 6. In neuropharmacological experiments, glycine applied to MSO neurons (n = 71) inhibited any tone-evoked response. In the presence of the glycine antagonist strychnine the response patterns changed from phasic to sustained (n = 35) and the neurons responded to both tones presented in double tone experiments independent of the intertone interval (n = 5). The effects of strychnine were reversible. 7. Twenty of 21 neurons tested with sinusoidally amplitude-modulated (SAM) signals exhibited low-pass or band-pass filter characteristics. Tests with SAM signals also revealed a weak temporal summation of inhibition in 13 of the 21 cells tested.(ABSTRACT TRUNCATED AT 400 WORDS)

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