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

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.

1991 ◽  
Vol 65 (3) ◽  
pp. 598-605 ◽  
Author(s):  
P. G. Finlayson ◽  
D. M. Caspary

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)


1995 ◽  
Vol 73 (3) ◽  
pp. 1043-1062 ◽  
Author(s):  
P. X. Joris ◽  
T. C. Yin

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)


1994 ◽  
Vol 71 (2) ◽  
pp. 706-721 ◽  
Author(s):  
B. Grothe

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)


2019 ◽  
Vol 597 (8) ◽  
pp. 2269-2295 ◽  
Author(s):  
Alexander U. Fischer ◽  
Nicolas I. C. Müller ◽  
Thomas Deller ◽  
Domenico Del Turco ◽  
Jonas O. Fisch ◽  
...  

2003 ◽  
Vol 90 (4) ◽  
pp. 2581-2591 ◽  
Author(s):  
F. Aura Ene ◽  
Paul H. M. Kullmann ◽  
Deda C. Gillespie ◽  
Karl Kandler

The lateral superior olive (LSO) is a binaural auditory brain stem nucleus that plays a central role in sound localization. Survival and maturation of developing LSO neurons critically depend on intracellular calcium signaling. Here we investigated the mechanisms by which glutamatergic afferents from the cochlear nucleus increase intracellular calcium concentration in LSO neurons. Using fura-2 calcium imaging in slices prepared from neonatal mice, we found that cochlear nucleus afferents can activate all major classes of ionotropic and metabotropic glutamate receptors, each of which contributes to an increase in intracellular calcium. The specific activation of different glutamate receptor classes was dependent on response amplitudes and afferent stimulus patterns. Low-amplitude responses elicited by single stimuli were entirely mediated by calcium-impermeable AMPA/kainate receptors that activated voltage-gated calcium channels. Larger-amplitude responses elicited by either single stimuli or stimulus trains resulted in additional calcium influx through N-methyl-d-aspartate receptors. Finally, high-frequency stimulation also recruited group I and group II metabotropic glutamate receptors, both of which mobilized intracellular calcium. This calcium release in turn activated a strong influx of extracellular calcium through a membrane calcium channel that is distinct from voltage-gated calcium channels. Together, these results indicate that before hearing onset, distinct patterns of afferent activity generate qualitatively distinct types of calcium responses, which likely serve in guiding different aspects of LSO development.


1985 ◽  
Vol 54 (4) ◽  
pp. 1006-1025 ◽  
Author(s):  
C. Xerri ◽  
S. Gianni ◽  
D. Manzoni ◽  
O. Pompeiano

The response characteristics of neurons located in the lateral vestibular nucleus (LVN) to neck rotation at 0.026 Hz, 10 degrees peak displacement, have been investigated in precollicular decerebrate cats submitted to ipsilateral acute (aVN) or chronic vestibular neurectomy (cVN). On the whole, 105 units were tested after aVN (i.e., during the first postoperative hours) and 132 units after cVN (i.e., after full compensation of the postural and locomotor deficits). The neurons were histologically located either in the rostroventral (rvLVN) or the dorsocaudal part (dcLVN) of Deiters' nucleus, which are known to project mainly to the cervical and the lumbosacral cord, respectively. Moreover, 55 units in the former group and 66 units in the latter group were identified as vestibulospinal neurons projecting to lumbosacral segments of the spinal cord. The responses of these 237 LVN neurons to the neck input were then compared with those of 120 LVN neurons recorded previously in decerebrate cats with intact labyrinths. Whereas 58.3% of the LVN units recorded in control experiments were responsive to neck rotation, 69.5% of the units were affected by this stimulation at the acute stage of the neurectomy and 74.2% at the chronic stage. This increase in responsive units after aVN and cVN with respect to the controls was found exclusively in the dcLVN. The mean discharge rate of the responsive LVN neurons decreased from 40.7 +/- 48.9 (SD) imp/s in control experiments to 22.1 +/- 15.8 (SD) imp/s after a VN. Similar value was also obtained after cVN [25.0 +/- 17.2 (SD) imp/s], suggesting that compensation of the postural deficits elicited by the vestibular neurectomy results from a redistribution of the excitatory drive within different populations of LVN neurons. Indeed, the relation found in control experiments, i.e., that the faster the conduction velocity of vestibulospinal axons the lower was the unit discharge at rest, was lost after aVN, due to a decrease in resting discharge of the slow units. The mean discharge rate of the slow units, however, recovered after cVN, so that the negative correlation between resting discharge rate and axonal conduction velocity was reestablished. The average gain and sensitivity of the first harmonic response of the LVN neurons to neck rotation recorded after aVN and cVN were comparable to those obtained in preparations with the vestibular nerves intact.(ABSTRACT TRUNCATED AT 400 WORDS)


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