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A modeling study of the responses of the lateral superior olive to ipsilateral sinusoidally amplitude-modulated tones.

Wang L, Colburn HS - J. Assoc. Res. Otolaryngol. (2011)

Bottom Line: In the model, AHP channels alone were not sufficient to induce the observed rate decrease at high modulation frequencies.In contrast, both the small and large rate decreases were replicated when KLT channels were included in the LSO neuron model.These results support the conclusion that KLT channels may play a major role in the large rate decreases seen in some units and that background inhibition may be a contributing factor, a factor that could be adequate for small decreases.

View Article: PubMed Central - PubMed

Affiliation: Department of Biomedical Engineering, Center for Hearing Research, Boston University, Boston, MA 02215, USA.

ABSTRACT
The lateral superior olive (LSO) is a brainstem nucleus that is classically understood to encode binaural information in high-frequency sounds. Previous studies have shown that LSO cells are sensitive to envelope interaural time difference in sinusoidally amplitude-modulated (SAM) tones (Joris and Yin, J Neurophysiol 73:1043-1062, 1995; Joris, J Neurophysiol 76:2137-2156, 1996) and that a subpopulation of LSO neurons exhibit low-threshold potassium currents mediated by Kv1 channels (Barnes-Davies et al., Eur J Neurosci 19:325-333, 2004). It has also been shown that in many LSO cells the average response rate to ipsilateral SAM tones decreases with modulation frequency above a few hundred Hertz (Joris and Yin, J Neurophysiol 79:253-269, 1998). This low-pass feature is not directly inherited from the inputs to the LSO since the response rate of these input neurons changes little with increasing modulation frequency. In the current study, an LSO cell model is developed to investigate mechanisms consistent with the responses described above, notably the emergent rate decrease with increasing frequency. The mechanisms explored included the effects of after-hyperpolarization (AHP) channels, the dynamics of low-threshold potassium channels (KLT), and the effects of background inhibition. In the model, AHP channels alone were not sufficient to induce the observed rate decrease at high modulation frequencies. The model also suggests that the background inhibition alone, possibly from the medial nucleus of the trapezoid body, can account for the small rate decrease seen in some LSO neurons, but could not explain the large rate decrease seen in other LSO neurons at high modulation frequencies. In contrast, both the small and large rate decreases were replicated when KLT channels were included in the LSO neuron model. These results support the conclusion that KLT channels may play a major role in the large rate decreases seen in some units and that background inhibition may be a contributing factor, a factor that could be adequate for small decreases.

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A Rate–fm functions of the HH-type LSO model with regular KLT channels. B Rate–fm function of the LSO model with a “frozen KLT” channel. The “frozen KLT” channel was modeled as a leaky conductance that represented the KLT conductance at resting potential. For both A and B, ratemean = 100 spikes/s, strE = 2.55 nS, and NE= 20. The blue, red, and green curves correspond to gKLT values of 0, 35, and 85 nS.
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Fig6: A Rate–fm functions of the HH-type LSO model with regular KLT channels. B Rate–fm function of the LSO model with a “frozen KLT” channel. The “frozen KLT” channel was modeled as a leaky conductance that represented the KLT conductance at resting potential. For both A and B, ratemean = 100 spikes/s, strE = 2.55 nS, and NE= 20. The blue, red, and green curves correspond to gKLT values of 0, 35, and 85 nS.

Mentions: To examine the effect of the KLT strength, the KLT conductance was varied while the number of excitatory inputs was set to 20 and the synaptic strength was fixed at 2.55 nS. Figure 6 shows the results for the simplified AN model with the ratemean parameter in Eq. 2 equal to 100 spikes/s. Three KLT conductance values were chosen (Fig. 6A) to illustrate the transition from an all-pass characteristic to a band-pass characteristic in the rate–fm function. Without the KLT channel, the average rates of the LSO model response were above 100 spikes/s at all modulation frequencies and showed a small peak at 200 Hz. When the KLT channel conductance increased to 35 nS, the rates at high (above 800 Hz) modulation frequencies were reduced more than the rates at low fm (say 200 Hz), which increased the RPH of the rate–fm function. For even larger KLT conductance of 85 nS, the average rates of the response at high fm became even lower while the rate at low fm remained at a much higher level, further increasing the RPH to about 70 spikes/s. [When KLT channel conductances higher than 85 nS were tested in the model, the rate at low modulation frequencies remained low and the RPH became smaller (results not shown)]. Overall, the KLT channel strongly suppressed the responses at high modulation frequencies, contributing to the low-pass characteristic in the rate–fm function, as shown in Figure 6A. This behavior is attributed to the suppressive effect of the KLT channel as documented by previous studies (Rothman and Manis 2003a, b, c). Another observation in Figure 6A is that the firing rate at 1,500 Hz approximately matched the firing rate at 0 Hz, independent of the absolute firing rate at 0 Hz. This characteristic was observed for all values of gKLT tested and may be caused by the membrane filtering at high modulation frequencies.FIG. 6


A modeling study of the responses of the lateral superior olive to ipsilateral sinusoidally amplitude-modulated tones.

Wang L, Colburn HS - J. Assoc. Res. Otolaryngol. (2011)

A Rate–fm functions of the HH-type LSO model with regular KLT channels. B Rate–fm function of the LSO model with a “frozen KLT” channel. The “frozen KLT” channel was modeled as a leaky conductance that represented the KLT conductance at resting potential. For both A and B, ratemean = 100 spikes/s, strE = 2.55 nS, and NE= 20. The blue, red, and green curves correspond to gKLT values of 0, 35, and 85 nS.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3298618&req=5

Fig6: A Rate–fm functions of the HH-type LSO model with regular KLT channels. B Rate–fm function of the LSO model with a “frozen KLT” channel. The “frozen KLT” channel was modeled as a leaky conductance that represented the KLT conductance at resting potential. For both A and B, ratemean = 100 spikes/s, strE = 2.55 nS, and NE= 20. The blue, red, and green curves correspond to gKLT values of 0, 35, and 85 nS.
Mentions: To examine the effect of the KLT strength, the KLT conductance was varied while the number of excitatory inputs was set to 20 and the synaptic strength was fixed at 2.55 nS. Figure 6 shows the results for the simplified AN model with the ratemean parameter in Eq. 2 equal to 100 spikes/s. Three KLT conductance values were chosen (Fig. 6A) to illustrate the transition from an all-pass characteristic to a band-pass characteristic in the rate–fm function. Without the KLT channel, the average rates of the LSO model response were above 100 spikes/s at all modulation frequencies and showed a small peak at 200 Hz. When the KLT channel conductance increased to 35 nS, the rates at high (above 800 Hz) modulation frequencies were reduced more than the rates at low fm (say 200 Hz), which increased the RPH of the rate–fm function. For even larger KLT conductance of 85 nS, the average rates of the response at high fm became even lower while the rate at low fm remained at a much higher level, further increasing the RPH to about 70 spikes/s. [When KLT channel conductances higher than 85 nS were tested in the model, the rate at low modulation frequencies remained low and the RPH became smaller (results not shown)]. Overall, the KLT channel strongly suppressed the responses at high modulation frequencies, contributing to the low-pass characteristic in the rate–fm function, as shown in Figure 6A. This behavior is attributed to the suppressive effect of the KLT channel as documented by previous studies (Rothman and Manis 2003a, b, c). Another observation in Figure 6A is that the firing rate at 1,500 Hz approximately matched the firing rate at 0 Hz, independent of the absolute firing rate at 0 Hz. This characteristic was observed for all values of gKLT tested and may be caused by the membrane filtering at high modulation frequencies.FIG. 6

Bottom Line: In the model, AHP channels alone were not sufficient to induce the observed rate decrease at high modulation frequencies.In contrast, both the small and large rate decreases were replicated when KLT channels were included in the LSO neuron model.These results support the conclusion that KLT channels may play a major role in the large rate decreases seen in some units and that background inhibition may be a contributing factor, a factor that could be adequate for small decreases.

View Article: PubMed Central - PubMed

Affiliation: Department of Biomedical Engineering, Center for Hearing Research, Boston University, Boston, MA 02215, USA.

ABSTRACT
The lateral superior olive (LSO) is a brainstem nucleus that is classically understood to encode binaural information in high-frequency sounds. Previous studies have shown that LSO cells are sensitive to envelope interaural time difference in sinusoidally amplitude-modulated (SAM) tones (Joris and Yin, J Neurophysiol 73:1043-1062, 1995; Joris, J Neurophysiol 76:2137-2156, 1996) and that a subpopulation of LSO neurons exhibit low-threshold potassium currents mediated by Kv1 channels (Barnes-Davies et al., Eur J Neurosci 19:325-333, 2004). It has also been shown that in many LSO cells the average response rate to ipsilateral SAM tones decreases with modulation frequency above a few hundred Hertz (Joris and Yin, J Neurophysiol 79:253-269, 1998). This low-pass feature is not directly inherited from the inputs to the LSO since the response rate of these input neurons changes little with increasing modulation frequency. In the current study, an LSO cell model is developed to investigate mechanisms consistent with the responses described above, notably the emergent rate decrease with increasing frequency. The mechanisms explored included the effects of after-hyperpolarization (AHP) channels, the dynamics of low-threshold potassium channels (KLT), and the effects of background inhibition. In the model, AHP channels alone were not sufficient to induce the observed rate decrease at high modulation frequencies. The model also suggests that the background inhibition alone, possibly from the medial nucleus of the trapezoid body, can account for the small rate decrease seen in some LSO neurons, but could not explain the large rate decrease seen in other LSO neurons at high modulation frequencies. In contrast, both the small and large rate decreases were replicated when KLT channels were included in the LSO neuron model. These results support the conclusion that KLT channels may play a major role in the large rate decreases seen in some units and that background inhibition may be a contributing factor, a factor that could be adequate for small decreases.

Show MeSH