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Bilateral collicular interaction: modulation of auditory signal processing in amplitude domain.

Mei HX, Cheng L, Tang J, Fu ZY, Wang X, Jen PH, Chen QC - PLoS ONE (2012)

Bottom Line: Bilateral collicular interaction produces a decrease in the response magnitude and an increase in the response latency of inhibited IC neurons but produces opposite effects on the response of facilitated IC neurons.The modulation effect is most effective at low sound level and is dependent upon the interval between the acoustic and electric stimuli.Three possible neural pathways underlying the bilateral collicular interaction are discussed.

View Article: PubMed Central - PubMed

Affiliation: College of Life sciences and Hubei Key Lab of Genetic Regulation and Integrative Biology, Central China Normal University, Wuhan, Hubei, China.

ABSTRACT
In the ascending auditory pathway, the inferior colliculus (IC) receives and integrates excitatory and inhibitory inputs from many lower auditory nuclei, intrinsic projections within the IC, contralateral IC through the commissure of the IC and from the auditory cortex. All these connections make the IC a major center for subcortical temporal and spectral integration of auditory information. In this study, we examine bilateral collicular interaction in modulating amplitude-domain signal processing using electrophysiological recording, acoustic and focal electrical stimulation. Focal electrical stimulation of one (ipsilateral) IC produces widespread inhibition (61.6%) and focused facilitation (9.1%) of responses of neurons in the other (contralateral) IC, while 29.3% of the neurons were not affected. Bilateral collicular interaction produces a decrease in the response magnitude and an increase in the response latency of inhibited IC neurons but produces opposite effects on the response of facilitated IC neurons. These two groups of neurons are not separately located and are tonotopically organized within the IC. The modulation effect is most effective at low sound level and is dependent upon the interval between the acoustic and electric stimuli. The focal electrical stimulation of the ipsilateral IC compresses or expands the rate-level functions of contralateral IC neurons. The focal electrical stimulation also produces a shift in the minimum threshold and dynamic range of contralateral IC neurons for as long as 150 minutes. The degree of bilateral collicular interaction is dependent upon the difference in the best frequency between the electrically stimulated IC neurons and modulated IC neurons. These data suggest that bilateral collicular interaction mainly changes the ratio between excitation and inhibition during signal processing so as to sharpen the amplitude sensitivity of IC neurons. Bilateral interaction may be also involved in acoustic-experience-dependent plasticity in the IC. Three possible neural pathways underlying the bilateral collicular interaction are discussed.

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Correlation among different modulated parameters of ICMdu neurons in relation to BF and MT differences.Linear regression analyses of the scatter plots showing the BF shift in relation to BF and MT differences (A,B) as well as to DR and MT shift (C,D). N: number of neurons (see Fig. 6 for legends).
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pone-0041311-g010: Correlation among different modulated parameters of ICMdu neurons in relation to BF and MT differences.Linear regression analyses of the scatter plots showing the BF shift in relation to BF and MT differences (A,B) as well as to DR and MT shift (C,D). N: number of neurons (see Fig. 6 for legends).

Mentions: In this study, ICES focal stimulation also produced BF shift of ICMdu neurons toward that of electrically stimulated ICES neurons when the BF difference was between 2 and 8 kHz (Cheng et al., in preparation). For comparison with a previous study of corticofugal modulation of collicular amplitude-domain processing ([25]; see Discussion), we performed linear regression analyses of the scatter plots of BF shift against BF and MT differences as well as DR and MT shifts (Fig. 10). These analyses revealed that the BF shift significantly increased with BF difference but decreased with DR and MT shifts (Fig. 10A, p<0.001; C,D, p<0.05). In agreement with the previous study [25], the BF shift is not significantly correlated with the MT difference (Fig. 10B).


Bilateral collicular interaction: modulation of auditory signal processing in amplitude domain.

Mei HX, Cheng L, Tang J, Fu ZY, Wang X, Jen PH, Chen QC - PLoS ONE (2012)

Correlation among different modulated parameters of ICMdu neurons in relation to BF and MT differences.Linear regression analyses of the scatter plots showing the BF shift in relation to BF and MT differences (A,B) as well as to DR and MT shift (C,D). N: number of neurons (see Fig. 6 for legends).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3404052&req=5

pone-0041311-g010: Correlation among different modulated parameters of ICMdu neurons in relation to BF and MT differences.Linear regression analyses of the scatter plots showing the BF shift in relation to BF and MT differences (A,B) as well as to DR and MT shift (C,D). N: number of neurons (see Fig. 6 for legends).
Mentions: In this study, ICES focal stimulation also produced BF shift of ICMdu neurons toward that of electrically stimulated ICES neurons when the BF difference was between 2 and 8 kHz (Cheng et al., in preparation). For comparison with a previous study of corticofugal modulation of collicular amplitude-domain processing ([25]; see Discussion), we performed linear regression analyses of the scatter plots of BF shift against BF and MT differences as well as DR and MT shifts (Fig. 10). These analyses revealed that the BF shift significantly increased with BF difference but decreased with DR and MT shifts (Fig. 10A, p<0.001; C,D, p<0.05). In agreement with the previous study [25], the BF shift is not significantly correlated with the MT difference (Fig. 10B).

Bottom Line: Bilateral collicular interaction produces a decrease in the response magnitude and an increase in the response latency of inhibited IC neurons but produces opposite effects on the response of facilitated IC neurons.The modulation effect is most effective at low sound level and is dependent upon the interval between the acoustic and electric stimuli.Three possible neural pathways underlying the bilateral collicular interaction are discussed.

View Article: PubMed Central - PubMed

Affiliation: College of Life sciences and Hubei Key Lab of Genetic Regulation and Integrative Biology, Central China Normal University, Wuhan, Hubei, China.

ABSTRACT
In the ascending auditory pathway, the inferior colliculus (IC) receives and integrates excitatory and inhibitory inputs from many lower auditory nuclei, intrinsic projections within the IC, contralateral IC through the commissure of the IC and from the auditory cortex. All these connections make the IC a major center for subcortical temporal and spectral integration of auditory information. In this study, we examine bilateral collicular interaction in modulating amplitude-domain signal processing using electrophysiological recording, acoustic and focal electrical stimulation. Focal electrical stimulation of one (ipsilateral) IC produces widespread inhibition (61.6%) and focused facilitation (9.1%) of responses of neurons in the other (contralateral) IC, while 29.3% of the neurons were not affected. Bilateral collicular interaction produces a decrease in the response magnitude and an increase in the response latency of inhibited IC neurons but produces opposite effects on the response of facilitated IC neurons. These two groups of neurons are not separately located and are tonotopically organized within the IC. The modulation effect is most effective at low sound level and is dependent upon the interval between the acoustic and electric stimuli. The focal electrical stimulation of the ipsilateral IC compresses or expands the rate-level functions of contralateral IC neurons. The focal electrical stimulation also produces a shift in the minimum threshold and dynamic range of contralateral IC neurons for as long as 150 minutes. The degree of bilateral collicular interaction is dependent upon the difference in the best frequency between the electrically stimulated IC neurons and modulated IC neurons. These data suggest that bilateral collicular interaction mainly changes the ratio between excitation and inhibition during signal processing so as to sharpen the amplitude sensitivity of IC neurons. Bilateral interaction may be also involved in acoustic-experience-dependent plasticity in the IC. Three possible neural pathways underlying the bilateral collicular interaction are discussed.

Show MeSH
Related in: MedlinePlus