小鼠双侧下丘间的相互作用对声信号强度域加工的调制
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摘要
在上行听觉通路中,下丘(inferior colliculus, IC)接收并整合众多来自于低位脑干的听觉核团,IC的内在投射,对侧IC的连合投射,以及来自听皮层的兴奋性和抑制性输入。所有这些投射联系使得IC成为皮层下听信息的时相和空间整合的一个重要中枢。本研究在自由声场条件下,通过电生理记录,局部电刺激和离子电泳技术,在昆明小鼠中研究了局部电刺激一侧IC(简称为ICES)如何对另一侧IC(简称为ICMdu)声信号强度域的加工进行调制,并探讨了与双侧IC间相互作用有关的生物学意义和可能的功能作用途径。所获得的主要研究结果如下：
1.在实时的ICES局部电刺激条件下,记录到50个ICMdu神经元在电刺激前后对声刺激的完整的强度-放电率函数(rate-amplitude function, RAF)。根据被刺激侧神经元(ICES)与被调制侧神经元(ICMdu)J的最佳频率差(best frequency, BF)将ICMdu神经元分为两类,其中26个ICMdu神经元的BF差≤2kHz,称为双侧对应频率层神经元(bilateral corresponding frequency laminea, BCFL);另外24个ICMdu(?)经元的BF差>2kHz,称为双侧非对应频率层神经元(bilateral non-corresponding frequency laminea, BNCFL)。ICES局部电刺激时,14.0%ICMdu神经元的声反应被易化,这部分受兴奋性调制的ICMdu神经元均位于BCFL;而86.0%ICMdu神经元的声反应被抑制,受抑制性调制的ICMdu神经元广泛分布于BCFL(38.0%)和BNCFL(48.0%)中。双侧IC间的相互作用可增加受兴奋性调制的ICMdu神经元的放电率拓宽神经元反应的动态范围(dynamic range, DR)并减小RAF的斜率,从而获得对声刺激强度更广泛的响应范围。相反,双侧IC间相互作用减少受抑制性调制的ICMdu神经元的放电率和DR,并增加RAF的斜率,使得神经元对声刺激强度的敏感性被锐化。而且BCFL神经元所受到的抑制性调制作用的程度显著强于BNCFL神经元。
2.实验获得了70个受双侧IC间调制的ICMdu神经元,局部电刺激一侧IC对对侧IC的声反应的影响表现为广泛的抑制(87.1%)和集中或局灶性(foucus)兴奋(12.9%),且受抑制性和兴奋性调制的两组神经元在IC中的分布并无明显的拓扑分界。这一调制作用的影响在较低声刺激强度下表现的更为明显,且依赖于声电刺激间间隔。在最佳声电刺激间隔下,受抑制性调制的IC神经元的反应幅度最小而反应潜伏期最长,而受兴奋性调制的IC神经元则表现出相反的效应。一侧IC的局部电刺激可以压抑或是易化对侧IC神经元的RAF,且双侧IC交互电刺激的结果显示这一调制作用在双侧IC间既可以是相互的,也可能是单侧的。局部电刺激同样可引起IC神经元的BF,最小阈值(minimum threshold, MT),反应潜伏期和DR的改变,这一变化平均可持续约150分钟。双侧IC间相互作用对这些参数的调制程度取决于刺激侧IC神经元与被调制IC神经元间BF差。对受抑制性和兴奋性调制的神经元分别离子电泳注射荷包牡丹碱(bicuculline, Bic)和犬尿酸(kynurenic acid, KA)后,由局部电刺激所致的双侧IC间抑制性和兴奋性调制作用的影响可全部或部分被解除。表明双侧IC间的相互作用主要由GABA能受体和谷氨酸能受体介导。
3.双侧IC间的调制作用通过集中的点对点兴奋性投射来增强IC神经元的声反应并获得对声刺激的更好的强度响应,或通过更为广泛分布的抑制性锐化IC神经元的强度敏感性来影响IC对声信号强度域的加工。双侧IC间少部分集中的兴奋性调制和大多数广泛的抑制性调制作用,有可能分别参与了IC神经元双耳听觉特性的形成,如EE(excitation-excitation)和El (excitation-inhibition)神经元的形成；这种不平衡的兴奋和抑制性投射的分布可能在动物听声辨位和保证单侧优势中起着重要的作用。双侧IC间相互作用对IC神经元强度信号加工的调制作用可能建立在双侧IC的声调拓扑组构基础之上,并参与了IC听经验依赖的可塑性。
以上结果和发现提示,双侧IC间的相互作用为IC声信号的加工提供了一种可调的且可塑的调制模式。
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 commisure 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 examined bilateral collicular interaction in modulating amplitude-domain signal processing using electrophysiological recording, focal electrical stimulation and ionophoresis. The responses of IC neurons (abbreviated as ICMdu neurons) of mice(Mus musculus, Km) were recorded before, during and after the electrical stimulating of contralateral IC neurons (abbreviated as ICES neurons). The possible biological significance and neural pathways underlying the bilateral collicular interaction were discussed.
1. Fifty ICMdu neurons were classified as two groups according to the best frequency (BF) difference between ICMdu and ICES neuron. For simplicity,26ICMdu neurons were called bilateral corresponding frequency lamina (BCFL) neurons only if the BF difference was within2kHz. Otherwise24ICMdu neurons were called bilateral non-corresponding frequency lamina (BNCFL) neurons. During focally electrical stimulation of the contralateral IC neurons,14.0%IC neurons were facilitated and located in BCFL while86.0%IC neurons were inhibited and widespreadly located in BCFL (38.0%) and BNCFL (48.0%). The facilitatory modulation of bilateral collicular interaction increased the number of impulses and dynamic ranges (DRs) of facilitated IC neurons but decreased the slope of their rate-amplitude functions (RAFs) for wider amplitude responses to sound stimulus. Otherwise, the inhibitory modulation of bilateral collicular interaction decreased the number of impulses and DR of inhibited IC neurons but increased the slopes of their RAFs for sharper sensitivity to sound amplitude. Moreover the degree of inhibitory modulation was greater in BCFL neurons than in BNCFL neurons.
2. Seventy ICMdu neurons were studied for bilateral collicular interaction. Focal electrical stimulation of ICES produces widespread inhibition (87.1%) and focused facilitation (12.9%) of responses of contralateral ICMdu neurons. This bilateral collicular interaction produces a decrease in the response magnitude and an increase in the response latency of inhibited ICmdu neurons but produces an opposite effect in the response of facilitated ICMdu neurons. This modulation effect is most effective at low sound amplitude and is dependent upon the time interval between the acoustic and electric stimuli. At the optimal inter-stimulus interval, the inhibited ICMdu neurons have the smallest response magnitude and the longest response latency during focal electrical stimulation while the opposite effects are observed for the facilitated ICMdu neurons. The focal electrical stimulation of ICES compresses or expands the RAF of contralateral ICMdu neurons to improve the sensitivity in the change or range of amplitude. This bilateral collicular interaction is found to be either reciprocal or unilateral by alternatively electical stimulating paires neurons in both IC. The focal electrical stimulation also produces a shift in a neuron's minimum threshold and dynamic range for as long as150minutes. The degree of bilateral collicular interaction is dependent upon the difference in BF between the electrically stimulated IC neurons and the affected IC neurons. The results suggest that bilateral collicular interaction is mainly to change the ratio between excitation and inhibition during signal processing so as to sharpen the amplitude sensitivity of IC neurons. Respective ionophoretic application of bicuculline and kynurenic acid to inhibited and facilitated neurons shows that bilateral collicular interaction induced by focal electrical stimulation can be eliminated or only partly abolished.
The role of bilateral collicular interaction in amplitude-domain signal processing is to mudulate the amplitude signal processing by sharpening the amplitude sensitivity through wide spread inhibition and by enhancing response of facilitated IC neurons for better amplitude responsiveness to tuned sound stimulus through the more focused point-to-point connections. The small proportion of bilateral collicular facilitatory interaction between neurons in BCFL observed in our study may be involved in the formation of binaural property of EE (excitation-excitation) neurons. Conversly, the large proportion of bilateral collicular inhibitory interaction between the neurons in BCFL and BNCFL can perhaps match a high proportion of the El (excitation-inhibition) neurons and may be involved in the formation of binaural property of El neurons. The unbalanced property between excitatory and inhibitory projections have very important role in the formation of unilateral auditory dominance and sound location. The bilateral collicular interaction modulates the amplitude signal processing of IC neuron on the basis of topographic projections between two ICs, and it may be also invovled in acoustic-experience-dependent plasticity in the IC. The bilateral collicular interaction which was mediated by GABAergic and glutamatergic receptors provide an adjustable and plastic modulation pattern for auditory signal processing of ICs.
1.在实时的ICES局部电刺激条件下,记录到50个ICMdu神经元在电刺激前后对声刺激的完整的强度-放电率函数(rate-amplitude function, RAF)。根据被刺激侧神经元(ICES)与被调制侧神经元(ICMdu)J的最佳频率差(best frequency, BF)将ICMdu神经元分为两类,其中26个ICMdu神经元的BF差≤2kHz,称为双侧对应频率层神经元(bilateral corresponding frequency laminea, BCFL);另外24个ICMdu(?)经元的BF差>2kHz,称为双侧非对应频率层神经元(bilateral non-corresponding frequency laminea, BNCFL)。ICES局部电刺激时,14.0%ICMdu神经元的声反应被易化,这部分受兴奋性调制的ICMdu神经元均位于BCFL;而86.0%ICMdu神经元的声反应被抑制,受抑制性调制的ICMdu神经元广泛分布于BCFL(38.0%)和BNCFL(48.0%)中。双侧IC间的相互作用可增加受兴奋性调制的ICMdu神经元的放电率拓宽神经元反应的动态范围(dynamic range, DR)并减小RAF的斜率,从而获得对声刺激强度更广泛的响应范围。相反,双侧IC间相互作用减少受抑制性调制的ICMdu神经元的放电率和DR,并增加RAF的斜率,使得神经元对声刺激强度的敏感性被锐化。而且BCFL神经元所受到的抑制性调制作用的程度显著强于BNCFL神经元。
2.实验获得了70个受双侧IC间调制的ICMdu神经元,局部电刺激一侧IC对对侧IC的声反应的影响表现为广泛的抑制(87.1%)和集中或局灶性(foucus)兴奋(12.9%),且受抑制性和兴奋性调制的两组神经元在IC中的分布并无明显的拓扑分界。这一调制作用的影响在较低声刺激强度下表现的更为明显,且依赖于声电刺激间间隔。在最佳声电刺激间隔下,受抑制性调制的IC神经元的反应幅度最小而反应潜伏期最长,而受兴奋性调制的IC神经元则表现出相反的效应。一侧IC的局部电刺激可以压抑或是易化对侧IC神经元的RAF,且双侧IC交互电刺激的结果显示这一调制作用在双侧IC间既可以是相互的,也可能是单侧的。局部电刺激同样可引起IC神经元的BF,最小阈值(minimum threshold, MT),反应潜伏期和DR的改变,这一变化平均可持续约150分钟。双侧IC间相互作用对这些参数的调制程度取决于刺激侧IC神经元与被调制IC神经元间BF差。对受抑制性和兴奋性调制的神经元分别离子电泳注射荷包牡丹碱(bicuculline, Bic)和犬尿酸(kynurenic acid, KA)后,由局部电刺激所致的双侧IC间抑制性和兴奋性调制作用的影响可全部或部分被解除。表明双侧IC间的相互作用主要由GABA能受体和谷氨酸能受体介导。
3.双侧IC间的调制作用通过集中的点对点兴奋性投射来增强IC神经元的声反应并获得对声刺激的更好的强度响应,或通过更为广泛分布的抑制性锐化IC神经元的强度敏感性来影响IC对声信号强度域的加工。双侧IC间少部分集中的兴奋性调制和大多数广泛的抑制性调制作用,有可能分别参与了IC神经元双耳听觉特性的形成,如EE(excitation-excitation)和El (excitation-inhibition)神经元的形成；这种不平衡的兴奋和抑制性投射的分布可能在动物听声辨位和保证单侧优势中起着重要的作用。双侧IC间相互作用对IC神经元强度信号加工的调制作用可能建立在双侧IC的声调拓扑组构基础之上,并参与了IC听经验依赖的可塑性。
以上结果和发现提示,双侧IC间的相互作用为IC声信号的加工提供了一种可调的且可塑的调制模式。
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 commisure 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 examined bilateral collicular interaction in modulating amplitude-domain signal processing using electrophysiological recording, focal electrical stimulation and ionophoresis. The responses of IC neurons (abbreviated as ICMdu neurons) of mice(Mus musculus, Km) were recorded before, during and after the electrical stimulating of contralateral IC neurons (abbreviated as ICES neurons). The possible biological significance and neural pathways underlying the bilateral collicular interaction were discussed.
1. Fifty ICMdu neurons were classified as two groups according to the best frequency (BF) difference between ICMdu and ICES neuron. For simplicity,26ICMdu neurons were called bilateral corresponding frequency lamina (BCFL) neurons only if the BF difference was within2kHz. Otherwise24ICMdu neurons were called bilateral non-corresponding frequency lamina (BNCFL) neurons. During focally electrical stimulation of the contralateral IC neurons,14.0%IC neurons were facilitated and located in BCFL while86.0%IC neurons were inhibited and widespreadly located in BCFL (38.0%) and BNCFL (48.0%). The facilitatory modulation of bilateral collicular interaction increased the number of impulses and dynamic ranges (DRs) of facilitated IC neurons but decreased the slope of their rate-amplitude functions (RAFs) for wider amplitude responses to sound stimulus. Otherwise, the inhibitory modulation of bilateral collicular interaction decreased the number of impulses and DR of inhibited IC neurons but increased the slopes of their RAFs for sharper sensitivity to sound amplitude. Moreover the degree of inhibitory modulation was greater in BCFL neurons than in BNCFL neurons.
2. Seventy ICMdu neurons were studied for bilateral collicular interaction. Focal electrical stimulation of ICES produces widespread inhibition (87.1%) and focused facilitation (12.9%) of responses of contralateral ICMdu neurons. This bilateral collicular interaction produces a decrease in the response magnitude and an increase in the response latency of inhibited ICmdu neurons but produces an opposite effect in the response of facilitated ICMdu neurons. This modulation effect is most effective at low sound amplitude and is dependent upon the time interval between the acoustic and electric stimuli. At the optimal inter-stimulus interval, the inhibited ICMdu neurons have the smallest response magnitude and the longest response latency during focal electrical stimulation while the opposite effects are observed for the facilitated ICMdu neurons. The focal electrical stimulation of ICES compresses or expands the RAF of contralateral ICMdu neurons to improve the sensitivity in the change or range of amplitude. This bilateral collicular interaction is found to be either reciprocal or unilateral by alternatively electical stimulating paires neurons in both IC. The focal electrical stimulation also produces a shift in a neuron's minimum threshold and dynamic range for as long as150minutes. The degree of bilateral collicular interaction is dependent upon the difference in BF between the electrically stimulated IC neurons and the affected IC neurons. The results suggest that bilateral collicular interaction is mainly to change the ratio between excitation and inhibition during signal processing so as to sharpen the amplitude sensitivity of IC neurons. Respective ionophoretic application of bicuculline and kynurenic acid to inhibited and facilitated neurons shows that bilateral collicular interaction induced by focal electrical stimulation can be eliminated or only partly abolished.
The role of bilateral collicular interaction in amplitude-domain signal processing is to mudulate the amplitude signal processing by sharpening the amplitude sensitivity through wide spread inhibition and by enhancing response of facilitated IC neurons for better amplitude responsiveness to tuned sound stimulus through the more focused point-to-point connections. The small proportion of bilateral collicular facilitatory interaction between neurons in BCFL observed in our study may be involved in the formation of binaural property of EE (excitation-excitation) neurons. Conversly, the large proportion of bilateral collicular inhibitory interaction between the neurons in BCFL and BNCFL can perhaps match a high proportion of the El (excitation-inhibition) neurons and may be involved in the formation of binaural property of El neurons. The unbalanced property between excitatory and inhibitory projections have very important role in the formation of unilateral auditory dominance and sound location. The bilateral collicular interaction modulates the amplitude signal processing of IC neuron on the basis of topographic projections between two ICs, and it may be also invovled in acoustic-experience-dependent plasticity in the IC. The bilateral collicular interaction which was mediated by GABAergic and glutamatergic receptors provide an adjustable and plastic modulation pattern for auditory signal processing of ICs.
引文
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