小鼠下丘神经元的频率表征及其频率调谐：在体细胞内记录
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摘要
频率(frequency)是声音的3个基本的特征参数之一,而每个听中枢神经元均能对一定范围的声频率产生反应,并可以不同的电位变化形式进行表征,将所感受到的频率变化以不同电位形式和时间形式进行编码。先前有关听神经元频率调谐及其表征的研究基本是采用细胞外记录方法研究获得。由于细胞内记录研究听神经元频率调谐具有较大的难度,致使至今少见有采用细胞内记录方法研究频率调谐方面的报道。本实验采用自由声场刺激,在体细胞内记录浅麻醉状态下昆明小鼠(Musmusculus, Km)下丘(inferior colliculus, IC)神经元在固定强度下对不同频率(1-48kHz)纯音刺激的反应及其调谐和表征方式。
实验共记录到80个声敏感的IC神经元,对其中39个具完整数据的神经元加以分析,这些神经元的记录深度、最佳频率、频率响应带宽、反应潜伏期(平均值士标准差)分别为：345～1871 (963±352)μm、5±33(17.0±8.6) kHz、7～47(30.3±11.7) kHz、3.5～19.2 (11.2±3.8) ms。
结果显示：1、依据神经元对频率变化反应和表征的形式分为4种类型：①以抑制性突触后电位(inhibitory post-synaptic potential, IPSP)或自发动作电位发放终止及持续时间的形式表征频率变化和调谐特性(n=9)。②以兴奋性突触后电位(excitatory postsynaptic potential, EPSP)形式表征频率变化和调谐特性(n=7)。③以动作电位((Action potential,AP)形式表征频率变化和调谐特性(n=18)。④以复杂性反应(complex response)即多种电位变化形式表征频率变化和调谐特性(n=5)。2、从第一个IPSP、EPSP和AP反应的潜伏期来看,三类反应的潜伏期均随给声频率的改变表现出一定的调谐特性,即在神经元最佳频率下潜伏期值最短,无论是向高或低偏离最佳频率时均随之延长；另从IPSP和EPSP反应的绝对幅度、持续时间、上升和衰减时间来看,除上升时间不随频率改变而发生显著性变化外,其余参数在最佳频率下均表现为最佳反应状态,随向高或低偏离最佳频率,反应逐渐减弱。3、在最佳频率下,3种电位变化的潜伏期组间比较显示,IPSP反应的平均潜伏期最短(8.8±3.4ms), EPSP反应潜伏期次之(9.3±4.0ms), AP反应的潜伏期最长(12.8±3.2 ms),其变化有显著性差异(P<0.05)；另外,最佳频率下IPSP的平均持续时间(285.3±187.5 ms)、上升时间(22.1±13.1 ms)和衰减时间(263.3±182.6ms),均较EPSP的持续时间(37.6±68.1 ms)、上升时间(5.0±6.5 ms)和衰减时间(32.6±62.0 ms)显著延长(P<0.05)；而EPSP(5.3±2.1mV)和IPSP(7.0±3.5mV)的幅度变化无显著性差异(P>0.05)。
上述结果提示,下丘神经元对频率改变的表征和调谐方式主要有动作电位、EPSP和IPSP3种形式,而3者的反应潜伏期和EPSP与IPSP的幅度、反应持续时间、上升时间和衰减时间,均可参与听神经元对频率的表征和调谐。另外,比较第一个反应的潜伏期,以IPSP反应的潜伏期最短、EPSP反应次之,AP反应最长,表明局部反应能实时(real time)反映刺激参量的变化；而AP要经EPSP的时间和空间总和达到某一临界值后才能爆发,故耗时较长；且IPSP反应潜伏期最短提示下丘神经元听反应过程中抑制性输入总是率先到达。而持续时间IPSP显著长于EPSP,这可能是由于从超极化性的IPSP恢复至静息电位需要的时间长于从去极化性的EPSP恢复至静息电位的时间所导致的。
Frequency of sound is one of the three basic characteristic of the sound, each central auditory neuron can respond to sound within some range of frequency, represent, and code these sound frequencies by different pattern of membrane potential. Because there are some difficulties in using intracellular recording in vivo, previous studies on frequency representation and tuning of sound in central auditory neurons were basically to use electrophysiological method of extracellular recording in vivo, In this study, under free field stimulation condition, we used the method of intracellular recording in vivo and investigated frequency representation and tuning of inferior collicular (IC) neurons in light anesthetized mice (Mus musculus, Km).
80 sound sensitive IC neurons were obtained by intracellular recording and frequency representation and tuning of 39 among these neurons were analyzed. The ranges (mean±standard deviation) of recording depth (μm), best frequency (kHz), frequency bandwidth (kHz), and response latency (ms) of 39 neurons were 345～1871 (963±352),5～33 (17.0±8.6),7～47 (30.3±11.7), and 3.5～19.2 (11.2±3.8), respectively.
According to responses and representation of neurons to different sound frequencies, they could be classified into four types, i.e.①the neurons (n=9) showed sound frequency representation and tuning property by inhibitory postsynaptic potential (IPSP) and duration of inhibitory action;②the neurons (n=7) showed sound frequency representation and tuning property by excitatory postsynaptic potential (EPSP);③the neurons (n=18) showed sound frequency representation and tuning property by action potential (AP); and④the neurons (n=5) showed sound frequency representation and tuning property by different ways of membrane potentials. On the other hand, the neurons had the shortest latency to best frequency sound stimulus and their latencies also showed some tuning properties, latency changed with frequency changing. By comparison of latencies of first IPSP, EPSP, and AP, the results showed latency (8.8±3.4 ms) of IPSP0.05) between mean amplitudes of IPSP (7.0±3.5 mV) and EPSP (5.3±2.1 mV).
These results from intracellular recording demonstrated that three ways, AP, EPSP, and IPSP, could be used in frequency representation and tuning of IC neurons, but their temporal properties were different. The longer duration of IPSP suggested that IC neurons needed longer recovery time from hyper-polarization to resting membrane potential (RP) than from EPSP to RP.
实验共记录到80个声敏感的IC神经元,对其中39个具完整数据的神经元加以分析,这些神经元的记录深度、最佳频率、频率响应带宽、反应潜伏期(平均值士标准差)分别为：345～1871 (963±352)μm、5±33(17.0±8.6) kHz、7～47(30.3±11.7) kHz、3.5～19.2 (11.2±3.8) ms。
结果显示：1、依据神经元对频率变化反应和表征的形式分为4种类型：①以抑制性突触后电位(inhibitory post-synaptic potential, IPSP)或自发动作电位发放终止及持续时间的形式表征频率变化和调谐特性(n=9)。②以兴奋性突触后电位(excitatory postsynaptic potential, EPSP)形式表征频率变化和调谐特性(n=7)。③以动作电位((Action potential,AP)形式表征频率变化和调谐特性(n=18)。④以复杂性反应(complex response)即多种电位变化形式表征频率变化和调谐特性(n=5)。2、从第一个IPSP、EPSP和AP反应的潜伏期来看,三类反应的潜伏期均随给声频率的改变表现出一定的调谐特性,即在神经元最佳频率下潜伏期值最短,无论是向高或低偏离最佳频率时均随之延长；另从IPSP和EPSP反应的绝对幅度、持续时间、上升和衰减时间来看,除上升时间不随频率改变而发生显著性变化外,其余参数在最佳频率下均表现为最佳反应状态,随向高或低偏离最佳频率,反应逐渐减弱。3、在最佳频率下,3种电位变化的潜伏期组间比较显示,IPSP反应的平均潜伏期最短(8.8±3.4ms), EPSP反应潜伏期次之(9.3±4.0ms), AP反应的潜伏期最长(12.8±3.2 ms),其变化有显著性差异(P<0.05)；另外,最佳频率下IPSP的平均持续时间(285.3±187.5 ms)、上升时间(22.1±13.1 ms)和衰减时间(263.3±182.6ms),均较EPSP的持续时间(37.6±68.1 ms)、上升时间(5.0±6.5 ms)和衰减时间(32.6±62.0 ms)显著延长(P<0.05)；而EPSP(5.3±2.1mV)和IPSP(7.0±3.5mV)的幅度变化无显著性差异(P>0.05)。
上述结果提示,下丘神经元对频率改变的表征和调谐方式主要有动作电位、EPSP和IPSP3种形式,而3者的反应潜伏期和EPSP与IPSP的幅度、反应持续时间、上升时间和衰减时间,均可参与听神经元对频率的表征和调谐。另外,比较第一个反应的潜伏期,以IPSP反应的潜伏期最短、EPSP反应次之,AP反应最长,表明局部反应能实时(real time)反映刺激参量的变化；而AP要经EPSP的时间和空间总和达到某一临界值后才能爆发,故耗时较长；且IPSP反应潜伏期最短提示下丘神经元听反应过程中抑制性输入总是率先到达。而持续时间IPSP显著长于EPSP,这可能是由于从超极化性的IPSP恢复至静息电位需要的时间长于从去极化性的EPSP恢复至静息电位的时间所导致的。
Frequency of sound is one of the three basic characteristic of the sound, each central auditory neuron can respond to sound within some range of frequency, represent, and code these sound frequencies by different pattern of membrane potential. Because there are some difficulties in using intracellular recording in vivo, previous studies on frequency representation and tuning of sound in central auditory neurons were basically to use electrophysiological method of extracellular recording in vivo, In this study, under free field stimulation condition, we used the method of intracellular recording in vivo and investigated frequency representation and tuning of inferior collicular (IC) neurons in light anesthetized mice (Mus musculus, Km).
80 sound sensitive IC neurons were obtained by intracellular recording and frequency representation and tuning of 39 among these neurons were analyzed. The ranges (mean±standard deviation) of recording depth (μm), best frequency (kHz), frequency bandwidth (kHz), and response latency (ms) of 39 neurons were 345～1871 (963±352),5～33 (17.0±8.6),7～47 (30.3±11.7), and 3.5～19.2 (11.2±3.8), respectively.
According to responses and representation of neurons to different sound frequencies, they could be classified into four types, i.e.①the neurons (n=9) showed sound frequency representation and tuning property by inhibitory postsynaptic potential (IPSP) and duration of inhibitory action;②the neurons (n=7) showed sound frequency representation and tuning property by excitatory postsynaptic potential (EPSP);③the neurons (n=18) showed sound frequency representation and tuning property by action potential (AP); and④the neurons (n=5) showed sound frequency representation and tuning property by different ways of membrane potentials. On the other hand, the neurons had the shortest latency to best frequency sound stimulus and their latencies also showed some tuning properties, latency changed with frequency changing. By comparison of latencies of first IPSP, EPSP, and AP, the results showed latency (8.8±3.4 ms) of IPSP
These results from intracellular recording demonstrated that three ways, AP, EPSP, and IPSP, could be used in frequency representation and tuning of IC neurons, but their temporal properties were different. The longer duration of IPSP suggested that IC neurons needed longer recovery time from hyper-polarization to resting membrane potential (RP) than from EPSP to RP.
引文
1.邱强,唐杰,余祖林,张娟,周英杰,肖中举,沈钧贤．小鼠下丘听神经元的反应潜伏期对特征频率的表达.中国科学,2007,37：190-197.
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3. Saldana E, Feliciano M, Mugnaini E.Distribution of descending projections from primary auditory neocortex to inferior colliculus mimics the topography of intracollicular projections.J Comp Neurol.1996,371:15-40.
4. Feliciano M, Potashner SJ.Evidence for a glutamatergic pathway from the guinea pig auditory cortex to the inferior colliculus. J Neurochem.1995,65,:1348-57.
5. Saldana E, Merchan MA.Intrinsic and commissural connections of the rat inferior colliculus.J Comp Neurol.1992,319:417-37.
6. Casseday JH, Covey E.Frequency tuning properties of neurons in the inferior colliculus of an FM bat. J Comp Neurol.1992,319:34-50.
7. Jen PH, Zhang J.The role of GABAergic inhibition on direction-dependent sharpening of frequency tuning in bat inferior collicular neurons. Brain Res. 2000,862:127-37.
8. Yang L, Pollak GD, Resler C.GABAergic circuits sharpen tuning curves and modify response properties in the mustache bat inferior colliculus. J Neurophysiol. 1992,68:1760-74.
9. Suga N, Zhang YF, Yan J. Sharpening of frequency tuning by inhibition in the thalamic auditory nucleus of the mustached Bat. J Neurophysiol.1997,77: 2098-2114.
10. Le Beau FE, Malmierca MS, Rees A.Iontophoresis in vivo demonstrates a key role for GABAA and glycinergic inhibition in shaping frequency response areas in the inferior colliculus of guinea pig. J Neurosci.2001,21:7303-7312.
11. Yang L, Pollak GD, Resler C.GABAergic circuits sharpen tuning curves and modify response properties in the mustache bat inferior colliculus.J Neurophysiol.1992,68:1760-1774.
12. Xie R, Gittelman JX, Li N, Pollak GD.Whole cell recordings of intrinsic properties and sound-evoked responses from the inferior colliculus. Neuroscience. 2008,154:245-56.
13. Xie R, Gittelman JX, Pollak GD.Rethinking tuning:in vivo whole-cell recordings of the inferior colliculus in awake bats. J Neurosci.2007,27:9469-81.
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18.王欣,吴飞健,陈其才.弱噪声前掩蔽对下丘神经元频率调谐的影响.听力学及言语疾病杂志,2005,13：333-336.
19. Fuzessery ZM, Hall JC.Role of GABA in shaping frequency tuning and creating FM sweep selectivity in the inferior colliculus. J Neurophysiol.1996,76:105-973.
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21. Xie R, Meitzen J, Pollak GD. Differing roles of inhibition in hierarchical processing of species-specific calls in auditory brainstem nuclei.J Neurophysiol.2005,94:4019-4037.
22. Kuwada S, Batra R, Yin TC, Oliver DL, Haberly LB, Stanford TR.Intracellular recordings in response to monaural and binaural stimulation of neurons in the inferior colliculus of the cat. J Neurosci.1997,17:7565-7581.
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24. Pedemonte M, Torterolo P, Velluti RA. In vivo intracellular characteristics of inferior colliculus neurons in guinea pigs. Brain Res.1997,759:24-31.
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43. Jen PH, Chen QC, Wu FJ. Interaction between excitation and inhibition affects frequency tuning curve, response size and latency of neurons in the auditory cortex of the big brown bat, Eptesicus fuscus. Hear Res.2002,174:281-289.
44. Casseday JH, Ehrlich D, Covey E. Neural tuning for sound duration:role of inhibitory mechanisms in the inferior colliculus. Science.1994,264:847-850.
45. Covey E, Kauer JA, Casseday JH. Whole-cell patch-clamp recording reveals subthreshold sound-evoked postsynaptic currents in the inferior colliculus of awake bats. J Neurosci.1996,16:3009-3018.
2. Gonzalez-Hernandez T, Mantolan-Sarmiento B, Gonzalez-Gonzalez B, Perez-Gonzalez H. Sources of GABAergic input to the inferior colliculus of the rat.J Comp Neurol.1996,372:309-26.
3. Saldana E, Feliciano M, Mugnaini E.Distribution of descending projections from primary auditory neocortex to inferior colliculus mimics the topography of intracollicular projections.J Comp Neurol.1996,371:15-40.
4. Feliciano M, Potashner SJ.Evidence for a glutamatergic pathway from the guinea pig auditory cortex to the inferior colliculus. J Neurochem.1995,65,:1348-57.
5. Saldana E, Merchan MA.Intrinsic and commissural connections of the rat inferior colliculus.J Comp Neurol.1992,319:417-37.
6. Casseday JH, Covey E.Frequency tuning properties of neurons in the inferior colliculus of an FM bat. J Comp Neurol.1992,319:34-50.
7. Jen PH, Zhang J.The role of GABAergic inhibition on direction-dependent sharpening of frequency tuning in bat inferior collicular neurons. Brain Res. 2000,862:127-37.
8. Yang L, Pollak GD, Resler C.GABAergic circuits sharpen tuning curves and modify response properties in the mustache bat inferior colliculus. J Neurophysiol. 1992,68:1760-74.
9. Suga N, Zhang YF, Yan J. Sharpening of frequency tuning by inhibition in the thalamic auditory nucleus of the mustached Bat. J Neurophysiol.1997,77: 2098-2114.
10. Le Beau FE, Malmierca MS, Rees A.Iontophoresis in vivo demonstrates a key role for GABAA and glycinergic inhibition in shaping frequency response areas in the inferior colliculus of guinea pig. J Neurosci.2001,21:7303-7312.
11. Yang L, Pollak GD, Resler C.GABAergic circuits sharpen tuning curves and modify response properties in the mustache bat inferior colliculus.J Neurophysiol.1992,68:1760-1774.
12. Xie R, Gittelman JX, Li N, Pollak GD.Whole cell recordings of intrinsic properties and sound-evoked responses from the inferior colliculus. Neuroscience. 2008,154:245-56.
13. Xie R, Gittelman JX, Pollak GD.Rethinking tuning:in vivo whole-cell recordings of the inferior colliculus in awake bats. J Neurosci.2007,27:9469-81.
14. Aitkin LM. The auditory midbrain:structure and function in the central auditory pathway. Clifton, NJ:Humana.1985.
15. Casseday JH, Fremouw T, Covey E.The inferior colliculus:a hub for the central auditory system. In:Integrative functions in the mammalian auditory pathway (Oertel D, Popper AN, Fay RR, eds),2002,238-318. New York:Springer.
16. Oliver DL, Huerta, MF. Inferior and superior colliculi. In:The mammalian auditory system:neuroanatomy (Webster DB, Popper AN, Fay RR, eds).1992,168-221. New York:Springer.
17. Pollak GD, Casseday JH. The neural basis of echolocation in bats.1986. New York: Springer.
18.王欣,吴飞健,陈其才.弱噪声前掩蔽对下丘神经元频率调谐的影响.听力学及言语疾病杂志,2005,13：333-336.
19. Fuzessery ZM, Hall JC.Role of GABA in shaping frequency tuning and creating FM sweep selectivity in the inferior colliculus. J Neurophysiol.1996,76:105-973.
20. Jen PH, Zhang JP.corticofugal regulation of excitatory and inhibitory frequency tuning curves of bat inferior collicular neurons. Brain Res.1999,841:184-188.
21. Xie R, Meitzen J, Pollak GD. Differing roles of inhibition in hierarchical processing of species-specific calls in auditory brainstem nuclei.J Neurophysiol.2005,94:4019-4037.
22. Kuwada S, Batra R, Yin TC, Oliver DL, Haberly LB, Stanford TR.Intracellular recordings in response to monaural and binaural stimulation of neurons in the inferior colliculus of the cat. J Neurosci.1997,17:7565-7581.
23. Nelson PG, Erulkar SD.Synaptic mechanisms of excitation and inhibition in the central auditory pathway. J Neurophysiol.1963,26:908-922.
24. Pedemonte M, Torterolo P, Velluti RA. In vivo intracellular characteristics of inferior colliculus neurons in guinea pigs. Brain Res.1997,759:24-31.
25. Voytenko SV, Galazyuk AV.Intracellular recording reveals temporal integration in inferior colliculus neurons of awake bats. J Neurophysiol.2007,97:1368-1378.
26. Casseday JH, Ehrlich D, Covey E. Neural tuning for sound duration:role of inhibitory mechanisms in the inferior colliculus. Science.1994,264:847-850.
27. Covey E, Kauer JA, Casseday JH.Whole-cell patch-clamp recording reveals subthreshold sound-evoked postsynaptic currents in the inferior colliculus of awake bats. J Neurosci.1996,16:3009-3018.
28. Tan ML, Borst JG.Comparison of responses of neurons in the mouse inferior colliculus to current injections, tones of different durations and sinusoidal amplitude-modulated tones. J Neurophysiol.2007,98:454-466.
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