Different forward masking patterns of sustained noise burst and segmental noise burst in the inferior collicular neurons of the mouse

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1 Acta Physiologica Sinica, April 25, 2006, 58 (2): Research Paper Different forward masking patterns of sustained noise burst and segmental noise burst in the inferior collicular neurons of the mouse LI An-An, CHEN Qi-Cai, WU Fei-Jian * School of Life Sciences, Central China Normal University, Wuhan , China Abstract: Although there has been a growing body of literature showing the neural correlation of forward masking caused by a pure tone masker in the auditory neurons, relative few studies have addressed the description of how the forward masking caused by a noise burst, especially a sequence of noise burst, is transformed into neuronal representation in the central auditory system. Using a noise forward masking paradigm under free field stimuli conditions, this in vivo study was devoted to exploring it in the inferior collicular (IC) neurons of the mouse (Mus musculus KM). A total of 96 IC neurons were recorded. Rate-intensity functions (RIFs) with and without the presentation of masker, sustained noise burst (SNB) or segmental noise burst (SGNB), were measured in 51 neurons. We found that the relative masker intensities were distributed over a wide range between 21 db below the minimum threshold (MT) and 19 db above the MT of the corresponding probe tone. The masking effect of the SGNB on firing rate in nearly half of neurons (type I, 45.10%) was stronger than that of the SNB (P<0.001), whereas in a smaller fraction of neurons (type III, 17.65%), it was weaker than that of the SNB (P<0.001). There was no significant difference in masking effect between the SNB and SGNB in type II neurons (37.25%, P>0.05). Irrespective of type I or type III neurons, the inhibitory effects of both kinds of maskers were all greater at lower probe intensities but decreased significantly with the increase of probe intensity (P<0.001). Interestingly, as the probe intensity increased, the difference of masking effect between the SNB and SGNB disappeared (P>0.05). In addition, we observed that temporal masking pattern could be transformed when the masker was changed from the SNB to SGNB. The main type of this transformation was from early-inhibition to proportional-inhibition pattern (53.85%, 7/13). Our data provide the evidence that the inhibitory effects of these two maskers have differential weights over time and intensity domains of the IC neurons responding to a pure tone. This suggests that the forward masking of noise is by no means the source of simply suppression in neuronal firing rate. There might be a few of active neural modulating ways in which the coding of temporal acoustical information can be operated. Key words: forward masking; noise; inferior colliculus; mouse 持续与间断噪声前掩蔽条件下小鼠下丘神经元的不同反应模式 李安安, 陈其才, 吴飞健 * 华中师范大学生命科学学院, 武汉 摘要 : 有关听中枢神经元纯音前掩蔽效应的神经表征已进行了大量研究, 但是, 噪声前掩蔽尤其是间断噪声前掩蔽效应的神经表征却鲜有报道 本研究观察了自由声场条件下, 昆明小鼠下丘神经元在持续与间断噪声前掩蔽条件下对纯音探测声的反应 共记录到 96 个下丘神经元, 测量了其中 51 个神经元在不同声刺激条件下的强度 - 放电率函数 结果显示, 掩蔽声强度分布较广 ( 探测声阈下 21 db 至阈上 19 db 之间 ) 在将近一半的神经元中, 间断噪声的前掩蔽效应比持续噪声强 (Ⅰ 型, 45.10%,P<0.001), 但也有少数神经元其间断噪声的掩蔽效应较持续噪声的弱 (Ⅲ 型,17.65%,P<0.001), 部分神经元无显著性差异 (Ⅱ 型,37.25%,P>0.05) 无论 Ⅰ 型还是 Ⅲ 型神经元, 持续噪声和间断噪声均在探测声强度较低时产生较强的抑制效应, 随着探测声强度的升高, 抑制效应逐渐降低 (P<0.001); 同时, 持续噪声和间断噪声之间前掩蔽效应差异亦不复存在 (P>0.05) 此外, 当掩蔽声由持续噪声换为间断噪声后, 部分 Ⅰ 型神经元掩蔽时相的类型发生转变, 其中最主要的转变为 Received Accepted This work was supported by the National Natural Science Foundation of China (No ), the Natural Science Foundation of Hubei Province (No. 2004ABA180), and Construction Fund for 211 Project of the Ministry of Education of China. * Corresponding author. Tel: ; Fax: ; wufj@mail.ccnu.edu.cn

2 142 Acta Physiologica Sinica, April 25, 2006, 58 (2): 由前期抑制转变为均衡抑制 (53.85%,7/13) 对下丘神经元声反应的时间域以及强度域, 持续与间断噪声具有分化性前掩蔽效应, 提示噪声前掩蔽并非简单的神经元发放压抑源, 某些主动性神经调制机制可能参与了噪声条件下时相声信息的编码过程 关键词 : 前掩蔽 ; 噪声 ; 下丘 ; 小鼠中图分类号 :Q437 Temporal summation is one of the most important coding strategies for auditory system to characterize the sound properties. Early auditory psychophysical studies have demonstrated that if two transient sounds are presented in rapid succession, perception of the lag sound (probe) would be impaired by the lead sound (masker). This phenomenon is referred to as forward masking, i.e., non-simultaneous temporal masking [1,2]. Masking phenomenon is ubiquitous in human speech cognition and animal acoustic communication. For example, when humans understand speech, foregoing syllables will cause forward masking effect on the subsequent syllables [3], and in echolocating bats, forward and backward masking would occur when they extract ethologically relevant information from a large population of environmental echoes [2,4]. Studies from a variety of perspectives have concluded that the origination of forward masking is attributable not only to the peripheral suppression, but also to the temporal summation in the central auditory system [5,6]. In everyday life, humans and animals are constantly exposed to a noise environment and they perceive their auditory scene as being composed of many interfering sounds originating from separate sources [7]. Therefore, it is noteworthy that the forward masking produced by noise is widespread features of auditory system. Although much progress has been made in the description of the characteristics of neuronal responses from in vivo electrophysiological studies under forward masking stimulation paradigm [2], to the best of our knowledge, very little is known about how an auditory neuron responses to a pure tone (lag sound) preceded by a weak noise tone burst (masker) because most of these investigations performed in the past decade mainly focused on the effects of the difference in frequency, intensity, location, duration, and onset asynchrony between two pure tones on temporal masking [2,6,8]. More recently, it is becoming increasingly clear that the response properties of auditory neurons can be dramatically altered as a result of noise masking. For instance, our previous studies of simultaneous masking have indicated that the weak noise could dynamically modulate the intensity and frequency sensitivity of the inferior collicular (IC) neurons in the mouse [9,10]. The data that have slowly accumulated during the recent years give us some hints on how to understand the general rules and cellular mechanisms that manage the acoustic responses of auditory neurons to a pure tone under the condition of forward noise masking. In addition, in view of the observation that auditory neurons exhibit differential response patterns to a single tone and a train of tones [11], it is therefore of interest to ask whether there is a difference in forward masking effects between a sustained noise burst (SNB) and a sequence of segmental noise burst (SGNB) at IC that a midbrain auditory nucleus which receives massive bilateral projections from practically all major auditory structures. The present study was designed to tackle this issue and we report here that the inhibitory effects of these two maskers have differential weights over time and intensity domains of the IC neurons responding to a pure tone. 1 MATERIALS AND METHODS 1.1 Animal preparation and sound stimulation The experiments were conducted on 10 adult healthy mice (Mus musculus KM) (20~25 g, body weight) with a positive Preyer s pinna reflex. The surgical procedures and electronic instruments used to generate acoustic stimuli have been described in our previous paper [9]. The pure tone burst (probe, duration: 40 ms; rice-decay time: 2 ms) was produced through a function (GFG-8016G, Good Will Inst. Co., Ltd., Malaysia), a tone burst generator (homemade), and an attenuator (LAT-45, Leader, Japan). The SGNB (masker, total duration: 40 ms) consisted of 5 noise segments with 4 ms duration. The interval between each noise segment is 9 ms. Likewise, the SNB (masker, duration: 40 ms; rice-decay time: 2 ms) or SGNB were produced through a white noise generator (HP 33220A, USA), a burst generator (homemade) driven by a stimulator (Nihon, Japan), and an attenuator (LAT-45, Leader, Japan). The tone burst and the SNB or SGNB were then combined with a custom-made mixer and amplified by an ultrasonic sound power amplifier (homemade) before sent to a small loudspeaker (AKG model CK 50, 1.5 cm in diameter, 1.2 g, frequency response 1~100 khz ). The loudspeaker, calibrated with a 1/4 inch microphone (4939,

3 LI An-An et al: Different Forward Masking Patterns of SNB and SGNB in IC Neurons 143 B & K, Denmark) placed at the mouse s ear using a measuring amplifier (2610, B & K, Denmark), was fixed at 0 in elevation and at 60 contralateral to the middle axis of recording site in azimuth. Sound intensity was expressed in db SPL referred to 20 µpa root mean square. The distance between the loudspeaker and the mouse s ear was 30 cm. The gap between masker and probe was 30 ms and they were delivered from the loudspeaker in free field at a rate of 2 per second. 1.2 Recording procedures Recordings were carried out in a sound-proof chamber lined with anechoic foam. A small hole with diameter of 200~500 µm was drilled in the skull above the IC for inserting 3 mol/l KCl glass pipette electrodes (impedance: 5~10 MΩ). Animals were grounded through an Ag-AgCl silver wire placed at the nearby temporal muscles. Each recording electrode was inserted as orthogonally as possible and the recording depth of each neuron was read from a small screen of a hydraulic drive (David Kopf 640, USA). Upon isolation of an acoustically evoked IC neuron, its action potentials were amplified (ISO-DAM, WPI, USA). Then the neuronal activities were synchronously sent to an oscilloscope (TDS210, Tek, USA), an audio monitor (Grass AM9, USA), and a computer for acquisition of poststimulus-time histograms (PSTHs) (bin width: 0.5 ms; sampling period: 200 ms) to 32 sound presentations with a special homemade programme. By systematically changing the frequency and intensity of tone bursts, each neuron s characteristic frequency (CF) and minimum threshold (MT) were determined. 1.3 Data collection and processing Firstly, the recorded neuron s CF and MT to tone burst were determined. The MT was defined as the intensity at which the neuron responded to each of two consecutive CF tones. Then the following data were collected: (1) Each neuron s impulses of acoustical responses to CF sounds delivered at 10 db increments above the MT. (2) After addition of the SNB as a masker, the SNB intensity was systematically changed and finally determined when the firing rate induced by a 10 db above MT probe tone reduced by 30%. Note that the masker intensity was expressed as relative intensity to the corresponding probe tone s MT in present study. Then the procedure (1) was repeated. (3) The SNB was replaced by the SGNB, and then procedure (1) was repeated. Each neuron s rate-intensity function (RIF) was plotted. Statistical analysis was performed on SigmaPlot2000 and the plot of the data was performed on the software of Origin 6.0. The values given in the text and in the figures were expressed as mean±sd. t-test for independent samples was used for statistical analysis in this paper. 2 RESULTS Among 91 recorded IC neurons, the forward masking effects of SNB and SGNB were examined in 51 neurons. The recording depths, CFs and MTs of these neurons were in the range of 302~2012 µm, 5.2~46.3 khz, and 20~65 db SPL, respectively. Under condition of forward noise masking stimulation, only 4 neurons (4/51, 7.84%) responded to masker. 2.1 Distribution of masker intensities To observe the variations in relative masker intensity of IC neurons, in this study we chose to fix the gap between masker and probe (30 ms). In this scenario, the relative masker intensities at which each neuron s firing rate responding to the probe (MT+10 db tone) was inhibited by 30% were distributed over a wide range between 21 db below the MT and 19 db above the MT (Fig.1). However, the relative masker intensities of nearly half of the neurons (39.22%, 22/51) were concentrated between 0~10 db below the MT. Fig. 1. Distribution of masker intensity relative to corresponding probe tone s MT. 2.2 Comparison of the masking efficacy of the SNB with the SGNB By comparing the inhibitory effect induced by the SGNB on firing rates of neurons responding to the probe sound (intensity: MT+10 db) with the SNB, 51 neurons were divided into three types. In type I (45.10%, 23/51), the inhibition in firing rate caused by the SGNB was >15% stronger than by the SNB, whereas in type III (17.65%,

4 144 Acta Physiologica Sinica, April 25, 2006, 58 (2): Fig. 2. Representative PSTHs of three different types of IC neurons. A, B, C represent type I, II and III IC neurons. (A, B, C)-1, probe-evoked responses; (A, B, C)-2, SNB + probe; (A, B, C)-3: SGNB + probe. Unfilled rectangle, filled rectangle and filled rectangle segments represent probe, SNB, SGNB, respectively. n, number of spikes (the same in the figure 4 and 6). The CFs, MTs, masker relative intensities and recording depths of the three representative IC neurons were 7.8, 24.5, 7.6 khz; 42.6, 50.5, 31.2 db SPL; -11, -3, +6 db remt and 893, 1 652, 851 μm, respectively. 9/51) the inhibition in firing rate caused by the SGNB was <15% weaker than that by the SNB. The rest were classified as type II (37.25%, 21/51) in which the difference of inhibition between the two maskers wasn t over 15% (Fig.2). Statistical analysis showed that in type I neurons the mean inhibition caused by the SGNB was significantly stronger than that by the SNB (P<0.001, paired t- test, n=23) whereas in type III neurons the mean inhibition caused by the SGNB was significantly smaller than that by the SNB (P<0.001, paired t-test, n=9) (Fig.3). For type II neurons, there was no significant difference of inhibition between Fig. 3. Comparison of mean inhibition difference between the SNB and SGNB masking in the three types of IC neurons. the two maskers (P>0.05, paired t-test, n=19). Table 1 shows the basic properties such as the MTs, CFs, recording depths, and masker intensities of the three types of neurons. It can be found that there was a significant difference in the MTs and masker intensities between type I and type III neurons (P<0.01 and P<0.001, respectively, unpaired t- test). 2.3 Effects of the SNB and SGNB masking on the RIF The PSTHs of a representative neuron at different stimuli conditions were shown in Fig.4. After adding the SNB or SGNB, its firing rates decreased at all intensities (Probe vs SNB; Probe vs SGNB). However, this inhibition decreased with the increase of probe intensity. To evaluate inhibitory effect of masker at different probe intensities, we calculated the % inhibition in firing rate at each intensity of RIF by dividing the difference in firing rate at each intensity (Fig.5A-1, B-1, solid circles vs unfilled circles and solid triangle) by firing rate of control (solid circles). Regardless of type I or type III neurons, % inhibition of both SNB and SGNB was stronger at lower probe intensities but decreased significantly with increasing probe intensity (Fig.5A-2, B- 2, One-way ANOVA, P<0.001). In addition, the difference of either type I or type III only existed in the lower probe intensities (MT 20 db above the MT, Fig.5A-2,

5 LI An-An et al: Different Forward Masking Patterns of SNB and SGNB in IC Neurons 145 Table 1. Comparison of basic properties in the three types of IC neurons Relative noise intensity (db remt) MT (db SPL) CF (khz) Recording depth (μm) Type I (n=23) Range 21~8 21~59 5.7~ ~1922 mean±sd 6.82± ± ± ± Type II (n=9) Range 19~ 12 37~58 5.2~ ~2005 mean ±SD 5.07± ± ± ± Type III (n=19) Range 1~19 20~50 7.1~ ~2012 mean±sd 12.41± ± ± ± Fig. 4. PSTHs of a representative type I IC neuron at different probe intensities. The CF, MT, masker relative intensity and recording depth of this IC neuron was 11.2 khz, 52 db SPL, -8 db remt and 867 μm. Fig. 5. RIFs of the representative type I (A-1) and type III IC neurons (B-1) and mean inhibition of all type I ( A-2) and type III (B-2) IC neurons at all probe intensities.

6 146 B-2, solid circles vs unfilled circles, paired t- test, P< 0.001). No significant difference could be found as the probe intensity increased to 20 db above the MT (paired t- test, P>0.05). 2.4 Temporal masking pattern in type I neurons In the current study, it was interesting to study whether the temporal masking pattern of IC neurons could be changed when the masker was converted from the SNB to SGNB. Because there was a relatively smaller fraction of type III neurons we obtained and there was no obvious difference of inhibition strength between the SNB and SGNB in type II neurons, the temporal masking patterns of SNB and SGNB were examined only in type I neurons. As shown in Fig.6, the PSTHs of probe responses (control) were Acta Physiologica Sinica, April 25, 2006, 58 (2): divided into two sections by the midline (shown by arrow). Then we calculated the percentage of inhibition in firing rate occurring in the former section and the whole duration of PSTH, respectively. Three types of temporal masking patterns were observed. We found the inhibition of some neurons mainly occurring in former section (more than 60% of the total inhibition) and this temporal masking pattern was classified as early-inhibition. On the contrary, the PSTHs of some neurons exhibited late-inhibition pattern, i. e., the inhibition occurring in the former section was smaller than 40% of the whole inhibition. The inhibition of the other neurons in the former section and latter section was proportionate, thus, they were regarded as the third type, proportional-inhibition. Fig. 6. Different transformations of temporal masking patterns when the SNB was replaced by the SGNB. The arrows below the abscissa represent the midpoint of the PSTHs. The CFs, MTs, masker relative intensities and recording depths of the five representative IC neurons were 11.6, 14.3, 17.6, 21.5, 9.2 khz; 50.6, 42.5, 36.2, 48.7, 39.6 db SPL; -12, -2, -7, 2, -5 db remt and 863, 958, 1 032, 1 420, 693 μm respectively. Fig. 7. Distribution of masking patterns of the SNB and SGNB. Figure 7 shows the comparison of temporal masking patterns between SNB and SGNB. Their main difference was that, when the SNB was replaced by the SGNB, many early-inhibition patterns changed into proportional-inhibition patterns (E P). Among 23 type I neurons we examined, the forward masking patterns of 13 neurons (56.5%) were transformed. This transformation included not only E P, but also early-inhibition to late-inhibition (E L), proportional-inhibition to early-inhibition (P E), proportional-inhibition to late-inhibition (P L), and late-inhibition to proportional-inhibition pattern (L P) (Fig.6).

7 LI An-An et al: Different Forward Masking Patterns of SNB and SGNB in IC Neurons DISCUSSION 3.1 Comparison with previous studies of noise masking In natural acoustic environment, a signal of interest is usually masked by noise originating from spatially and temporally discrete sources [12]. Therefore, most auditory psychophysical and neurophysiological investigations on noise masking have intensively focused on the effects of the separation of signal and noise in space and time [1,2,5-8]. As expected, a vast majority of data have documented that noise masking effect, both in central auditory neuron s responses and in human perception, decreases with the separation of noise and signal in space and time. In the present study, the gap between masker and probe for all recorded neurons was fixed at 30 ms. The procedure gave us an opportunity to observe the intensity relationship between the masker and the probe. We found that the distribution of masker intensity had a very wide variance ranged from 21 db below MT to 19 db above MT relative to the probe (Fig.1), suggesting that IC neurons had diverse capacity for resisting noise masking. This is highly consistent with the previous observation reported by Barsz et al. They found that some IC neurons were sensitive to background noise whereas others displayed noise resistant under the paradigm of simultaneously noise masking [13]. Similarly, there are many studies showing that when the masker intensity was fixed the gap was also distributed over a wide range. For example, in the IC neurons of cat, when the responses induced by the probe decreased by 50% as the same masker intensity was used, the gaps between the probe and masker were ranged from 2 to 100 ms [8]. Similar data were also obtained in AC [6], cochlear nucleus [14] and auditory nerve [15]. Our results taken together with these investigations reveal that there is a negative summation of wide scope not only in time domain but also in intensity domain for noise masking. Psychophysical results also showed that the increase in the level of the probe reduces echo thresholds and an opposite effect occurs when the probe level decreases. The current experiment demonstrated that inhibitory strength of noise, irrespective of the SNG or SGNB, was typically stronger at lower probe intensity but decreased with increasing probe intensity (Fig.4, 5). It closely mirrors our previous observations of simultaneously noise masking in the mouse and two-tone inhibition in the bat [9,16,17]. This result implies that the inhibitory effect of forward masking may be determined by a dynamic balance of excitatory and inhibitory input upon the recorded neurons. Our conjecture was further annotated by Fig.5 in which the significant difference of masking effect between the SNB and SGNB, regardless of type I or III neurons, disappeared when the intensity of the probe was much higher (20 db above MT or more), demonstrating that at higher probe intensity excitatory input dominates the forward masking summation. 3.2 Correlation of temporal summation and different masking patterns The main interest of present study is to explore the difference of the masking effect between the SNB and SGNB. Unexpectedly, the two contrary results were obtained. In nearly half of neurons (type I), the masking effect of SGNB was much greater than that of SNB whereas in a smaller fraction of neurons (type III), the opposite effect was observed. By comparing their basic properties we noticed that they had significant difference in the MT and masked intensity (Table 1). The masker intensities of type I neurons were lower than that of type III neurons, strongly suggesting that type I neurons may be more sensitive to noise, and the different masking effect of the SNB and SGNB is most likely related to the basic features of IC neurons. On the other hand, in recent years there are many studies conducted on brain slice showing the lower repetitive stimulation on presynaptic input produces temporal facilitation of postsynaptic potentials during synaptic transmission [18,19]. However, the temporal facilitation could be replaced by temporal inhibition at higher repetitive stimulation, demonstrating that the efficiency of synaptic transmission is dynamically modulated by different pulse repetition rates. Hence, we speculate that the inhibitory postsynaptic potential (IPSP) induced by the SGNB in type I neurons might be greater than that by the SNB whereas in type III neurons the negative summation strength of the SGNB was weaker than that of the SNB. In other words, the temporal summation characteristic of synaptic transmission play a key role in shaping the forward masking patterns of SNB and SGNB. Besides the observation of masking strength difference between SNB and SGNB, what is more interesting, but less explored in the past, is our examination of the negative summation in time domain. We noted that when the SNB was replaced by the SGNB as a masker, the negative summation patterns in more than half of neurons (13/23, 56.52%) were changed (Fig.6). Among these changed neurons, many of them (7/13, 53.85%) were changed from early-inhibition to proportional-inhibition pattern (E P) (Fig.7), moreover, the other transformation including E L, P E, P L, and L P (Fig.6) can be found, revealing

8 148 that in type I neurons the forward masking of the SGNB not only caused more effective inhibition in firing rate than the SNB, but also changed the temporal summation pattern. Lots of reports have pointed out that the inhibitory response in the IC neurons is mediated by GABA A and glycine receptors. GABAergic inhibition dominates over the sustained period of the neuronal firing while glycinergic inhibition is more effective in the early part of the response [18, 20-22]. GABAergic activity is an important cellular mechanism underlying the normal balance of excitation and inhibition and serves as a gate to control activation and modulation of ongoing activity mediated by glutamate receptors. Our data taken together with these in vivo and in vitro investigations make it most likely that the masking pattern transformation is attributable to the different ration of GABAergic/glycinergic input and different temporal activation pattern of GABAergic inhibition induced by SNB and SGNB. 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