Encoding of sound duration by neurons in the auditory cortex of the little brown bat, Myotis lucifugus

Responses of 117 single- or multi-units in the auditory cortex (AC) of bats (Myotis lucifugus) to tone bursts of different stimulus durations (1– 400 ms) were studied over a wide range of stimulus intensities to determine how stimulus duration is represented in the AC. 36% of AC neurons responded more strongly to short stimulus durations showing short-pass duration response functions, 31% responded equally to all pulse durations (i.e., all-pass), 18% responded preferentially to stimuli having longer durations (i.e., long-pass), and 15% responded to a narrow range of stimulus durations (i.e., band-pass). Neurons showing long-pass and short-pass duration response functions were narrowly distributed within two horizontal slabs of the cortex, over the rostrocaudal extent of the AC. The effects of stimulus level on duration selectivity were evaluated for 17 AC neurons. For 65% of these units, an increase in stimulus intensity resulted in a progressive decrease in the best duration. In light of the unusual intensity-dependent duration responses of AC neurons, we hypothesized that the response selectivities of AC neurons is different from that in the brainstem. This hypothesis was validated by results of study of the duration response characteristics of single neurons in the inferior colliculus. Accepted: 8 November 1996     

恒频-调频蝙蝠下丘神经元的恢复周期决定声脉冲跟随率

为探究恒频-调频蝙蝠下丘神经元恢复周期特点及其对声脉冲跟随率的影响,实验采用模拟的大蹄蝠(Hipposideros armiger)自然状态下的恒频-调频发声信号为声刺激,在5只听力正常的大蹄蝠上记录了下丘神经元的声反应和恢复周期(n = 93)．结果发现,根据神经元恢复率达50%时的双声刺激间隔(inter pulse interval,IPI),可将其分为长时恢复型(long recovery,LR;47.4%)、中等时间恢复型(moderate recovery,MR;35.1%)和短时恢复型(short recovery,SR;17.5%)．每种类型依据其恢复率随IPI增加而呈现的不同变化又可进一步分为单IPI反应区神经元,多IPI反应区神经元,以及单调IPI反应神经元．LR,MR和SR型神经元恢复率达50%时的平均IPI分别为(64.0 ± 24.8),(19.6 ± 5.8)和(7.1 ± 2.4) ms (P < 0.001),相对应的平均理论每秒声脉冲数分别为(18.2 ± 7.0),(55.4 ± 15.7)和(171.3 ± 102.9) Hz (P < 0.001)．结果提示,单IPI和多IPI反应区神经元具有特殊IPI反应特性,能对蝙蝠捕食和巡航期间所处的时相做出准确判断,而单调IPI反应神经元对IPI变化的敏感性较强,但时相判断性较差．另外LR,MR和SR型神经元恢复周期和理论脉冲跟随率的平均结果均能与这种蝙蝠回声定位期间3个时相的发声行为相匹配,且神经元恢复周期参与决定声脉冲跟随率,满足了蝙蝠巡航、捕食的行为学需要．     

Recovery cycle of neurons in the inferior colliculus of the FM bat determined with varied pulse-echo duration and amplitude

The recovery cycle of auditory neurons is an important neuronal property which underlies a bat's ability in analyzing returning echoes and to determine target distance (i.e., echo ranging). In the same token, duration selectivity of auditory neurons plays an important role in pulse recognition in bat echolocation. Because insectivorous bats progressively vary the pulse parameters (repetition rate, duration, and amplitude) during hunting, the recovery cycle of auditory neurons is inevitably affected by their selectivity to other co-varying echo parameters. This study examines the effect of pulse duration and amplitude on recovery cycle of neurons in the central nucleus of the inferior colliculus (IC) of the FM bat, Pipistrellus abramus, using biologically relevant pulse-echo (P-E) pairs with varied duration and amplitude difference. We specifically examine how duration selectivity may affect a neuron's recovery cycle. IC neurons have wide range of recovery cycle and best duration (BD) covering P-E intervals and duration occurring different phases of hunting. The recovery cycle of most IC neurons increases with P-E duration and amplitude difference. Most duration-selective IC neurons recover rapidly when stimulated with biologically relevant P-E pairs. As such, neurons with short BD recover rapidly when stimulated with P-E pairs of short duration and small P-E amplitude difference. Conversely, neurons with long BD recover rapidly when stimulated with P-E pairs of long duration and large P-E amplitude difference. These data suggest that bats may potentially utilize the response of IC neurons with different BD and recovery cycle to effectively perform echo detection, recognition of echo duration and echo ranging throughout a target approaching sequence.     

Duration selectivity of bat inferior collicular neurons improves with increasing pulse repetition rate

Insectivorous big brown bats, Eptesicus fuscus, progressively increase the pulse repetition rate (PRR) throughout the course of hunting. While increasing PRR conceivably facilitates bats to extract information about the targets, it also inevitably affects sensitivity of their auditory neurons to pulse parameters. The present study examined the effect of increasing PRR on duration selectivity of this bat's inferior collicular (IC) neurons by comparing their impulse-duration functions determined at different PRRs. Impulse-duration functions plotted with the number of impulses in response to single pulses against pulse duration at different PRRs were described as short-pass, band-pass, long-pass, and all-pass. Short- or long-pass neurons discharged maximally to a range of short or long pulse durations. Band-pass neurons discharged maximally to one pulse duration. These three types of IC neurons were called duration tuned neurons. All-pass neurons were not duration tuned because they did not discharge maximally to any pulse duration. Increasing PRR improved duration selectivity of IC neurons by (1) increasing the number of duration tuned neurons; (2) decreasing the critical duration concomitant with increasing slope of the impulse-duration function; and (3) decreasing the 50% duration range of the impulse-duration function. This improved duration selectivity with PRR may potentially facilitate prey capture by bats.     

The influence of stimulus duration on the delay tuning of cortical neurons in the FM bat,Myotis lucifugus

1. Echolocating bats use echo delay as the primary cue to determine target distance. During target-directed flight, the emitted pulses increase in repetition rate and shorten in duration as distance decreases. To determine how these parameters affect the delay tuning of neurons in the auditory cortex of the awake bat, Myotis lucifugus, we examined the responses of 104 delay-sensitive neurons as the pulse repetition rate (PRR) and duration were independently varied. Stimulus duration of 4, 2 and 1 ms and PRR of 5-100/s were used for both the pulse and echo to determine delay sensitivity. These parameter ranges span those used during the search, approach, and the initial terminal phases of echolocation. 2. As the stimulus duration was shortened, the range of PRRs for delay sensitivity was extended to higher rates in 41% of the neurons, narrowed or disappeared in 40%, and remained unchanged in 4%. The remaining 15% were not categorized since it was not possible to determine a trend in which the range of delay-sensitive PRRs changed with stimulus duration. 3. Three types of tracking neurons (i.e., neurons that change their best delay during target-directed flight) were found. For the first type, the best delay (BD) shortened with shorter stimulus duration, for the second type, BD shortened with both shorter stimulus durations and higher PRRs, and for the third type, BD shortened with higher PRRs. 4. These results suggest that the stimulus parameters of sonar emission influence delay tuning and hence processing by cortical neurons in FM bats.     

不同时程弱前掩蔽声对小鼠下丘神经元声反应的选择性抑制

自由声场条件下,以强度为神经元最小阈值阈上5dB,时程分别为40、60、80和100ms的纯音作为前掩蔽声,观察和记录了不同时程弱前掩蔽声对小鼠（Musmusculus Km）下丘神经元发放和声强处理的影响。实验记录到154个神经元,对其中的104个神经元做了不同时程掩蔽声影响的测试。结果发现：掩蔽声对神经元放电率的抑制作用在时间上表现为前抑制（41％）、后抑制（9％）和全抑制（50％）三种类型。改变掩蔽声时程时,大部分神经元（72％）的抑制类型不发生改变,但少部分神经元（28％）随掩蔽声时程的增加,大量的后抑制类型转变为前抑制或全抑制类型。此外,超过一半的神经元（58．06％）其强度．放电率函数曲线随掩蔽声时程的改变而发生转变,主要表现为单调型向饱和型转变及饱和型向非单调型转变,这种转变并不随掩蔽声时程增加表现出规律性的变化。结果表明,前掩蔽作用于下丘神经元声反应的时间域和强度域时具有不均衡性,推测不同时程弱前掩蔽声激活的抑制性输入能分化性调制下丘神经元声反应特性。     

Intracellular responses of antennal chordotonal sensilla of the American cockroach

The responses of mechanoreceptor neurons in the antennal chordotonal organ have been examined in cockroaches by intracellular recording methods. The chordotonal organ was mechanically stimulated by sinusoidal movement of the flagellum. Stimulus frequencies were varied between 0.5 and 150 Hz. Receptor neurons responded with spike discharges to mechanical stimulation, and were classed into two groups from plots of their average spike frequencies against stimulus frequency. Neurons in one group responded to stimulation over a wide frequency range (from 0.5 to 150 Hz), whereas those in a second group were tuned to higher frequency stimuli. The peak stimulus frequency at which receptor neurons showed maximum responses differed from cell to cell. Some had a peak response at a stimulus frequency given in the present study (from 0.5 to 150 Hz), whereas others were assumed to have peak responses beyond the highest stimulus frequency examined. The timing for the initiation of spikes or of a burst of spikes plotted against each stimulus cycle revealed that spike generation was phase-locked in most cells. Some cells showed phase-independent discharges to stimulation at lower frequency, but increasing stimulus frequencies spike initiation began to assemble at a given phase of the stimulus cycle. The response patterns observed are discussed in relation to the primary process of mechanoreception of the chordotonal organ.     

Masking effect of different durations of forward masker sound on acoustical responses of mouse inferior collicular neurons to probe sound

To study the effects of different durations of forward masker sound on neuronal firing and rate-intensity function(RIF)of mouse inferior collicular(IC)neurons,a tone relative to 5 dB above the minimum threshold(re MT+5 dB)of the best frequency of recorded neurons was used as forward masker sound under free field stimulation condition.The masker durations used were 40,60,80,and 100 ms.Results showed that as masker duration was increased,inhibition in neuronal firing was enhanced(P＜0.0001,n=41)and the latency of neurons was lengthened(P＜0.01,n=41).In addition,among 41 inhibited IC neurons,90.2%(37/41)exhibited narrowed dynamic range(DR)when masker sound duration was increased(P＜0.0001),whereas the DR of 9.8%(4/41)became wider.These data suggest that masking effects of different durations of forward masker sound might be correlated with the amplitude and duration of inhibitory input to IC neurons elicited by the masker sound.     

Dose-dependent response characteristics of antennal lobe neurons in the male moth Agrotis segetum (Lepidoptera: Noctuidae)

Responses of antennal lobe neurons to different amounts of the female-produced pheromone blend and to its individual components were investigated in Agrotis segetum males using intracellular recording methods. We identified three physiological types of antennal lobe neurons, categorized according to their response thresholds to single pheromone components and to the blend: generalist neurons, component-specific neurons and blend-specific neurons. Response and specificity of antennal lobe neurons were largely dose dependent. In most cases specific responses occurred only at low stimulus amounts, while increasing concentrations often resulted in an increase of the number of pheromone stimuli to which the neuron responded. Dose-response relationships often differed between different stimuli activating a neuron. Accepted: 24 May 1997     

GABA-mediated echo duration selectivity of inferior collicular neurons of Eptesicus fuscus, determined with single pulses and pulse–echo pairs

When insectivorous bats such as Eptesicus fuscus emit ultrasonic signals and analyze the returning echoes to hunt insects, duration selectivity of auditory neurons plays an important role in echo recognition. The success of prey capture indicates that they can effectively encode progressively shortened echo duration throughout the hunting process. The present study examines the echo duration selectivity of neurons in the central nucleus of the bat inferior colliculus (IC) under stimulation conditions of single pulses and pulse–echo (P–E) pairs. This study also examines the role of gamma-aminobutyric acid (GABA)ergic inhibition in shaping echo duration selectivity of IC neurons. The data obtained show that the echo duration selectivity of IC neurons is sharper when determined with P–E pairs than with single pulses. Echo duration selectivity also sharpens with shortening of pulse duration and P–E gap. Bicuculline application decreases and GABA application increases echo duration selectivity of IC neurons. The degree of change in echo duration selectivity progressively increases with shortening of pulse duration and P–E gap during bicuculline application while the opposite is observed during the GABA application. These data indicate that the GABAergic inhibition contributes to sharpening of echo duration selectivity of IC neurons and facilitates echo recognition by bats throughout different phases of hunting.     

Parallel processing of afferent input by identified interneurones in the auditory pathway of the noctuid moth Noctua pronuba (L.)

1. Interneurones 501 and 504 are identified sound-sensitive interneurones in the pterothoracic ganglion of the noctuid moth Noctua pronuba. Both neurones receive monosynaptic input from the A1 afferent and experiments with current injection suggest that the synapse is chemical. The EPSPs evoked in either IN 501 or 504 by the A1 afferent do not facilitate. 2. Temporal integration in INs 501 and 504 was compared by presenting the moth with tones at repetition rates found in the search, approach and terminal phases of the echolocating call of a hunting bat. INs 501 and 504 differ in their capacity to resolve stimulus repetition rates because the mean decay times of their compound EPSPs differ by a factor of three, although both interneurones receive monosynaptic input from the A1 afferent. 3. The features extracted from the authentic, prerecorded, call of an echolocating bat at the level of the pterothoracic ganglion were examined by recording sequentially from a range of interneurones in the same preparation. The capacity of INs 501 and 504 to encode the various phases of the call was examined in the light of their measured mean decay times and related to the avoidance behaviour of the insect.     

抑制性频谱整合对大棕蝠下丘神经元声强敏感性的影响

自由声场条件下 ,采用特定双声刺激方法研究了不同频率通道之间的非线性整合对下丘神经元声强敏感性的调制作用。实验在 1 2只麻醉与镇定的大棕蝠 (Eptesicusfuscus)上进行 ,双电极同步记录 2个配对神经元的声反应动作电位。主要结果如下 :1 )所获 1 1 0个 (5 5对 )配对神经元中 ,85 5 %表现为抑制性频谱整合作用 ,其余 1 4 5 %为易化性频谱整合 ;2 )阈上 1 0dB (SPL)放电率抑制百分比与神经元最佳频率 (BF)及记录深度呈负相关 ;3)抑制效率随声刺激强度升高而逐步下降 ;4 )当掩蔽声分别位于神经元兴奋性频率调谐曲线(FTC)内 (MSin) /外 (MSout)时 ,其抑制效率存在差异。前者的放电率抑制百分比及声反应动力学范围(DR)下降百分比均显著高于后者 ;5 )抑制性频谱整合导致 3类DR改变 :6 1 6 %为下降、 1 0 9%增加、另有2 7 5 %变化小于 1 0 %。本结果进一步支持如下设想 :下丘不同频率通道之间的抑制性频谱整合参与了对强度编码的主动神经调制活动     

Response dynamics of bullfrog ON-OFF RGCs to different stimulus durations

Stimulus duration is an important feature of visual stimulation. In the present study, response properties of bullfrog ON-OFF retinal ganglion cells (RGCs) in exposure to different visual stimulus durations were studied. By using a multi-electrode recording system, spike discharges from ON-OFF RGCs were simultaneously recorded, and the cells’ ON and OFF responses were analyzed. It was found that the ON response characteristics, including response latency, spike count, as well as correlated activity and relative latency between pair-wise cells, were modulated by different light OFF intervals, while the OFF response characteristics were modulated by different light ON durations. Stimulus information carried by the ON and OFF responses was then analyzed, and it was found that information about different light ON durations was more carried by transient OFF response, whereas information about different light OFF intervals were more carried by transient ON response. Meanwhile, more than 80 % information about stimulus durations was carried by firing rate. These results suggest that ON-OFF RGCs are sensitive to different stimulus durations, and they can efficiently encode the information about visual stimulus duration by firing rate.     

Sound-evoked oscillation and paradoxical latency shift in the inferior colliculus neurons of the big fruit-eating bat, <Emphasis Type="Italic">Artibeus jamaicensis</Emphasis>

Frequency tuning, temporal response pattern and latency properties of inferior colliculus neurons were investigated in the big fruit-eating bat, Artibeus jamaicensis. Neurons having best frequencies between 48–72 kHz and between 24–32 kHz are overrepresented. The inferior colliculus neurons had either phasic (consisting in only one response cycle at all stimulus intensities) or long-lasting oscillatory responses (consisting of multiple response cycles). Seventeen percent of neurons displayed paradoxical latency shift, i.e. their response latency increased with increasing sound level. Three types of paradoxical latency shift were found: (1) stable, that does not depend on sound duration, (2) duration-dependent, that grows with increasing sound duration, and (3) progressive, whose magnitude increases with increasing sound level. The temporal properties of paradoxical latency shift neurons compare well with those of neurons having long-lasting oscillatory responses, i.e. median inter-spike intervals and paradoxical latency shift below 6 ms are overrepresented. In addition, oscillatory and paradoxical latency shift neurons behave similarly when tested with tones of different durations. Temporal properties of oscillation and PLS found in the IC of fruit-eating bats are similar to those found in the IC of insectivorous bats using downward frequency-modulated echolocation calls.     

Neurons in the inferior colliculus of the big brown bat show maximal amplitude sensitivity at the best duration

The big brown bats, Eptesicus fuscus, emit ultrasonic signals and analyze the returning echoes in multi-parametric domains to extract target features. The variation of different pulse parameters during hunting predicts that analysis of an echo parameter by bats is inevitably affected by other co-varying echo parameters. In this study, we presented data to show that the bat inferior collicular (IC) neurons have maximal amplitude sensitivity at the best duration (BD). A family of rate-amplitude function (RAF) of each IC neuron is plotted with the BD and non-BD sound pulses. The RAF plotted with BD pulses has sharper slope (SL) and smaller dynamic range (DR) than the RAF plotted with non-BD pulses has. All RAFs can be described as monotonic, saturated or non-monotonic. IC neurons with monotonic RAF are mostly recorded at deeper IC and they have the largest average BD, best amplitude (BA) and DR. Conversely, IC neurons with non-monotonic RAF are mostly recorded at upper IC and they have the smallest average BD, BA and DR. Low best frequency (BF) neurons at upper IC have shorter BD, smaller BA and DR than high BF neurons at deeper IC have. These data suggest that IC neurons that tune to an echo duration also have the greatest sensitivity to echo amplitude. These data also suggest that sensitivity in frequency, duration and amplitude appears to be orderly represented along the dorso-ventral axis of the IC.     

Latency represents sound frequency in mouse IC

Frequency is one of the fundamental parameters of sound.The frequency of an acoustic stimulus can be represented by a neural response such as spike rate,and/or first spike latency(FSL)of a given neuron.The spike rates/frequency function of most neurons changes with different acoustic ampli-tudes,whereas FSL/frequency function is highly stable.This implies that FSL might represent the fre-quency of a sound stimulus more efficiently than spike rate.This study involved representations of acoustic frequency by spike rate and FSL of central inferior colliculus(IC)neurons responding to free-field pure-tone stimuli.We found that the FSLs of neurons responding to characteristic frequency(CF)of sound stimulus were usually the shortest,regardless of sound intensity,and that spike rates of most neurons showed a variety of function according to sound frequency,especially at high intensities.These results strongly suggest that FSL of auditory IC neurons can represent sound frequency more precisely than spike rate.     

Latency represents sound frequency in mouse IC

Frequency is one of the fundamental parameters of sound. The frequency of an acoustic stimulus can be represented by a neural response such as spike rate, and/or first spike latency (FSL) of a given neuron. The spike rates/frequency function of most neurons changes with different acoustic amplitudes, whereas FSL/frequency function is highly stable. This implies that FSL might represent the frequency of a sound stimulus more efficiently than spike rate. This study involved representations of acoustic frequency by spike rate and FSL of central inferior colliculus (IC) neurons responding to free-field pure-tone stimuli. We found that the FSLs of neurons responding to characteristic frequency (CF) of sound stimulus were usually the shortest, regardless of sound intensity, and that spike rates of most neurons showed a variety of function according to sound frequency, especially at high intensities.These results strongly suggest that FSL of auditory IC neurons can represent sound frequency more precisely than spike rate.     

GABA能抑制调制大棕蝠下丘神经元对串声刺激的强度敏感性

本文采用不同重复率的串声刺激,模拟大棕蝠回声定位不同阶段听到的调频声纳信号,利用电生理方法和微电泳技术研究不同重复率串刺激条件下GABA能抑制对下丘神经元强度敏感性的影响。结果发现,随串刺激重复率的增加,有的神经元强度敏感性增强,有的神经元强度敏感性则降低。在不同串刺激条件下,微电泳荷包牡丹碱,神经元放电率均增加,随重复率增加强度敏感性增强或减弱的趋势消失,提示GABA能抑制调制下丘神经元对不同重复率串刺激反应的强度敏感性。串刺激强度在最低闽值附近时,微电泳荷包牡丹碱导致放电率增加的百分率最大,随串刺激强度增加,放电率增加的百分率逐渐减小。提示刺激强度较低时,GABA能抑制对下丘神经元强度敏感性的影响更有效。     

Analysing neuronal correlates of the comparison of two sequentially presented sensory stimuli

In a typical sequential sensory discrimination task, subjects are required to make a decision based on comparing a sensory stimulus against the memory trace left by a previous stimulus. What is the neuronal substrate for such comparisons and the resulting decisions? This question was studied by recording neuronal responses in a variety of cortical areas of awake monkeys (Macaca mulatta), trained to carry out a vibrotactile sequential discrimination task. We describe methods to analyse responses obtained during the comparison and decision phases of the task, and describe the resulting findings from recordings in secondary somatosensory cortical area (S2). A subset of neurons in S2 become highly correlated with the monkey''s decision in the task.     

Single unit activity of dopaminergic neurons in freely moving cats

Single unit activity was recorded from the area of the substantia nigra in freely moving cats. A sub-population of these neurons had the following characteristics: long action potential durations (2–4 msec); relatively slow discharge rates (2–6 spikes/sec); firing as single spikes along with periods of bursting activity in which spike amplitude successively decreased; suppression of unit activity by systemic injection of apomorphine and increased activity after systemic injection of haloperidol. These characteristics are similar to those of identified dopamine neurons recorded in chloral hydrate anesthetized or peripherally paralyzed rats. Therefore, based upon these physiological and pharmacological similarities, this study represents the first systematic report providing evidence for recording the activity of dopaminergic neurons in freely moving cats. In addition, when these cells were studied across the sleep-waking cycle they displayed little variation in firing rates between waking, slow wave sleep and REM sleep.