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The Journal of Neuroscience, June 1, 2003, 23(11):4717-4725
Previous Article | Next Article
Corollary Discharge Inhibition of Ascending Auditory Neurons in the Stridulating Cricket
James F. A. Poulet andBerthold Hedwig Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, United Kingdom
Abstract
Top
Abstract
Introduction
Acoustically communicating animals are able to process external acoustic stimuli despite generating intense sounds during vocalization. We have examined how the crickets' ascending auditory pathway copes with self-generated, intense auditory signals (chirps) during singing (stridulation). We made intracellular recordings from two identified ascending auditory interneurons, ascending neuron 1 (AN1) and ascending neuron 2 (AN2), during pharmacologically elicited sonorous (two-winged), silent (one-winged), and fictive (isolated CNS) stridulation.During sonorous chirps, AN1 responded with bursts of spikes, whereas AN2 was inhibited and rarely spiked. Low-amplitude hyperpolarizing potentials were recorded in AN1 and AN2 during silent chirps. The potentials were also present during fictive chirps. Therefore, they were the result of a centrally generated corollary discharge from the stridulatory motor network. The spiking response of AN1 and AN2 to acoustic stimuli was inhibited during silent and fictive chirps. The maximum period of inhibition occurred in phase with the maximum spiking response to self-generated sound in a sonorously stridulating cricket. In some experiments (30%) depolarizing potentials were recorded during silent chirps. Reafferent feedback elicited by wing movement was probably responsible for the depolarizing potentials.
In addition, two other sources of inhibition were present in AN1: (1) IPSPs were elicited by stimulation with 12.5 kHz stimuli and (2) a long-lasting hyperpolarization followed spiking responses to 4.5 kHz stimuli. The hyperpolarization desensitized the response of AN1 to subsequent quieter stimuli. Therefore, the corollary discharge will reduce desensitization by suppressing the response of AN1 to self-generated sounds.
Key words: corollary discharge; efference copy; stridulation; presynaptic inhibition; postsynaptic inhibition; ascending neuron 1; ascending neuron 2
Introduction
Sensory processing is generally studied by presenting stimuli to resting or anesthetized animals. However, in their natural environment, an animal's sensory systems will respond both to external sensory information and to sensory information generated as a byproduct of its behavior. To cope with intense self-generated, or reafferent (von Holst and Mittelstaedt, 1950), sensory information many animals reduce the sensitivity of their sensory pathway while generating reafferent information (Murphey and Palka, 1974
In the cricket's auditory pathway, information ascends from the prothoracic ganglion to the brain via ascending auditory interneurons. Ascending neuron 1 (AN1) responds best to 4.5 kHz, the carrier frequency of calling song, and is thought to process conspecific sounds (Boyan, 1980
Materials and Methods
Details of all methods used have been described previously (Poulet and Hedwig, 2003Repetitive acoustic stimuli were presented with a short duration (8 msec) and period (15 msec) at 75 dB sound pressure level (SPL) relative to 20 µPa root mean square (RMS) to obtain as many data points as possible throughout the chirp and chirp interval. To mimic cricket calling song, stimuli had the natural syllable duration (21 msec), period (42 msec), intensity (100 dB SPL RMS), and frequency (4.5 kHz). Stimuli presented to AN2 during silent stridulation had a duration of 21 msec, an intensity of 75 dB SPL (RMS), and a period of 250 msec. The relatively long period gave AN2 sufficient recovery time. Acoustic stimuli had a carrier frequency of 4.5 or 12.5 kHz. All analysis was done using the software packages Neurolab (Knepper and Hedwig, 1997
Results
Responses of AN1 and AN2 to external acoustic stimuli in resting crickets
The dendritic branches and ascending axons of AN1 and AN2 are located contralateral to their soma in the auditory neuropil of the prothoracic ganglion, in which they make monosynaptic connections to auditory afferents (Wohlers and Huber, 1982
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Figure 1. Responses of AN1 and AN2 to 4.5 and 12.5 kHz stimulation. Acoustic stimuli of 4.5 kHz elicit a burst of 4 spikes in AN1 (A), whereas at 80 dB SPL, 12.5 kHz stimuli cause a mix of excitation and inhibition in AN1 (B). Acoustic stimuli of 75 dB SPL, 4.5 kHz causes IPSPs in AN2 (C), whereas 75 dB SPL, 12.5 kHz stimuli elicit a burst of spikes (D). AN1,Intracellular recording of AN1; AN2, intracellular recording of AN2;Acoustic Stimuli, sound pulses.
Responses of AN1 and AN2 during sonorous stridulation
Stridulating male Gryllus bimaculatus rub their forewings together to generate 100 dB SPL sound pulses, generally termed syllables, with a carrier frequency of 4.5 kHz; these are arranged into chirps (Fig. 2Ai). During sonorous chirps, AN1 was rhythmically excited and produced bursts of spikes in phase with the syllables (Fig. 2A, asterisks). Wing opening at the start of a chirp produced a quiet sound (Fig. 2Ai, arrow 1) that caused a depolarizing potential in AN1 (Fig. 2Ai, arrow 2) and sometimes a spike. Thereafter, AN1 produced bursts of spikes in response to the louder syllables generated during wing closing (Fig. 2Ai, asterisk). Quantitative evaluation of the response of AN1 during sonorous stridulation shows the peristimulus time (PST) histogram overlaid with the spike frequency (Fig. 2Aii, top traces) along with the average wing movement (Fig. 2Aii, middle trace) and rectified sound recording (Fig. 2Aii, bottom trace). The spiking response correlates with the sound intensity, with the loudest syllable, generated during wing closing (Fig. 2Aii, asterisk), causing the strongest spiking response, during wing opening (Fig. 2Aii, dashed line). On average, AN1 reached a maximum spike frequency of 183 ± 25 Hz during sonorous chirps (mean ± SEM, n = 6 crickets).
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Figure 2. Activity of auditory neurons during sonorous singing. Ai, AN1 responded to the loud syllables (asterisk) produced during the chirp. The quieter sounds (arrow1) caused by wing opening generated a depolarizing potential (arrow 2), which occasionally elicited a spike. Wing opening and closing are marked at the side of the wing recording. Aii, The PST histogram and the overlaid, averaged spike frequency (top), averaged wing movement (middle), and rectified sound recording (bottom) show that the response of AN1 is in phase with sound production. The peak response of AN1 occurs during the closing wing movements and is indicated by a dashed line. Bi, AN2 was inhibited during sonorous chirps, an IPSP was generated in response to the initial quiet sound produced by opening wing movement (arrow 3) and in response to each loud sound generated during wing closing (arrow 4). Between each IPSP, AN2 rapidly repolarized (asterisk). A chirp, chirp interval, and syllables are marked below the recording. Bii, The PST histogram and overlaid spike frequency show that AN2 rarely spiked during sonorous stridulation. Crickets above the figures symbolize two-winged, one-winged, or fictive singing with or without ears (see Figs. 3, 4, 5, 6, 7, 8, 9, 10). Wing, Stridulatory wing movements; Sound, microphone recording; AP, Action potential.
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Figure 3. Low-amplitude hyperpolarizations were normally observed in both AN1 (Ai) and AN2 (Bi) during silent one-winged chirps. Superpositions of AN1 (Aii) and AN2 (Bii) (top traces), triggered by the onset of the wing movement (bottom traces), demonstrate the time course of the hyperpolarizations in relation to the average wing movement. They began just after the start of the closing wing movements, indicted by the dashed lines, and reached a maximum during the consecutive wing opening movements, indicated by the solid line. For additional details see Figure 2.
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Figure 4. Ai, Bi, Depolarizations were sometimes observed in recordings of AN1 and AN2 during silent one-winged stridulation. Superimposed recordings of AN1 (Aii) and AN2 (Bii) together with the averaged wing movement and sound demonstrate the timing of the depolarizations in relation to the wing movement. The timing varied from animal to animal. In general, the depolarizations started during wing closing and peaked at the transition from closing to opening. The spikes have been truncated in the superpositions. For additional details see Figure 2.
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Figure 5. Response of AN1 and AN2 to wing movement in deafened crickets. EPSPs were elicited in AN1 (A) and AN2 (B) during manual wing movement in deafened crickets. For additional details see Figure 2.
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Figure 6. Activity of AN1 and AN2 during fictive stridulation. Low-amplitude hyperpolarizations were recorded in AN1 (Ai) and AN2 (Bi) during the fictive chirps with the similar amplitude and timing as in silently stridulating crickets. Fictive chirps are indicated by thoracic motor activity. Aii, Bii, Superimposed traces of neuron recordings (top) show the timing of the PADs and IPSPs in relation to the averaged, rectified mesothoracic nerve 3A recording (bottom). Meso Nv 3A, Extracellular nerve recording with several units of opener and closer motor neuron activity. For additional details see Figure 2.
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Figure 7. Response of AN1 and AN2 to acoustic stimuli during silent stridulation. Ai, The spiking response of AN1 to a train of sound pulses (4.5 kHz, 75 dB SPL, 7 msec duration, 15 msec interval) is inhibited during the chirps (asterisk). Aii, Quantitative analysis showing the PST histogram with the superimposed spike frequency (top), the averaged wing movement (middle), and the distribution of the sound stimuli (bottom) shows a clear inhibition of the response of AN1 during silent chirps. The inhibition began at the start of the first wing closing, as indicated by the dashed line. Bi, AN2 responded to a train of sound stimuli (12.5 kHz, 75 dB SPL, 7 msec duration, 15 msec interval) during the chirp intervals, but its response was inhibited during the chirps. EPSPs were recorded during the chirp (asterisk), and occasionally spikes were recorded on top of the larger EPSPs during the transition between closing and opening wing movement. Bii, Again the PST histogram and the average spike frequency of the response of AN2 show a clear reduction during the chirp that began at the start of wing closing, as indicated by the dashed line. The bottom PST histogram in Aii and Bii shows that the sound stimuli were evenly distributed throughout the chirp and the chirp interval. For additional details see Figure 2.
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Figure 8. Auditory responses to acoustic stimulation during fictive singing. Ai, AN1 spiked to the sequence of 4.5 kHz, 75 dB SPL acoustic stimuli during the chirp interval, but was inhibited during the chirp.Aii,Inhibition during the chirp was clearly demonstrated by the PST histogram, with an overlaid average spike rate. Bi, The spiking response of AN2 to 12.5 kHz acoustic stimuli was inhibited during the fictive chirps but not during the chirp intervals. Bii, The PST histogram and overlaid average spike rate (top) of the response of AN2 to acoustic stimuli (bottom) show an inhibition of the response of AN2 during the fictive chirp, as indicated by the rectified and averaged motor activity (middle). For additional details see Figure 2.
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Figure 9. Effectiveness of the centrally generated inhibition during silent stridulation. A, AN1 responded to 100 dB SPL, 4.5 kHz acoustic stimuli during the chirp intervals (black) with bursts of spikes. The strength of response was reduced during the chirps (gray). B, AN2 responded to 12.5 kHz, 75 dB SPL acoustic stimuli with bursts of spikes during the chirp interval (black). The response was reduced during the chirp (gray). For additional details see Figure 2.
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Figure 10. Timing of the centrally generated inhibition in AN1. The maximum spike frequency of AN1 to individual 4.5 kHz, 100 dB SPL stimuli presented during silent stridulation was plotted as a dot against the average wing movement. The gray line represents the average spike frequency. The close temporal relationship of responses near the temporal reference point at 0 sec is attributable to the analysis procedure. Gray bars show that the timing of the maximum response reduction during silent singing coincides with the opening wing movement, which is the time AN1 would respond to self-generated sound. For additional details see Figure 2.
In contrast to the response of AN1, AN2 was inhibited and rarely spiked during sonorous chirps (Fig. 2B) (n = 5 crickets). At the start of the chirp an IPSP occurred at the transition between wing opening and closing (Fig. 2Bi, solid vertical line). This was generated in response to the quiet sound produced during wing opening (Fig. 2Bi, arrow 3). Thereafter, IPSPs occurred in phase with the opening movement (Fig. 2Bi, dashed line), which followed the loud sounds produced during wing closing (Fig. 2Bi, arrow 4). Between each IPSP the membrane potential of AN2 repolarized (Fig. 2Bi, asterisk); however, the repolarization was so rapid that it seems likely that this was in part attributable to an excitatory input during singing. High-intensity 4.5 kHz signals or high-frequency harmonics of the calling song could have excited AN2. The quantitative evaluation of the response of AN2 during sonorous stridulation confirmed that few spikes were generated during sonorous chirps (Fig. 2Bii). The responses of AN1 and AN2 during stridulation were similar to their responses to 4.5 kHz acoustic stimuli at rest (Fig. 1). Therefore, we suspected that these neurons were responding to reafferent sound. To test this, we recorded their responses during "silent" stridulation in crickets with one wing removed.Responses of AN1 and AN2 during silent stridulation
The spikes in AN1 and high-amplitude IPSPs in AN2 recorded during sonorous stridulation were absent during silent stridulation. Therefore, these responses were a reaction to self-generated sounds. We recorded small hyperpolarizing potentials during silent chirps in nine recordings of AN1 (Fig. 3Ai) and nine recordings of AN2 (Fig. 3Bi). The hyperpolarizations began just after the start of wing closing (Fig. 3Aii,Bii, dashed lines) and reached a maximum during the consecutive wing opening (Fig. 3Aii,Bii, solid vertical lines). On average, the maximum amplitude of these potentials were -1.57 ± -0.22 mV (n = 6 crickets) in AN1 and -0.71 ± -0.13 mV in AN2 (n = 6 crickets). If the ears of silently stridulating crickets were removed, the hyperpolarization was still present but had a lower amplitude both in AN1 (-0.39 mV, n = 1) and AN2 (-0.40 ± 0.05 mV, n = 4). This is probably attributable to the removal of any spontaneously firing auditory afferents that would normally depolarize AN1 and AN2. With this depolarizing input removed, the membrane potential would return to its, slightly more negative, resting value and the hyperpolarization would appear to be smaller.
In 30% of experiments, EPSPs that sometimes generated spikes were recorded in AN1 (n = 3) and AN2 (n = 5) during silent stridulation (Fig. 4Ai,Bi). On average, the EPSPs reached 5.48 ± 2.18 mV (n = 3) in AN1 and 1.76 ± 0.42 mV (n = 5) in AN2. The phase of the EPSP varied from animal to animal, but generally they started in phase with wing closing and reached a maximum during the consecutive wing opening (Fig. 4Aii,Bii). EPSPs were normally recorded during chirps with high-amplitude wing movement. They could also be elicited by manually moving the right wing of intact AN1 (n = 2) and AN2 (n = 4), and deafened AN1 (n = 1) and AN2 (n = 2) (Fig. 5), crickets. It is not known which sense organ mediates this excitation.
Therefore, the responses of AN1 and AN2 during sonorous stridulation are the result of a mix of inputs from reafferent sound and wing movement and a low-amplitude hyperpolarization. To determine whether the hyperpolarization was centrally generated or the result of nonauditory sensory feedback, we recorded the responses of AN1 and AN2 in crickets with their thoracic or thoracic and abdominal ganglia isolated. Even under these circumstances, the isolated CNS generated the motor output for stridulation. Because this type of stridulation did not involve any movement or sensory feedback it was termed fictive stridulation.
Responses of AN1 and AN2 during fictive stridulation
AN1 and AN2 rarely spiked during fictive stridulation (Fig. 6Ai,Bi). Low-amplitude hyperpolarizing potentials were recorded in phase with the fictive chirps in four of five recordings of AN1 and in four of five recordings of AN2 (Fig. 6Aii,Bii). They increased in size during the chirp and reached an average maximum amplitude of -2.2 ± 0.73 mV (n = 4 crickets) in AN1 and -0.65 ± 0.05 mV (n = 4 crickets) in AN2. Because of the delay between motor nerve activity and wing movement, the hyperpolarizations occurred slightly later during fictive chirps than during silent chirps. In one of five crickets, in both AN1 and AN2, the membrane potential remained unchanged during fictive chirps. Depolarizing potentials were never recorded during fictive chirps in either neuron. With the cricket's ears removed, hyperpolarizing potentials were recorded during fictive chirps in one recording of AN1 (-0.28 mV) and in one recording of AN2 (-1.0 mV). Therefore, based on this limited result it appears that the hyperpolarizations were the result of a centrally generated corollary discharge.
Responses of AN1 and AN2 to acoustic stimulation during stridulation
The corollary discharge mediates presynaptic inhibition of auditory afferent terminals (Poulet and Hedwig, 2002AN1 and AN2 spiked consistently to the acoustic stimuli when the cricket was at rest and during chirp intervals but their auditory responses were inhibited during silent chirps (Figs. 7Ai,Bi). The inhibition began at the start of wing closing (Fig. 7Aii,Bii, dashed lines) and lasted throughout the chirp. Inhibition was present even in the cases in which EPSPs were generated during the silent chirps. EPSPs, which occasionally generated spikes, were recorded at the transition between wing opening and closing (Fig. 7Ai,Bi, asterisks). Wing movement and/or the increased afferent input during those phases of the chirp in which the amplitude of the inhibitory inputs to the afferents and interneurons was decreased may have mediated the EPSPs.
During fictive chirps, both neurons showed similar effects to those recorded during silent stridulation (Fig. 8A,B). However, the amplitude of the EPSPs compared with those recorded during silent chirps was reduced. Therefore, the inhibition mediated by the corollary discharge (hyperpolarizations in AN1 and AN2 and presynaptic inhibition of auditory afferents) suppresses the responses of AN1 and AN2 to sound during the chirps.
The impact of the inhibition on the processing of sound patterns similar to cricket song
We then examined the strength of the corollary discharge inhibition on auditory processing in silently stridulating crickets presented with more natural stimuli. When recording from AN1 (Fig. 9A), we presented the cricket with acoustic stimuli that mimicked cricket song (4.5 kHz, 100 dB SPL, 21 msec duration, 21 msec period); when recording from AN2 (Fig. 9B) we used 12.5 kHz sound pulses (21 msec duration, 250 msec period). Because AN2 was normally inhibited by 4.5 kHz stimuli, we did not examine its response at this frequency. At rest and during the chirp intervals, AN1 responded with a burst of
The responses of AN1 to 100 dB SPL sound pulses varied depending on the phase of stimulation. For example, compare the responses to each of the four stimuli presented during the silent chirp in Figure 9A. To examine this difference in more detail, we plotted the maximum spike frequency of the response to each acoustic stimulus presented during silent stridulation against wing movement and then calculated the average response of AN1 (Fig. 10, gray line). During the chirp interval AN1 responded with bursts of spikes (in this example at
Response of AN1 to sound patterns mimicking cricket song
We have shown previously that the stimulation of ON1 in the male cricket, induces a burst of spikes followed by a long-lasting hyperpolarization (Poulet and Hedwig, 2002
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Figure 11. A, A long-lasting hyperpolarization that followed spiking of AN1 in response to a train of 4.5 kHz, 75 dB SPL stimuli. The dashed line indicates the resting membrane potential before acoustic stimulation. B, AN1 responded vigorously to a series of 4.5 kHz, 80 dB SPL stimuli. C, The response of AN1 to the 80 dB SPL stimuli was slightly reduced if they were preceded by 100 dB SPL chirps. For additional details see Figure 2.
Discussion
We have demonstrated previously that the cricket's tympanic nerve and tympanic membrane respond fully to self-generated sounds (Poulet and Hedwig, 2001Frequency tuning of AN1 and AN2
AN1 and AN2 are two identified ascending auditory interneurons that project from the prothoracic ganglion to the brain. AN2 is inhibited or weakly excited by 4.5 kHz and responds best to 12.5 kHz (Wohlers and Huber, 1978Inputs to AN1 and AN2 during stridulation
AN1 spiked whereas AN2 received high-amplitude IPSPs during sonorous chirps (Fig. 2). During silent stridulation, only low-amplitude hyperpolarization or depolarizations were recorded in AN1 and AN2 (Figs. 3, 4). Stimuli at the carrier frequency of cricket calling song (4.5 kHz) elicit very similar responses in AN1 and AN2. Therefore, the reactions during sonorous chirps can be explained as a response to self-generated sound.Two other inputs to AN1 and AN2 were identified during silent stridulation. In 70% of experiments low-amplitude hyperpolarizing potentials were observed in AN1 and AN2 during silent (Fig. 3) and fictive (Fig. 6) chirps. Their timing was very similar to the IPSPs recorded in ON1 (Poulet and Hedwig, 2002
In 30% of recordings of AN1 and AN2, depolarizing potentials were recorded during silent chirps that occasionally elicited spikes (Fig. 4). Three observations led us to conclude that they were generated by reafferent feedback via an unidentified sensory pathway activated by wing movement: (1) chirps that caused depolarizations generally were produced by high-amplitude wing movements; (2) depolarizing potentials were never recorded during fictive stridulation with all sensory feedback removed; and (3) depolarizing potentials were elicited by manual wing movement in deafened crickets (Fig. 4). Auditory interneurons in the cricket, e.g., ON1 (Wiese, 1981
Responses to external sound during stridulation
AN1 and AN2 responded to acoustic stimulation during chirp intervals, but their responses were inhibited during silent and fictive chirps (Figs. 7, 8). This was attributable to presynaptic inhibition of the auditory afferent terminals and the low-amplitude hyperpolarizations in AN1 and AN2. The strength of the combined inhibition was tested by playing test stimuli at the best frequency of the neuron to silently stridulating crickets. AN2 responded vigorously during the chirp interval (Fig. 9), but its response was reduced by 65% during the chirps. The response of AN1 to stimuli that mimicked cricket song (4.5 kHz, 100 dB) was reduced by 71% during silent chirps (Fig. 9). The percent reduction in response to external stimuli was very similar in AN1 (71%) and AN2 (65%) to that recorded in ON1 (67%) (Poulet and Hedwig, 2002The presynaptic afferent depolarizations (PADs) in the afferents (Poulet and Hedwig, 2002
Biological significance of the corollary discharge
In this study, we recorded a long-lasting hyperpolarization in AN1 that followed a spiking response to a series of 4.5 kHz stimuli (Fig. 11). A very similar effect has also been recorded in ON1 (Pollack, 1988Spiking in AN2 during flight elicits escape behavior in Teleogryllus (Nolen and Hoy, 1983
Future experiments
Studies made on vocalizing vertebrates have also indicated a reduction in neural activity during sound production (Suga and Schlegel, 1972
Footnotes
Received Dec. 6, 2002; revised Feb. 3, 2003; accepted Feb. 21, 2003.This work was supported by a Biotechnology and Biological Sciences Research Council studentship and grants from the Royal Society and the Wellcome Trust.
Correspondence should be addressed to Dr. James Poulet, Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK. E-mail: jfap2{at}cam.ac.uk.
Copyright © 2003 Society for Neuroscience 0270-6474/03/234717-09$15.00/0
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