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Brain-stem evoked potentials and noise effects in seagulls
Camp. Biochen~. Phvsiol. Vol. 8lA, No. 4, pp. 837-845, 1985 Printed in Great B&in
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0300-9629/85 $3.00 + 0.00 1985 Pergamon Press Ltd
BRAIN-STEW EVOKED POTENTIALS AND NOISE EFFECTS IN SEAGULLS S.
A.
COUNTER
The Biological Laboratories, Harvard University, Cambridge, MA 02138, USA (Received 22 October 1984) Abstract-l.
Brain-stem auditory evoked potentials (BAEP) recorded from the seagull were largeamplitude, short-latency, vertex-positive deflections which originate in the eighth nerve and several brain-stem nuclei. 2. BAEP waveforms were similar in latency and configurations to that reported for certain other lower vertebrates and some mammals. 3. BAEP recorded at several pure tone frequencies throughout the seagull’s auditory spectrum showed an area of heightened auditory sensitivity between 1 and 3 kHz. This range was also found to be the primary bandwidth of the vocalization output of young seagulls. 4. Masking by white noise and pure tones had remarkable effects on several parameters of the BAEP. In general, the tone- and click-induced BAEP were either reduced or obliterated by both pure tone and white noise maskers of specific signal to noise ratios and high intensity levels. 5. The masking effects observed in this study may be related to the manner in which seagulls respond to intense environmental noise. One possible conclusion is that intense environmental noise, such as aircraft engine noise, may severely alter the seagull’s localization apparatus and induce sonogenic stress, both of which could cause collisions with low-flying aircraft.
INTRODUCYITON
This study is part of a series of experiments designed to investigate aspects of hearing in the seagulls (Larus argentatus and Larus marinus) with the aim of determining the responsivity to sound at the peripheral and central levels. Preliminary behavioral and morphological observations of the seagull’s auditory system suggest that it is comparatively very well developed and capable of responding selectively to a variety of species-specific sounds (Evans, 1973; Counter and Tsao, 1985). The organization and function of the seagull’s peripheral and central hearing systems are of special interest from a comparative physiological point of view. Also, of particular relevance to this study is the observation that in some areas these organisms live in close and often conflicting proximity to other avian species and to human populations, in the latter case frequently creating a serious safety hazard through collisions with aircraft. Preliminary field studies suggest the hearing of seagulls may be a factor in such collisions. A more thorough knowledge of the neurophysiology of the seagull’s auditory system and its capacities will increase our understanding of some of the bird’s behavior cis-ri-cis other avian species and human ecology. Auditory function was measured by averaged potentials evoked from the eighth nerve and brain-stem by click and tonal stimuli. The effects of masking, noise exposure and stapedius muscle tension on the brain-stem auditory evoked response were also examined in an attempt to understand the special features and limitations of the system. Both extracranial and intracranial recordings of averaged brain-stem auditory evoked potentials have been shown to be an effective method of studying
brain function and specifically the sensory systems of a variety of animals {Bullock, 198 1; Corwin et al., 1982). The evoked waveforms represent the summation of neuronal activity in identifiable central nuclei (Buchwald and Huang, 1975). Computer averaged auditory evoked potentials (BAEP) have been recorded from several avian species in attempts to measure auditory sensitivity and assess the relative contribution of identified nuclei (BiedermanThorson, 1970a,b; Saunders et al., 1973, 1974; Dooling et al., 1975; Dooling and Walsh, 1976). However, these studies have not included species of seagulls, nor have they examined individual components of short latency, click-induced potentials which are thought to reflect eighth nerve and brain-stem nuclei activity. Short latency volume conducted, far-field potentials can be reliably recorded from surface or intra-brain electrodes located several centimeters from the active neuron populations and such recordings involve minimum trauma to the animal. Spectral analyses of seagull vocalizations were also made in order to compare the frequency components of the vocal output with the area(s) of heightened sensitivity in its hearing range. METHODS
AND MATERIALS
Thirty-seven seagulls (Laws argentatus and Larus tnarinus) ranging from hatchlings to adults (> 4 months) were used in this investigation (25 animals were used in the BAEP component and 12 in the combined BAEP-noise, vocalization, audiogenic startle and morphology studies). The fertile eggs and gulls were collected on permit from Mononomy Island, Massachusetts through the US Fish and Wild Life service and Boston’s Logan International Airport. The eggs were hatched in the laboratory in standard domestic fowl incubators. Hatchlings and older gulls were housed 837
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according to age and size under proper animal room conditions. The animals were fed a regular diet of sand eels and other fish. For BAEP studies, the animals were anesthetized with Nembutal (60mg/kg body weight) then placed in a restrainer within a high attenuation sound chamber measuring 3 x 3 x 3 feet. BAEP were recorded extracranially (subcutaneously) or intracranially with insulated platinum wires (tips exposed), or stainless steel screws. The active surface electrode was placed in the middle of the skull over the cerebellum. In some preparations the stainless steel crew electrode was positioned in a hole, previously placed in the braincase and in contact with the cerebrospinal fluid. In others, either the screw or the platinum wire electrode was positioned in the brain-stem proper. The reference electrode was placed in contact with the posterior tongue or palate of the mouth and the needle ground electrode was placed in the foot. The responses were amplified, filtered (150 to 3 kHz) and led directly to the averaging computer (Nicolet 1 171). Sweeps of 256-1024 were used in each trial, the number of sweeps being determined by the identifiability of component waves of the BAEP. At suprathreshold levels 512 sweeps were generally sufficient for identification of all components of the BAEP. The resultant BAEP was stored in memory. displayed on the CRT or printed for measurement in hard copy by a Hewlett Packard Model 7010B XY plotter. Acoustic stimuli were generated by a click generator and an audio oscillator (NIC 102). The click was a 100 Hz-10 K wide band signal of 100 psec in duration, presented at a rate of 10.7isec. The pure tones had a 15 msec plateau with rise decay ramps of 5 msec. The stimuli were amplified by a conventional audio amplifier and delivered by a standard 15 inch, 40 W loudspeaker (for sound field measurements) located 40 cm from the head, or delivered directly to the ear by a connecting (12cm rubber) tube attached to a 4cm plastic funnel over a TDH 39 earphone. All sound levels were measured and calibrated on a general radio 1933 sound
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level meter (SPL). All decibal values for click and tonal stimuli were expressed in hearing level (HL-ANSI 1969). The white noise masking signal was produced by a Nicolet Model 102 noise generator. Pure tone masking was produced by a Hewlett Packard Model 600 audio oscillator and standard amplifier. Impact noise was produced by 0.22 caliber blanks, fired within the sound chamber. Spectral analyses of seagull vocalization patterns were made by placing the animal under a suspended high quality omnidirectional microphone (about IO cm from the animal’s head) all located in an acoustically insulated sound isolation chamber (IAC). Spontaneous vocalizations were recorded on a high quality, high resolution tape recorder. These signals were amplified, low pass filtered (for antialiasing). then sampled, digitized and fed directly into the memory of a PDPII computer. Segments of varying durations were then selected for analyses using discrete Fourier transform techniques. All signal recording, processing and displays were effected using the MITSYN interactive dialogue language for time signal processing (a computer based language system). RESULTS
Brain -stem evoked responses (1) Wave form and amplitude. Short latency, clickinduced BAEP responses consisting of 3-5 vertexpositive waveform deflections were reliably recorded in the first 10msec. Typically the first two positive deflections in the waveform occurred at around 1.3 and 2.3 msec respectively (depending on the stimulus level) and were of high amplitude, followed by a low amplitude, slow wave at about 4msec. These waves are herein labeled P,, P, and P, (Fig. 1). Occasionally, on the- position if vertex (positive) and depending
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Fig. I. Amplitude and waveform analyses of brain-stem auditory evoked potentials (BAEP) from the seagull. Left: Graph of the amplitudes of the first two positive deflections, P, and PZ as a function of sound intensity level. Both intracranial (IC) and surface (S) electrode measurements are represented. Right: Waveforms of surface recorded seagull BAEP in response to clicks of varying intensity levels. The single trace of the first record shows the absence of large wave activity after 6msec. The next five records (6C-20dB) show two superimposed trials of 512 sweeps at each intensity level. The waveform traces begin at the approximate time the stimuli reach the ear.
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Noise effects in seagulls 6
more than twice that of the S electrode recording at the higher intensity levels. The differences in the amplitude between the IC and S electrode recordings of Pz were less in magnitude than the differences observed for P,. The waveforms shown in Fig. 1 serve as illustrations of the amplitude, latency and configuration of the typical short latency BAEP recorded from surface electrodes. The traces shown in this figure begin at the approximate time the stimuli reach the ear. The longer duration BAEP recording shown in the top waveform (60 dB) of Fig. 1 demonstrates that large amplitude positive waves are generally not recorded after 5 msec or between 5 and 15 msec. In some older birds, however, additional large fast and slow positive waves were recorded at around 7 and 9msec. The waveforms of Fig. 1 also in amplitude, show the progressive changes configuration and latency during an intensity series. In some instances recognizable P, responses were recorded as low as 15 dB (HL). (2) Latency. The latencies of P,, P, and P, for 10 animals as a function of intensity are shown in Fig. 2. This figure shows that the average latencies of P,, P, and P, decrease systematically with increases in stimulus intensity. Because the latency differences between IC and S electrode recordings were insignificant, the IC and S latency values were combined in these curves. P,, which may originate from the auditory nerve and the first brain-stem nuclei, showed the best fit to a regression line. P, appears from about 2.1-3.1 msec after the stimulus onset and usually has a sharp peak. (3) BAEP as a function of stimulus frequency. Figure 3 shows mean BAEP amplitude in response to pure tones presented at a constant stimulus intensity at various frequencies throughout the seagull’s auditory spectrum. The method used here, the inverse of the standard threshold technique, offers a straight forward and efficient means of estimating regions of
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Fig. 2. Latency of the first three positive waveform deflections, P,, P, and P,, of the seagull BAEP measured as a function of sound intensity level. electrode, the waves were more uniform in amplitude. The electrode arrangement which gave the most consistent BAEP waveform was vertex referenced to the posterior palate. Only gross repositioning of the vertex or reference electrode could change the configuration of the BAEP. Figure 1 illustrates the relationship between the amplitude of the BAEP and stimulus intensity. This figure shows the average amplitude (measured peak to trough) of waves P, and P, recorded both intracranially (IC) and from surface (S) electrodes. The amplitude of the BAEP for both IC and S measurements increases systematically with signal intensity up to about 80dB. At higher signal levels the slope of the function shows no further increase, or declines slightly. In some S recordings a third fast wave (Pl) followed by a fourth (slow) wave (PJ or in some IC recordings a fourth fast wave followed by a fifth, slow wave (P,) was observed. The amplitude of P, recorded intracranially (when the electrode was positioned in the brain-stem near the eighth nerve) was SEAGULL:
Auditory frequency response and vocalization spectrum
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Fig. 3. Amplitude of seagull BAEP and vocalization output as a function sound frequency. The vocal output was derived by Fourier analysis.
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heightened sensitivity in the auditory spectrum. This figure shows that the average amplitude of the BAEP to discrete pure tones is greatest in the region of 1.5-3 kHz, with the highest mean amplitude around 2.5 kHz. Above 2.5 kHz the response amplitude (and possibly the ear’s sensitivity) drops off rapidly. The BAEP amplitude-frequency curve of the ear is similar to the spectral content of spontaneous distress vocalizations made by young l&30-day-old seagulls as determined by Fourier transform analysis and shown in the top curve of Fig. 3. (Older and adult seagulls do not readily vocalize in captivity.) The first large peak in the vocal output curve represents a narrow band of frequencies around the fundamental frequency. (4) BAEP during stapedius muscle tension. Vocalization of young and adult seagulls may reach levels in excess of 85 dB (SPL). This creates considerable self-stimulation during vocalization, with the sound level at the head reaching possible acoustic trauma levels. Also, as shown in Fig. 3, the predominant acoustic energy in the seagull’s vocalization spectrum occurs in a frequency range of heightened responsivity for the seagull ear. Counter and Borg (1979) have shown that birds involuntarily activate the single, bilateral middle ear muscle, the M. stapedius, during vocalization to attenuate acoustic self-stimulation. The seagull possesses a welldeveloped stapedius muscle which attaches both the tympanic membrane and columella. When slight mechanical tension (a degree sufficient to induce observable tightening of the tympanic membrane) was induced in stapedius muscle the amplitude of the BAEP was reduced substantially from pre-tension control levels. The mechanical tension simulated the natural stapedius muscle contractions during vocal-
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ization. The average reduction in the click-induced P, amplitude for four animals was 56% (range 30-74”<). The dashed curve and arrow of Fig. 4C (MST) show the average reduction in amplitude of P, during stapedius muscle tension (relative to control, pretension levels). (5) High intensity noise exposure. The effects of high intensity noise on the auditory sensitivity of the seagull was examined by BAEP in eight animals. The averaged BAEP (P,) recorded immediately after exposure to a 120 dB (SPL) impact noise (IN) is shown in Fig. 4A. In this experiment, the BAEP was measured at three intensity levels (60, 70 and 80dB) immediately following the impact noise. Amplitudes were normalized to the pre-treatment control measurements. The temporary threshold shift caused by the IN is reflected in the resultant 500; (average) reduction in the amplitude of P, of the BAEP observed in the first few minutes following exposure to the 120dB impact sound. Also, the click-induced BAEP response immediately following exposure to 12 hr of a 110 dB (SPL), 2 kHz sound field pure tone is shown in this same figure. In these animals the prolonged noise exposure (PE) caused a substantial reduction in the BAEP amplitude relative to the control response (approximately 35%). Both the IN and the PE effects were generally reversible and hearing appeared to return to normal or near normal levels in a few hours to a few days. In some cases, however, the BAEP was permanently reduced following both IN and PE treatments, suggesting permanent threshold shift or irreversible hearing loss. (6) Masking. Masking is herein defined as the reduction in size or elimination of the click- or tone-induced BAEP as a result of the continuous
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Fig. 4. (A) Percentage reduction in the amplitude of a 60 dB click evoked P, following prolonged exposure (PE) to intense pure tones, impact noise (IN) of 1 lo-120 dB, and during white noise masking (WNM) with signal-to-noise ratios of 0, 10 and 20dB. (B) Percentage reduction in the amplitude of a pure tone-evoked P, in the presence of a white noise masker (WNM) with a signal to noise ratio of - IOdB (---) and the percentage reduction in the amplitude of a click-evoked P, in the presence of various pure tone maskers (PTM) with a signal to noise ratio of - 30 (-). (C) Percentage reduction in the amplitude of P, during mechanically induced stapedius muscle tension (MST) and percentage reduction in the amplitude of a click induced Pz in the presence of the pure tone maskers of B.
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Fig. 5. (A) Seagull BAEP waveforms from a single experiment showing the effect of sound field [SS dB (SK)) pure tone maskers of various frequencies on 50 dB click-evoked BAEP responses. (3) Single click evoked (55 dB) BAEP recorded in quiet (-) and in the presence of an 85 dB 2.5 kHz sound field masker (---f. (C) Single click evoked (70 dB) BAEP recorded in quiet f----) and in the presence of a 70 dB white noise masker. All waveform traces begin at the approximate time the stimuli reach the ear.
of an interfering sound masker. In these experiments the term signal to noise ratio (S/N) refers to the decibel value of the wide band click (LOOHz to IO kHz) stimulus or the pure tone (I-3.5 kHz) stimulus in the presence of a simultaneous wide band (10 Hz-10 kHz) masking noise or pure tone maskers. The effects of masking frequency, intensity, duration and spectrum were investigated. The effects of a presentation
wideband, white noise masker (WNM) on a 60 dB cfick-evoked P, (delivered via a tube in the ipsilateral ear canal), are shown in Fig. 4A. The amplitude of the P, responses were reduced by about 70% when the signal to noise ratio was OdB and further reduced to 90% of the control amplitude when the signal to noise ratio was - 20 dB (stimulus = 60 dB, masker = 80 dB). Figure 4B shows the BAEP responses to pure
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tone and click stimuli in the presence of both white noise and pure tone maskers. The white noise masker (WNM) was presented to the ear through a sound field speaker at an S/N ratio of - 10 dB. The pure tone maskers (PTM) were delivered by sound field speakers. The P, responses to pure tone stimuli were masked by white noise (dashed curve), and the P, responses to clicks were masked by sound field pure tones (solid curve). Figure 4B shows that the greatest masking effects for both maskers occur between 1.5 and 3 kHz, with peak effect at around 2.5 kHz. The white noise masker reduced the amplitude of the pure tone-induced P, by approximately 6Oyd in the region of 1.5-3 kHz. The pure tone maskers had a maximum intensity level of 80 dB (f 5 dB). The average values plotted from the PTM in Fig. 4B were derived from data sampled at a - 30 dB S/N ratio. These pure tone masking sounds caused an average reduction in the click-evoked P, amplitude of around 807,. The most effective pure tone maskers were those from 1.5 3 kHz. The masking effect of pure tones on either side of this narrow band was significantly lower. The results of both the white noise and pure tone masking studies are consistent with the finding of higher amplitude BAEP and possible heightened auditory sensitivity in the frequency range of about I-3 kHz. The click-induced P2 was equally reduced or completely eliminated by the same pure tone maskers (Fig. 4C). Figure 5A shows the results of one experiment in which a 50 dB click stimulus is masked by pure tones of 80dB (k5 dB) from sound field speakers. This figure shows a systematic reduction in the amplitudes of waves P, and PZ in the masker frequency range of l-3.5 kHz. Also, a significant shift in the latencies of P, and PZ occurs in the effectively masked situation. This pattern is more vividly illustrated in the single intracranial BAEP recording of Fig. 5B. Here it can be seen that the amplitudes of P,, PZ and P, are dramatically reduced in the presence of a pure tone masker of sufficient intensity. This figure also shows four fast, vertex-positive deflections and one slow, late deflection in the control waveform. Further, the latency of P, in the masked response is delayed by about 1 msec. White noise masking has similar amplitude and latency effects on the click-induced BAEP (Fig. X), depending on the noise level and signal to noise ratio. Generul physiological responses to sounds Sonogenic convulsions have been reported in a variety of vertebrates, including birds (Ginsburg, 1954: Lehman and Busnel, 1963). Sonogenic convulsions are characterized by sound-induced startle/ jumps, followed serially by running fits, modified cardiac and respiratory rhythm, physical collapse and violent clonic-tonic seizures of the entire body, after which there is a slow dazed recovery or death from anoxia. This audiogenic seizure activity is believed to be a CNS-mediated response to auditory sensory overload in susceptible animals (Lehman and Busnel, 1963). Behavioral observations were made on seagulls (ranging in age from 2 days old to adults) which were exposed to high intensity noise (85-120 dB) of varying duration. The shortest duration noise, impact noise (from 0.22 caliber blanks), induced instanta-
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Fig. 6. Increase in heart rate as a function of time (set) after the impact noise stimulus (1 l&120 dB (SPL)). (A) Curve derived from five animais collected at Boston’s Logan International Airport. (B) Curve measured in seven animals collected from the Mononomy island Wildlife Refuge
neous sonogenic startle in each animal, but no sign of audiogenic convulsions or seizures. Behaviorally, startle was manifested by head jerks and other rapid body movements with each impact noise. Prolonged exposure to pure tones and white noise of 8551 IO dB evoked similar startle responses at the stimulus onset only. Occasional head shakes and avoidance behavior (moving away from the speaker) were observed during high intensity noise exposure periods ranging from several minutes to hours or days. While the classical pattern of audiogenic seizures was not observed in these experiments audiogenic stress responses were recorded consistently. The most quantifiable measure of audiogenic stress was the modification in cardiac rhythm caused by intense noise exposure. Figure 6 shows the average increase in heart rate (for 12 animals}, during periods of audiogenic stress induced by high intensity impact noise (11%120dB). The two curves of this figure represents two distinct populations of seagulls. The steeply rising curve (A) which peaks at a 50:: increase in heart rate in 1 set after the impact noise stimulus and rapidly returns to baseline rate in 8 sec. was obtained from the seagulls collected at Boston’s Logan International Airport. The more gradually rising curve (B) which peaks at about a 20’: increase in heart rate and remains elevated for 16 set post srimulus was obtained from seagulls collected at the Mononomy Island Wildlife Refuge, some 100 miles away from the first population. The animals used in curve (A) were invariably adults which lived in and around the airport. The second population consisted mainly of younger (but not necessarily smaller) birds, either hatchlings or older animals with no known previous exposure to intense unnatural noise. DISCUSSION
BAEP wawform, a~plitu~ie, urtd latency The waveforms of the click-induced BAEP recorded from seagulls, using both surface and intracranial electrodes, are similar to the short latency brain-stem recordings from doves (Bullock, 198 I).
Noise effects in seagulls but remarkably different from those recorded in other Aves (Saunders et al., 1974; Dooling et al., 1975). The waveforms recorded in the present study consist mainly of 34 characteristically fast, vertex-positive deflections in the first 5msec, followed by a large, slow deflection. Each waveform was repeatable and remained consistent in both amplitude and latency over time. Surface changes in electrode position had only a slight effect on either parameter of the BAEP. However, the vertex (positive) to posterior palate electrode arrangement yielded the most consistent and reliable BAEP. The first and largest deflection (P,) probably corresponds to summed eighth nerve and brain-stem nuclei activity. The later deflections (P2, P, and P4) most likely represent summed, volume conducted potentials from several higher brain-stem auditory structures. When the metal electrode was positioned in the brain-stem proper (and closer to the eighth nerve), the amplitude of P, increased more than two-fold. The amplitudes of P, and P, of the intracranial response were also significantly larger than the surface electrode response. This growth in amplitude as the electrode traverses the brain-stem would seem to support the notion that component P, (and possibly Pz) is locally generated from lower level auditory structures, whereas P, is likely to be a volume conducted response from several brain-stem auditory nuclei. It should be added that the filter settings on the amplifier could possibly have eliminated additional slow components in the first 20 msec. The latency of P, (range = l&1.8 msec) is similar to that recorded from the eighth nerve of cats (Buchwald and Huang, 1975; Achor and Starr, 1980; Jewett, 1970) and humans (Jewett and Williston, 1971; Moore, 1971). The latencies of P, and P, in this study decreased systematically with increases in the stimulus intensity, while the latency of P, showed only minor changes. The latency differences between the IC and S electrode recordings (P,, P,, and PI) were unremarkable. Studies by Biederman-Thorsen (1970a,b) have suggested that the avian and mammalian central auditory systems are notably similar. However, the comparatively fewer positive waves observed in the first 20msec of the BAEP would appear to support Schwartzkopff s (1967) hypothesis that birds have fewer relay stations (synapses) between the ear and telencephalon than mammals. Response to stimulus frequency
It is possible that a behavioral audiogram could be obtained in seagulls as in other avian species through a lengthy conditioning process. However, BAEP responses to pure tones can also be used to assess hearing sensitivity and involves less time and variability. Brain-stem evoked potentials cannot provide absolute measures of auditory thresholds because they are summed potentials which are dependent on factors such as the size of neuronal populations and the spatial relationship between the recording electrode and those cell populations. Nevertheless, regions of high sensitivity can be reliably predicted by changes in the amplitude of the BAEP at various frequencies within the auditory spectrum. Using the amplitude of P, as the index of sensitivity, the results
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of this study showed the range of 1-3 kHz to be a region of heightened auditory responsivity in seagulls. This finding is similar to that observed in other avian species (viz. domestic fowl and pigeon) by several investigators (Gates et al., 1975; Tanaka and Smith, 1978; Counter and Borg, 1979). Discrete Fourier transforms performed on selected segments of distress and other types of vocalizations from young (l O-30-day-old) seagulls (particularly herring gulls) showed that most of the vocal energy falls in the frequency range of 1.5-3 kHz, with a peak output level at around 2.5 kHz. These findings lend further support to the observations of heightened auditory sensitivity around 2.5 kHz. It is also interesting to note that the seagull’s hearing is particularly acute in the same broad frequency range that humans hear best, a finding which may have implications for seagull control procedures. Masking Of particular interest in this study was the effects of certain bandwidths and types of noise on seagull hearing. This aspect of the study was especially relevant to the question of the effect of certain components of jet and propeller driven aircraft engine noise on the ears of exposed seagulls. Seagulls around coastal airports account for a high percentage of the bird/aircraft collisions worldwide. No generally accepted scientific explanation has been advanced to explain these collisions. It is possible that the noise from jet and other aircraft engines may have profound effects on the behavior and physiology of seagulls in the immediate vicinity. However, additional studies are necessary in order to elucidate the precise nature of the effects of aircraft noise on the ears of seagulls and other birds. In any event, it seems particularly significant that the findings of the present study show that one region of heightened sensitivity in seagull hearing corresponds to the bandwidth of maximum output in many jet aircraft, i.e. around l-3 kHz. The amplitudes of P, and P, were systematically reduced by wideband noise and pure tone masking stimuli with signal to noise ratios ranging from 0 to 30dB. Pure tone masking stimuli of l-3.5 kHz were used because these discrete frequencies cover a region of heightened sensitivity in the seagulls’ auditory spectrum and correspond to the major frequency components of jet aircraft engine noise. The most effective pure tone maskers were those in the 1.5-2.5 kHz range. A 2.5 kHz masker was found to be particularly effective (Fig. 5A). Also, masking of the pure tone-induced BAEP by wide band noise was most effective when the pure tone stimulus was in l-3 kHz range, at all signal to noise ratios. These findings also add additional support to the conclusion regarding heightened auditory responsivity in seagulls around 2.5 kHz. In field studies at Boston’s Logan International Airport it was found that many seagulls are exposed to intense jet noise for several hours during the day. This is particularly evident in the earlier morning hours when hundreds of herring, blackback and other seagulls congregate to roost on several “favorite” runways. Some of these animals are exposed to take-offs and landings of jets and propeller aircraft
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every 90 or so set, at least 10 hr a day for many days. Sound level measurements of jet noise show it to be in excess of 85 dB SPL (close to IOOdB) within 1500 feet of the aircraft. Most of the intense noise energy of the older model jet aircraft (which tend to be noisier than some newer models) is concentrated in the region of 1-3 kHz, while that of the newer models is in the area of l-2 kHz. The equally intense “rumble” sound made by old and new aircraft as they pass a stationary receiver and travel a short distance from the receiver, is similar to wideband white noise. It is reasonable to assume that these intense jet noises would have detrimental effects on the hearing of seagulls. In the first instance, the acoustic masking effects of jet aircraft in the near-field are likely to create sonic interference for all other auditory signals or cues available to the organisms and may possibly cause a breakdown in binaural reception and localization, leading eventually to disorientation. Counter and Borg (1979) have shown that sound travels through a complex interaural passageway in the avian cranium in such a way as to enable the animal to localize a sound source. Any noise interference with this delicately balanced system may render it ineffective, and make the animal unable to locate the source of even threatening sounds in the near and far fields. Such effects could possibly lead to runway and mid-air collisions between birds and aircraft. Secondly, the intense and rapidly rising noise levels may cause audiogenic stress in some seagulls. Cardiac responses to the early seconds of intense, long duration noise and impact noise caused dramatic increases in heart rate (and in some instances volume), reflecting a sonogenic stress reaction. While no seizure activity was noted, these sonogenic startle or stress reactions, when induced by aircraft noises, could possibly lead to disorientation and collisions. In order to clear the runway of seagulls, some airports engage Field Maintenance “Bird Control Teams” that patrol the runways and perimeter of the airport in vehicles, and fire warning shots from 12 gauge shotguns at individual seagulls or flocks of seagulls (and other birds) near the runways. The impact noise component of this study was similar, both quantitatively and qualitatively, to that produced by the Field Maintenance impact noise equipment. The purpose of this component of the study was to examine the primary and secondary auditory physiology changes in seagulls resulting from the impact noise. The results show several remarkable effects. First, at close range the impact noise causes an immediate auditory threshold shift (or reduction in auditory sensitivity as reflected by a decrease in BAEP amplitude). The development and extent of permanent threshold shift has not been fully determined at this time. Secondly, sonogenic startle and stress were observed. It is significant to note, however, that seagulls collected around the airport (which tended to be older) exhibit a very dramatic increase in heart rate immediately following the noise onset. In these birds, the heart rate returned to normal, pre-stimulus levels within a few seconds after the startle-inducing stimulus. This response suggests a form of adaptation to the impact noise stimulus. On the other hand, birds collected from an isolated area some 100 miles away from the airport and with no
previous (known) exposure to intense unnatural or impact noise exhibited significantly less sonogenic startle or stress immediately following the stimulus onset. Rather, the latter group showed only a small (20x), slow rise in heart rate, but this remained elevated for twice as long as that of the airport birds. These findings suggest that the airport seagulls which may have routinely experienced the explosive warning shot noise are effectively startled by the sound, but disregard the threat after a few seconds. Conversely, the inexperienced birds are only mildly startled by the curious noise, but for a longer period, possibly because it is a totally unfamiliar and meaningless stimulus. It is difficult to test the validity of Schwartzkopff’s hypothesis that central analysis of acoustic information is more important than peripheral analysis in Aves (Schwartzkopff, 1960a,b, 1967, 1968). However, the masking experiments of this study may shed some light on the relative contributions of both levels. At moderately high intensity levels, pure tone maskers which have a more specific place effect along the basilar papilla caused a general reduction in the amplitude of P,, P, and P,, but did not cause a major alteration in the shape or configuration of the waveforms. This kind of response might suggest that the masking effect was more peripheral than central. On the other hand, white noise maskers (which activate most regions of the cochlea) and very high intensity pure tone maskers effectively obliterated the BAEP and/or altered its configuration beyond recognition. These responses suggest both central and peripheral effects. High intensity white noise and pure tones would be expected to cause massive displacement of the entire basilar membrane and desynchronize the firing of eighth nerve fibers. Brain-stem nuclei would therefore receive less synchronized threshold level summated activity, as reflected by the substantially reduced BAEP recordings. Further interaural masking studies are necessary to fully evaluate the central and peripheral effects of masking. Acknowledgements-The author wishes to thank Priscilla Tsao for laboratory assistance, John Dowling and C. James Ciotti for laboratory support, John Lortie and Denver Holt of the U.S.A. Fish and Wild Life Service, the Massachusetts Division of Fisheries and Wild Life, Robert D’Etremont and the Boston Logan International Airport Field Maintenance, George Deegan, Robert Paris, Steven Grasse for animal room assistance, Erik Borg, Ernest Moore and Manny Don for helpful comments and the Harvard Biological Laboratories.
REFERENCES Achor L. and Starr A. (1980) Auditory brain-stem responses in the cat. I. Intracranial and extracranial recordings. Electroencephal. clin. Neurophysiol. 48, 154173. Adamo N. J. and King R. L. (1967) Evoked responses in the chicken telencephalon to auditory, visual and tactile stimultion. Exp: Neural. 17, 498-564. Biederman-Thorson M. A. (1970a) Auditory evoked responses in the cerebrum (Field L) and the ovoid nucleus of the ring dove. Brain Res. 24, 235-246. Biederman-Thorson M. A. (1970b) Auditory responses of units in the ovoid nucleus and cerebrum (Field L) of the ring dove. Brain Res. 24, 2477256.
Noise effects in seagulls Buchwald .I. S. and Huang C. M. (1975) Far-field acoustic response: Origins on the cat. Science 189, 382-384. Bullock T. H. (198 1) Neuroethology deserves more study of evoked responses. Neuroscience 6, 1203-l 2 15. Corwin J. T., Bullock T. H. and Schweitzer J. (1982) The auditory brain-stem response in five vertebrate classes. Electroencephal clin. Neurophysiol. 54, 629-64 1. Counter S. A. and Borg E. (1979) Physiological activation of the stapedius muscle in Gallus gallus. Acta otol. 88, 13-19. Counter S. A. and Borg E. (1982) The avian stapedius muscle: influence on auditory sensitivity and sound transmission. Acta otol. 94, 267-274. Counter S. A. and Tsao P. (1985) Structure of the seagull inner ear. To be published. Dooling R. J. and Walsh J. K. (1976) Auditory evoked response correlates of hearing in the parakeet (Melopsittacus undulatus). Physiol. Psych. 4, 224232. Dooling R. J., Walsh J. K. and Tepas D. I. (1975) Auditory evoked brain responses from the parakeet: Intensity functions. Physiol. Psych. 3, 307-311. Evans R. M. (1973) Differential responsiveness of young ring-billed gulls and herring gulls to adult vocalizations of their own species. Can. J. Zool. 51, 7599770. Gates G. R., Perry D. R. and Coles R. B. (1975) Cochlear microphonics in the adult domestic fowl (Gallus domesticus). Camp. biochem. Physiol. SlA, 251-252. Ginsburg B. E. (1954) Genetics and the physiology of the nervous system. Genetics and the inheritance of integrated neurological and psychiatric patterns. Proc. Assoc. Res. new. ment. Dis. 33, 39945. Jewett D. L. Volume-conducted potentials in response to auditory stimuli as detected by averaging in the cat. Elecrroencephal. clin. Neurophysiol. 28, 609-618. Jewett D. L. and Williston (1971) Auditory-evoked far fields averaged from the scalp of humans. Brain 94, 681-696. Knudsen E. L. and Konishi M. (1979) Mechanisms of sound
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localization by the barn owl (Tyfo alba). J. cotnp. Physiol. 133, 13-21. Konishi M. (1969) Hearing, single unit analysis and vocalizations in song birds. Science 166, 1178-I 18 I. Konishi M. (1970) Comparative neurophysiological studies of hearing and vocalizations in song birds. Z. Verg. Physiol. 66, 257-272. Lehman A. and Busnel R. G. (1963) A study of audiogenic seizure. In Acoustic Behavior qf Animals (Edited by Busnel R. G.), pp. 244274. Elsevier. Amsterdam. Moore E. J. (1971) Human cochlear microphonics and auditory nerve action potentials from surface electrodes. Unpublished Ph.D. dissertation, University of Wisconsin. Madison, Wisconsin. Saunders J. C., Coles R. B. and Gates G. R. (1973) The development of auditory evoked responses in the cochlea and cochlear nuclei of the chick. Brain Res. 63, 59974. Saunders J. C., Gates G. R. and Coles R. B. (1974) Brain-stem evoked responses as an index of hearing thresholds in one-day-old chicks and ducklings. J. camp. Physiol. Psych. 86, 42643 1. Schwartzkopff J. (1958) Uber der Einfluss der Bewegungsrichtung der Basilarmembran auf die Ausbildung der Cochlea-Potentiale von Strix vasia (Bartur) und Melopsittacus undulatus (Shaw). Z. Vergl. Physiol. 41, 35-38. Schwartzkopff J. (1960a) Physiology der hoheren Sinne bein Saugern und Vogeln. J. Ornifh. 101, 61-91. Schwartzkopff J. and Winter P. (1960b) Zur Anatomie der Vogel-Cochlea unter naturlich bedingungen. Biol. Zbl. 79, 607-625. Schwartzkopff J. (1968) Structure and function of the ear and of the auditory brain area in birds. In: Hearing Mechanisms in Vertebrates (Edited by De Reuck A. V. S. and Knoght J.), p. 41-63. Little, Brown, Boston. Tanaka K. and Smith C. A. (1978) Structure of the chicken’s inner ear: SEM and TEM study. Am. J. Anat. 153, 251-271.
6
0300-9629/85 $3.00 + 0.00 1985 Pergamon Press Ltd
BRAIN-STEW EVOKED POTENTIALS AND NOISE EFFECTS IN SEAGULLS S.
A.
COUNTER
The Biological Laboratories, Harvard University, Cambridge, MA 02138, USA (Received 22 October 1984) Abstract-l.
Brain-stem auditory evoked potentials (BAEP) recorded from the seagull were largeamplitude, short-latency, vertex-positive deflections which originate in the eighth nerve and several brain-stem nuclei. 2. BAEP waveforms were similar in latency and configurations to that reported for certain other lower vertebrates and some mammals. 3. BAEP recorded at several pure tone frequencies throughout the seagull’s auditory spectrum showed an area of heightened auditory sensitivity between 1 and 3 kHz. This range was also found to be the primary bandwidth of the vocalization output of young seagulls. 4. Masking by white noise and pure tones had remarkable effects on several parameters of the BAEP. In general, the tone- and click-induced BAEP were either reduced or obliterated by both pure tone and white noise maskers of specific signal to noise ratios and high intensity levels. 5. The masking effects observed in this study may be related to the manner in which seagulls respond to intense environmental noise. One possible conclusion is that intense environmental noise, such as aircraft engine noise, may severely alter the seagull’s localization apparatus and induce sonogenic stress, both of which could cause collisions with low-flying aircraft.
INTRODUCYITON
This study is part of a series of experiments designed to investigate aspects of hearing in the seagulls (Larus argentatus and Larus marinus) with the aim of determining the responsivity to sound at the peripheral and central levels. Preliminary behavioral and morphological observations of the seagull’s auditory system suggest that it is comparatively very well developed and capable of responding selectively to a variety of species-specific sounds (Evans, 1973; Counter and Tsao, 1985). The organization and function of the seagull’s peripheral and central hearing systems are of special interest from a comparative physiological point of view. Also, of particular relevance to this study is the observation that in some areas these organisms live in close and often conflicting proximity to other avian species and to human populations, in the latter case frequently creating a serious safety hazard through collisions with aircraft. Preliminary field studies suggest the hearing of seagulls may be a factor in such collisions. A more thorough knowledge of the neurophysiology of the seagull’s auditory system and its capacities will increase our understanding of some of the bird’s behavior cis-ri-cis other avian species and human ecology. Auditory function was measured by averaged potentials evoked from the eighth nerve and brain-stem by click and tonal stimuli. The effects of masking, noise exposure and stapedius muscle tension on the brain-stem auditory evoked response were also examined in an attempt to understand the special features and limitations of the system. Both extracranial and intracranial recordings of averaged brain-stem auditory evoked potentials have been shown to be an effective method of studying
brain function and specifically the sensory systems of a variety of animals {Bullock, 198 1; Corwin et al., 1982). The evoked waveforms represent the summation of neuronal activity in identifiable central nuclei (Buchwald and Huang, 1975). Computer averaged auditory evoked potentials (BAEP) have been recorded from several avian species in attempts to measure auditory sensitivity and assess the relative contribution of identified nuclei (BiedermanThorson, 1970a,b; Saunders et al., 1973, 1974; Dooling et al., 1975; Dooling and Walsh, 1976). However, these studies have not included species of seagulls, nor have they examined individual components of short latency, click-induced potentials which are thought to reflect eighth nerve and brain-stem nuclei activity. Short latency volume conducted, far-field potentials can be reliably recorded from surface or intra-brain electrodes located several centimeters from the active neuron populations and such recordings involve minimum trauma to the animal. Spectral analyses of seagull vocalizations were also made in order to compare the frequency components of the vocal output with the area(s) of heightened sensitivity in its hearing range. METHODS
AND MATERIALS
Thirty-seven seagulls (Laws argentatus and Larus tnarinus) ranging from hatchlings to adults (> 4 months) were used in this investigation (25 animals were used in the BAEP component and 12 in the combined BAEP-noise, vocalization, audiogenic startle and morphology studies). The fertile eggs and gulls were collected on permit from Mononomy Island, Massachusetts through the US Fish and Wild Life service and Boston’s Logan International Airport. The eggs were hatched in the laboratory in standard domestic fowl incubators. Hatchlings and older gulls were housed 837
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according to age and size under proper animal room conditions. The animals were fed a regular diet of sand eels and other fish. For BAEP studies, the animals were anesthetized with Nembutal (60mg/kg body weight) then placed in a restrainer within a high attenuation sound chamber measuring 3 x 3 x 3 feet. BAEP were recorded extracranially (subcutaneously) or intracranially with insulated platinum wires (tips exposed), or stainless steel screws. The active surface electrode was placed in the middle of the skull over the cerebellum. In some preparations the stainless steel crew electrode was positioned in a hole, previously placed in the braincase and in contact with the cerebrospinal fluid. In others, either the screw or the platinum wire electrode was positioned in the brain-stem proper. The reference electrode was placed in contact with the posterior tongue or palate of the mouth and the needle ground electrode was placed in the foot. The responses were amplified, filtered (150 to 3 kHz) and led directly to the averaging computer (Nicolet 1 171). Sweeps of 256-1024 were used in each trial, the number of sweeps being determined by the identifiability of component waves of the BAEP. At suprathreshold levels 512 sweeps were generally sufficient for identification of all components of the BAEP. The resultant BAEP was stored in memory. displayed on the CRT or printed for measurement in hard copy by a Hewlett Packard Model 7010B XY plotter. Acoustic stimuli were generated by a click generator and an audio oscillator (NIC 102). The click was a 100 Hz-10 K wide band signal of 100 psec in duration, presented at a rate of 10.7isec. The pure tones had a 15 msec plateau with rise decay ramps of 5 msec. The stimuli were amplified by a conventional audio amplifier and delivered by a standard 15 inch, 40 W loudspeaker (for sound field measurements) located 40 cm from the head, or delivered directly to the ear by a connecting (12cm rubber) tube attached to a 4cm plastic funnel over a TDH 39 earphone. All sound levels were measured and calibrated on a general radio 1933 sound
BAEP:
r;
hmsiem
Auditory
Evoked
Poteni~als
level meter (SPL). All decibal values for click and tonal stimuli were expressed in hearing level (HL-ANSI 1969). The white noise masking signal was produced by a Nicolet Model 102 noise generator. Pure tone masking was produced by a Hewlett Packard Model 600 audio oscillator and standard amplifier. Impact noise was produced by 0.22 caliber blanks, fired within the sound chamber. Spectral analyses of seagull vocalization patterns were made by placing the animal under a suspended high quality omnidirectional microphone (about IO cm from the animal’s head) all located in an acoustically insulated sound isolation chamber (IAC). Spontaneous vocalizations were recorded on a high quality, high resolution tape recorder. These signals were amplified, low pass filtered (for antialiasing). then sampled, digitized and fed directly into the memory of a PDPII computer. Segments of varying durations were then selected for analyses using discrete Fourier transform techniques. All signal recording, processing and displays were effected using the MITSYN interactive dialogue language for time signal processing (a computer based language system). RESULTS
Brain -stem evoked responses (1) Wave form and amplitude. Short latency, clickinduced BAEP responses consisting of 3-5 vertexpositive waveform deflections were reliably recorded in the first 10msec. Typically the first two positive deflections in the waveform occurred at around 1.3 and 2.3 msec respectively (depending on the stimulus level) and were of high amplitude, followed by a low amplitude, slow wave at about 4msec. These waves are herein labeled P,, P, and P, (Fig. 1). Occasionally, on the- position if vertex (positive) and depending
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Fig. I. Amplitude and waveform analyses of brain-stem auditory evoked potentials (BAEP) from the seagull. Left: Graph of the amplitudes of the first two positive deflections, P, and PZ as a function of sound intensity level. Both intracranial (IC) and surface (S) electrode measurements are represented. Right: Waveforms of surface recorded seagull BAEP in response to clicks of varying intensity levels. The single trace of the first record shows the absence of large wave activity after 6msec. The next five records (6C-20dB) show two superimposed trials of 512 sweeps at each intensity level. The waveform traces begin at the approximate time the stimuli reach the ear.
839
Noise effects in seagulls 6
more than twice that of the S electrode recording at the higher intensity levels. The differences in the amplitude between the IC and S electrode recordings of Pz were less in magnitude than the differences observed for P,. The waveforms shown in Fig. 1 serve as illustrations of the amplitude, latency and configuration of the typical short latency BAEP recorded from surface electrodes. The traces shown in this figure begin at the approximate time the stimuli reach the ear. The longer duration BAEP recording shown in the top waveform (60 dB) of Fig. 1 demonstrates that large amplitude positive waves are generally not recorded after 5 msec or between 5 and 15 msec. In some older birds, however, additional large fast and slow positive waves were recorded at around 7 and 9msec. The waveforms of Fig. 1 also in amplitude, show the progressive changes configuration and latency during an intensity series. In some instances recognizable P, responses were recorded as low as 15 dB (HL). (2) Latency. The latencies of P,, P, and P, for 10 animals as a function of intensity are shown in Fig. 2. This figure shows that the average latencies of P,, P, and P, decrease systematically with increases in stimulus intensity. Because the latency differences between IC and S electrode recordings were insignificant, the IC and S latency values were combined in these curves. P,, which may originate from the auditory nerve and the first brain-stem nuclei, showed the best fit to a regression line. P, appears from about 2.1-3.1 msec after the stimulus onset and usually has a sharp peak. (3) BAEP as a function of stimulus frequency. Figure 3 shows mean BAEP amplitude in response to pure tones presented at a constant stimulus intensity at various frequencies throughout the seagull’s auditory spectrum. The method used here, the inverse of the standard threshold technique, offers a straight forward and efficient means of estimating regions of
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Fig. 2. Latency of the first three positive waveform deflections, P,, P, and P,, of the seagull BAEP measured as a function of sound intensity level. electrode, the waves were more uniform in amplitude. The electrode arrangement which gave the most consistent BAEP waveform was vertex referenced to the posterior palate. Only gross repositioning of the vertex or reference electrode could change the configuration of the BAEP. Figure 1 illustrates the relationship between the amplitude of the BAEP and stimulus intensity. This figure shows the average amplitude (measured peak to trough) of waves P, and P, recorded both intracranially (IC) and from surface (S) electrodes. The amplitude of the BAEP for both IC and S measurements increases systematically with signal intensity up to about 80dB. At higher signal levels the slope of the function shows no further increase, or declines slightly. In some S recordings a third fast wave (Pl) followed by a fourth (slow) wave (PJ or in some IC recordings a fourth fast wave followed by a fifth, slow wave (P,) was observed. The amplitude of P, recorded intracranially (when the electrode was positioned in the brain-stem near the eighth nerve) was SEAGULL:
Auditory frequency response and vocalization spectrum
(BAEP)
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Fig. 3. Amplitude of seagull BAEP and vocalization output as a function sound frequency. The vocal output was derived by Fourier analysis.
S. A. COUNTER
840
heightened sensitivity in the auditory spectrum. This figure shows that the average amplitude of the BAEP to discrete pure tones is greatest in the region of 1.5-3 kHz, with the highest mean amplitude around 2.5 kHz. Above 2.5 kHz the response amplitude (and possibly the ear’s sensitivity) drops off rapidly. The BAEP amplitude-frequency curve of the ear is similar to the spectral content of spontaneous distress vocalizations made by young l&30-day-old seagulls as determined by Fourier transform analysis and shown in the top curve of Fig. 3. (Older and adult seagulls do not readily vocalize in captivity.) The first large peak in the vocal output curve represents a narrow band of frequencies around the fundamental frequency. (4) BAEP during stapedius muscle tension. Vocalization of young and adult seagulls may reach levels in excess of 85 dB (SPL). This creates considerable self-stimulation during vocalization, with the sound level at the head reaching possible acoustic trauma levels. Also, as shown in Fig. 3, the predominant acoustic energy in the seagull’s vocalization spectrum occurs in a frequency range of heightened responsivity for the seagull ear. Counter and Borg (1979) have shown that birds involuntarily activate the single, bilateral middle ear muscle, the M. stapedius, during vocalization to attenuate acoustic self-stimulation. The seagull possesses a welldeveloped stapedius muscle which attaches both the tympanic membrane and columella. When slight mechanical tension (a degree sufficient to induce observable tightening of the tympanic membrane) was induced in stapedius muscle the amplitude of the BAEP was reduced substantially from pre-tension control levels. The mechanical tension simulated the natural stapedius muscle contractions during vocal-
c A
10
ization. The average reduction in the click-induced P, amplitude for four animals was 56% (range 30-74”<). The dashed curve and arrow of Fig. 4C (MST) show the average reduction in amplitude of P, during stapedius muscle tension (relative to control, pretension levels). (5) High intensity noise exposure. The effects of high intensity noise on the auditory sensitivity of the seagull was examined by BAEP in eight animals. The averaged BAEP (P,) recorded immediately after exposure to a 120 dB (SPL) impact noise (IN) is shown in Fig. 4A. In this experiment, the BAEP was measured at three intensity levels (60, 70 and 80dB) immediately following the impact noise. Amplitudes were normalized to the pre-treatment control measurements. The temporary threshold shift caused by the IN is reflected in the resultant 500; (average) reduction in the amplitude of P, of the BAEP observed in the first few minutes following exposure to the 120dB impact sound. Also, the click-induced BAEP response immediately following exposure to 12 hr of a 110 dB (SPL), 2 kHz sound field pure tone is shown in this same figure. In these animals the prolonged noise exposure (PE) caused a substantial reduction in the BAEP amplitude relative to the control response (approximately 35%). Both the IN and the PE effects were generally reversible and hearing appeared to return to normal or near normal levels in a few hours to a few days. In some cases, however, the BAEP was permanently reduced following both IN and PE treatments, suggesting permanent threshold shift or irreversible hearing loss. (6) Masking. Masking is herein defined as the reduction in size or elimination of the click- or tone-induced BAEP as a result of the continuous
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Fig. 4. (A) Percentage reduction in the amplitude of a 60 dB click evoked P, following prolonged exposure (PE) to intense pure tones, impact noise (IN) of 1 lo-120 dB, and during white noise masking (WNM) with signal-to-noise ratios of 0, 10 and 20dB. (B) Percentage reduction in the amplitude of a pure tone-evoked P, in the presence of a white noise masker (WNM) with a signal to noise ratio of - IOdB (---) and the percentage reduction in the amplitude of a click-evoked P, in the presence of various pure tone maskers (PTM) with a signal to noise ratio of - 30 (-). (C) Percentage reduction in the amplitude of P, during mechanically induced stapedius muscle tension (MST) and percentage reduction in the amplitude of a click induced Pz in the presence of the pure tone maskers of B.
Noise effects in seagulls
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BAEP: Seagull (Pure tone masking)
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-
Conlrol~
70 dB Click
---
Mashed.
70 d6cl,ck.
70 dEI WN
Fig. 5. (A) Seagull BAEP waveforms from a single experiment showing the effect of sound field [SS dB (SK)) pure tone maskers of various frequencies on 50 dB click-evoked BAEP responses. (3) Single click evoked (55 dB) BAEP recorded in quiet (-) and in the presence of an 85 dB 2.5 kHz sound field masker (---f. (C) Single click evoked (70 dB) BAEP recorded in quiet f----) and in the presence of a 70 dB white noise masker. All waveform traces begin at the approximate time the stimuli reach the ear.
of an interfering sound masker. In these experiments the term signal to noise ratio (S/N) refers to the decibel value of the wide band click (LOOHz to IO kHz) stimulus or the pure tone (I-3.5 kHz) stimulus in the presence of a simultaneous wide band (10 Hz-10 kHz) masking noise or pure tone maskers. The effects of masking frequency, intensity, duration and spectrum were investigated. The effects of a presentation
wideband, white noise masker (WNM) on a 60 dB cfick-evoked P, (delivered via a tube in the ipsilateral ear canal), are shown in Fig. 4A. The amplitude of the P, responses were reduced by about 70% when the signal to noise ratio was OdB and further reduced to 90% of the control amplitude when the signal to noise ratio was - 20 dB (stimulus = 60 dB, masker = 80 dB). Figure 4B shows the BAEP responses to pure
842
S. A. COUNTER
tone and click stimuli in the presence of both white noise and pure tone maskers. The white noise masker (WNM) was presented to the ear through a sound field speaker at an S/N ratio of - 10 dB. The pure tone maskers (PTM) were delivered by sound field speakers. The P, responses to pure tone stimuli were masked by white noise (dashed curve), and the P, responses to clicks were masked by sound field pure tones (solid curve). Figure 4B shows that the greatest masking effects for both maskers occur between 1.5 and 3 kHz, with peak effect at around 2.5 kHz. The white noise masker reduced the amplitude of the pure tone-induced P, by approximately 6Oyd in the region of 1.5-3 kHz. The pure tone maskers had a maximum intensity level of 80 dB (f 5 dB). The average values plotted from the PTM in Fig. 4B were derived from data sampled at a - 30 dB S/N ratio. These pure tone masking sounds caused an average reduction in the click-evoked P, amplitude of around 807,. The most effective pure tone maskers were those from 1.5 3 kHz. The masking effect of pure tones on either side of this narrow band was significantly lower. The results of both the white noise and pure tone masking studies are consistent with the finding of higher amplitude BAEP and possible heightened auditory sensitivity in the frequency range of about I-3 kHz. The click-induced P2 was equally reduced or completely eliminated by the same pure tone maskers (Fig. 4C). Figure 5A shows the results of one experiment in which a 50 dB click stimulus is masked by pure tones of 80dB (k5 dB) from sound field speakers. This figure shows a systematic reduction in the amplitudes of waves P, and PZ in the masker frequency range of l-3.5 kHz. Also, a significant shift in the latencies of P, and PZ occurs in the effectively masked situation. This pattern is more vividly illustrated in the single intracranial BAEP recording of Fig. 5B. Here it can be seen that the amplitudes of P,, PZ and P, are dramatically reduced in the presence of a pure tone masker of sufficient intensity. This figure also shows four fast, vertex-positive deflections and one slow, late deflection in the control waveform. Further, the latency of P, in the masked response is delayed by about 1 msec. White noise masking has similar amplitude and latency effects on the click-induced BAEP (Fig. X), depending on the noise level and signal to noise ratio. Generul physiological responses to sounds Sonogenic convulsions have been reported in a variety of vertebrates, including birds (Ginsburg, 1954: Lehman and Busnel, 1963). Sonogenic convulsions are characterized by sound-induced startle/ jumps, followed serially by running fits, modified cardiac and respiratory rhythm, physical collapse and violent clonic-tonic seizures of the entire body, after which there is a slow dazed recovery or death from anoxia. This audiogenic seizure activity is believed to be a CNS-mediated response to auditory sensory overload in susceptible animals (Lehman and Busnel, 1963). Behavioral observations were made on seagulls (ranging in age from 2 days old to adults) which were exposed to high intensity noise (85-120 dB) of varying duration. The shortest duration noise, impact noise (from 0.22 caliber blanks), induced instanta-
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Time (51
Fig. 6. Increase in heart rate as a function of time (set) after the impact noise stimulus (1 l&120 dB (SPL)). (A) Curve derived from five animais collected at Boston’s Logan International Airport. (B) Curve measured in seven animals collected from the Mononomy island Wildlife Refuge
neous sonogenic startle in each animal, but no sign of audiogenic convulsions or seizures. Behaviorally, startle was manifested by head jerks and other rapid body movements with each impact noise. Prolonged exposure to pure tones and white noise of 8551 IO dB evoked similar startle responses at the stimulus onset only. Occasional head shakes and avoidance behavior (moving away from the speaker) were observed during high intensity noise exposure periods ranging from several minutes to hours or days. While the classical pattern of audiogenic seizures was not observed in these experiments audiogenic stress responses were recorded consistently. The most quantifiable measure of audiogenic stress was the modification in cardiac rhythm caused by intense noise exposure. Figure 6 shows the average increase in heart rate (for 12 animals}, during periods of audiogenic stress induced by high intensity impact noise (11%120dB). The two curves of this figure represents two distinct populations of seagulls. The steeply rising curve (A) which peaks at a 50:: increase in heart rate in 1 set after the impact noise stimulus and rapidly returns to baseline rate in 8 sec. was obtained from the seagulls collected at Boston’s Logan International Airport. The more gradually rising curve (B) which peaks at about a 20’: increase in heart rate and remains elevated for 16 set post srimulus was obtained from seagulls collected at the Mononomy Island Wildlife Refuge, some 100 miles away from the first population. The animals used in curve (A) were invariably adults which lived in and around the airport. The second population consisted mainly of younger (but not necessarily smaller) birds, either hatchlings or older animals with no known previous exposure to intense unnatural noise. DISCUSSION
BAEP wawform, a~plitu~ie, urtd latency The waveforms of the click-induced BAEP recorded from seagulls, using both surface and intracranial electrodes, are similar to the short latency brain-stem recordings from doves (Bullock, 198 I).
Noise effects in seagulls but remarkably different from those recorded in other Aves (Saunders et al., 1974; Dooling et al., 1975). The waveforms recorded in the present study consist mainly of 34 characteristically fast, vertex-positive deflections in the first 5msec, followed by a large, slow deflection. Each waveform was repeatable and remained consistent in both amplitude and latency over time. Surface changes in electrode position had only a slight effect on either parameter of the BAEP. However, the vertex (positive) to posterior palate electrode arrangement yielded the most consistent and reliable BAEP. The first and largest deflection (P,) probably corresponds to summed eighth nerve and brain-stem nuclei activity. The later deflections (P2, P, and P4) most likely represent summed, volume conducted potentials from several higher brain-stem auditory structures. When the metal electrode was positioned in the brain-stem proper (and closer to the eighth nerve), the amplitude of P, increased more than two-fold. The amplitudes of P, and P, of the intracranial response were also significantly larger than the surface electrode response. This growth in amplitude as the electrode traverses the brain-stem would seem to support the notion that component P, (and possibly Pz) is locally generated from lower level auditory structures, whereas P, is likely to be a volume conducted response from several brain-stem auditory nuclei. It should be added that the filter settings on the amplifier could possibly have eliminated additional slow components in the first 20 msec. The latency of P, (range = l&1.8 msec) is similar to that recorded from the eighth nerve of cats (Buchwald and Huang, 1975; Achor and Starr, 1980; Jewett, 1970) and humans (Jewett and Williston, 1971; Moore, 1971). The latencies of P, and P, in this study decreased systematically with increases in the stimulus intensity, while the latency of P, showed only minor changes. The latency differences between the IC and S electrode recordings (P,, P,, and PI) were unremarkable. Studies by Biederman-Thorsen (1970a,b) have suggested that the avian and mammalian central auditory systems are notably similar. However, the comparatively fewer positive waves observed in the first 20msec of the BAEP would appear to support Schwartzkopff s (1967) hypothesis that birds have fewer relay stations (synapses) between the ear and telencephalon than mammals. Response to stimulus frequency
It is possible that a behavioral audiogram could be obtained in seagulls as in other avian species through a lengthy conditioning process. However, BAEP responses to pure tones can also be used to assess hearing sensitivity and involves less time and variability. Brain-stem evoked potentials cannot provide absolute measures of auditory thresholds because they are summed potentials which are dependent on factors such as the size of neuronal populations and the spatial relationship between the recording electrode and those cell populations. Nevertheless, regions of high sensitivity can be reliably predicted by changes in the amplitude of the BAEP at various frequencies within the auditory spectrum. Using the amplitude of P, as the index of sensitivity, the results
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of this study showed the range of 1-3 kHz to be a region of heightened auditory responsivity in seagulls. This finding is similar to that observed in other avian species (viz. domestic fowl and pigeon) by several investigators (Gates et al., 1975; Tanaka and Smith, 1978; Counter and Borg, 1979). Discrete Fourier transforms performed on selected segments of distress and other types of vocalizations from young (l O-30-day-old) seagulls (particularly herring gulls) showed that most of the vocal energy falls in the frequency range of 1.5-3 kHz, with a peak output level at around 2.5 kHz. These findings lend further support to the observations of heightened auditory sensitivity around 2.5 kHz. It is also interesting to note that the seagull’s hearing is particularly acute in the same broad frequency range that humans hear best, a finding which may have implications for seagull control procedures. Masking Of particular interest in this study was the effects of certain bandwidths and types of noise on seagull hearing. This aspect of the study was especially relevant to the question of the effect of certain components of jet and propeller driven aircraft engine noise on the ears of exposed seagulls. Seagulls around coastal airports account for a high percentage of the bird/aircraft collisions worldwide. No generally accepted scientific explanation has been advanced to explain these collisions. It is possible that the noise from jet and other aircraft engines may have profound effects on the behavior and physiology of seagulls in the immediate vicinity. However, additional studies are necessary in order to elucidate the precise nature of the effects of aircraft noise on the ears of seagulls and other birds. In any event, it seems particularly significant that the findings of the present study show that one region of heightened sensitivity in seagull hearing corresponds to the bandwidth of maximum output in many jet aircraft, i.e. around l-3 kHz. The amplitudes of P, and P, were systematically reduced by wideband noise and pure tone masking stimuli with signal to noise ratios ranging from 0 to 30dB. Pure tone masking stimuli of l-3.5 kHz were used because these discrete frequencies cover a region of heightened sensitivity in the seagulls’ auditory spectrum and correspond to the major frequency components of jet aircraft engine noise. The most effective pure tone maskers were those in the 1.5-2.5 kHz range. A 2.5 kHz masker was found to be particularly effective (Fig. 5A). Also, masking of the pure tone-induced BAEP by wide band noise was most effective when the pure tone stimulus was in l-3 kHz range, at all signal to noise ratios. These findings also add additional support to the conclusion regarding heightened auditory responsivity in seagulls around 2.5 kHz. In field studies at Boston’s Logan International Airport it was found that many seagulls are exposed to intense jet noise for several hours during the day. This is particularly evident in the earlier morning hours when hundreds of herring, blackback and other seagulls congregate to roost on several “favorite” runways. Some of these animals are exposed to take-offs and landings of jets and propeller aircraft
844
S. A. COUNTER
every 90 or so set, at least 10 hr a day for many days. Sound level measurements of jet noise show it to be in excess of 85 dB SPL (close to IOOdB) within 1500 feet of the aircraft. Most of the intense noise energy of the older model jet aircraft (which tend to be noisier than some newer models) is concentrated in the region of 1-3 kHz, while that of the newer models is in the area of l-2 kHz. The equally intense “rumble” sound made by old and new aircraft as they pass a stationary receiver and travel a short distance from the receiver, is similar to wideband white noise. It is reasonable to assume that these intense jet noises would have detrimental effects on the hearing of seagulls. In the first instance, the acoustic masking effects of jet aircraft in the near-field are likely to create sonic interference for all other auditory signals or cues available to the organisms and may possibly cause a breakdown in binaural reception and localization, leading eventually to disorientation. Counter and Borg (1979) have shown that sound travels through a complex interaural passageway in the avian cranium in such a way as to enable the animal to localize a sound source. Any noise interference with this delicately balanced system may render it ineffective, and make the animal unable to locate the source of even threatening sounds in the near and far fields. Such effects could possibly lead to runway and mid-air collisions between birds and aircraft. Secondly, the intense and rapidly rising noise levels may cause audiogenic stress in some seagulls. Cardiac responses to the early seconds of intense, long duration noise and impact noise caused dramatic increases in heart rate (and in some instances volume), reflecting a sonogenic stress reaction. While no seizure activity was noted, these sonogenic startle or stress reactions, when induced by aircraft noises, could possibly lead to disorientation and collisions. In order to clear the runway of seagulls, some airports engage Field Maintenance “Bird Control Teams” that patrol the runways and perimeter of the airport in vehicles, and fire warning shots from 12 gauge shotguns at individual seagulls or flocks of seagulls (and other birds) near the runways. The impact noise component of this study was similar, both quantitatively and qualitatively, to that produced by the Field Maintenance impact noise equipment. The purpose of this component of the study was to examine the primary and secondary auditory physiology changes in seagulls resulting from the impact noise. The results show several remarkable effects. First, at close range the impact noise causes an immediate auditory threshold shift (or reduction in auditory sensitivity as reflected by a decrease in BAEP amplitude). The development and extent of permanent threshold shift has not been fully determined at this time. Secondly, sonogenic startle and stress were observed. It is significant to note, however, that seagulls collected around the airport (which tended to be older) exhibit a very dramatic increase in heart rate immediately following the noise onset. In these birds, the heart rate returned to normal, pre-stimulus levels within a few seconds after the startle-inducing stimulus. This response suggests a form of adaptation to the impact noise stimulus. On the other hand, birds collected from an isolated area some 100 miles away from the airport and with no
previous (known) exposure to intense unnatural or impact noise exhibited significantly less sonogenic startle or stress immediately following the stimulus onset. Rather, the latter group showed only a small (20x), slow rise in heart rate, but this remained elevated for twice as long as that of the airport birds. These findings suggest that the airport seagulls which may have routinely experienced the explosive warning shot noise are effectively startled by the sound, but disregard the threat after a few seconds. Conversely, the inexperienced birds are only mildly startled by the curious noise, but for a longer period, possibly because it is a totally unfamiliar and meaningless stimulus. It is difficult to test the validity of Schwartzkopff’s hypothesis that central analysis of acoustic information is more important than peripheral analysis in Aves (Schwartzkopff, 1960a,b, 1967, 1968). However, the masking experiments of this study may shed some light on the relative contributions of both levels. At moderately high intensity levels, pure tone maskers which have a more specific place effect along the basilar papilla caused a general reduction in the amplitude of P,, P, and P,, but did not cause a major alteration in the shape or configuration of the waveforms. This kind of response might suggest that the masking effect was more peripheral than central. On the other hand, white noise maskers (which activate most regions of the cochlea) and very high intensity pure tone maskers effectively obliterated the BAEP and/or altered its configuration beyond recognition. These responses suggest both central and peripheral effects. High intensity white noise and pure tones would be expected to cause massive displacement of the entire basilar membrane and desynchronize the firing of eighth nerve fibers. Brain-stem nuclei would therefore receive less synchronized threshold level summated activity, as reflected by the substantially reduced BAEP recordings. Further interaural masking studies are necessary to fully evaluate the central and peripheral effects of masking. Acknowledgements-The author wishes to thank Priscilla Tsao for laboratory assistance, John Dowling and C. James Ciotti for laboratory support, John Lortie and Denver Holt of the U.S.A. Fish and Wild Life Service, the Massachusetts Division of Fisheries and Wild Life, Robert D’Etremont and the Boston Logan International Airport Field Maintenance, George Deegan, Robert Paris, Steven Grasse for animal room assistance, Erik Borg, Ernest Moore and Manny Don for helpful comments and the Harvard Biological Laboratories.
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