Central auditory metabolic activity induced by intense noise exposure

24 Hearing Research, 61 (1992) 24-30 © 1992 Elsevier Science Publishers B.V. All rights reserved 0378-5955/92/$05.00

HEARES 01762

Central auditory metabolic activity induced by intense noise exposure

Allen F. Ryan a,b, G. AIf Axelsson c and Nigel K. Woolf "~ Departments of a Surgery / Otolaryngology and h Neurosciences, UCSD School of Medicine and VA Medical Center La Jolla, California, USA

and c Department of Audiology, Sahlgrenska Hospital, Goteborg, Sweden

(Received 23 October 1991; Revision received 6 March 19q2; Accepted 12 March 1992)

Neural activity in the central auditory system was mapped by measuring 2-deoxyglucose (2-DG) uptake during a one hour exposure to a two-octave (1414-5656 Hz) hand of noise. Gerbils were exposed to 100, I l0 or 120 dB SPL, intensities which can produce only temporary (100 dB) or both temporary and permanent (120 dB) hearing loss. Exposure to 100 dB SPL evoked high levels of neural activity throughout responsive regions of auditory nuclei. At 110 dB SPL, a central region of low neural activity was surrounded by areas exhibiting increased activity. At 120 dB SPL, neural activity was low in almost all areas of auditory nuclei. To study the effects of permanent hearing loss on auditory neuronal activity, other animals were given 2-DG during exposure to 65 dB SPL broad band noise as a test stimulus, two months after exposure to the noise band at I l0 dB SPL. Central auditory nuclei showed a tonotopic region of low neural activity corresponding to an approximately 3 kHz pure tone, surrounded by regions of evoked activity. The deficits in evoked metabolic activity observed both during and long after noise exposure appear to exceed those predicted from the degree of temporary and permanent threshold shift produced by the same noise exposures.

Noise damage; Cochlea; 2-Deoxyglucose; Gerbil; Auditory neurons

Introduction

Exposure to high levels of acoustic energy produces losses in hearing sensitivity which can be temporary, or permanent. Much of this loss is thought to occur in the end organ: temporary threshold shift (TTS) through changes in the sensitivity of the cochlear hair cells, and permanent threshold shift (PTS) through their outright loss. However, recordings from single neurons in central auditory structures have indicated that noise exposure can produce profound changes in the responses of central auditory neurons. These central changes often exceed those observed in the cochlea (Lonsbury-Martin and Meikle, 1978; Salvi et al., 1979; Popelar and Syka, 1982). The reason for this difference is not clear. However, these authors have suggested that excessive sound stimulation overtaxes central auditory as well as cochlear capabilities, leading to threshold shifts which originate within the central auditory pathway itself.

The 2-deoxyglucose autoradiographic technique provides a method of exploring the responses of neurons in many neural systems (Sokoloff et at., 1977), includ- ing the auditory system (e.g. Webster et al., 1978; Sharp et al., 1981; Nudo and Masterton, 1986; Ryan and Woolf, 1988; Ryan et at., 1989, 1990). It is espe- cially useful in mapping activity in the spatial domain.

Correspondence w: Allen F. Ryan, ENT, UCSD, 9500 Gilman Dr., 0666, LaJolla, CA 92093-0666, USA. Fax: (619) 534-5319.

It provides information about metabolic responses of tissue, which in brain are closely related to neural activity (Sokoloff, 1977).

The present study was designed to explore the effects of noise exposure on central auditory metabolism and neural activity. Noise exposures which have been well characterized in our laboratory were chosen, so that the relationship between metabolic responses to noise and eventual development of "vrs and PTS could be examined. To determine the immediate effects of traumatic noise on central auditory neural activity, 2-DG uptake was assessed during intense noise exposure. To determine the effects of PTS on evoked 2-DG uptake, some animals were tested two months after exposure to noise trauma.

Methods

Subjects Mongolian gerbils (Meriones unguiculatus) were used

as subjects. Only young adult (45-90 days old) animals were used since gerbils tend to develop vesicular neu- ropathology in the cochlear nucleus (CN) with increas- ing age (Ostapoff and Morest, 1989). While this pathology has no known functional correlate, young animals were employed to minimize any possible effects.

Noise exposure Wide-band noise generated by a Grason-Stadler

1285 noise generator was band-passed filtered (1414-

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5656 Hz) through a Rockland 852 active filter, ampli- fied with a Crown D60 amplifier, attenuated with a Hewlett-Packard 350D attenuator, and applied to a JBL 2482 midrange driver coupled to an Altec 5lIB horn. Animals were stimulated continuously for one hour in a c:,'lindrical cage (20 cm diameter) suspended centrally in a double-walled, sound attenuated cham- ber (IAC 1200A) with anechoic lining, 10 cm from the aperture of the horn. The intensity of the noise was either 100, 110 or 120 dB SPL (re 0.002 dyne/cm2). Three animals were exposed to each intensity.

Noise intensity was measured for each exposure using a Bruel and Kjaer 2209 sound level meter with a 1" condenser microphone and type 1613 octave filter set, by averaging the readings obtained in the 2.0 and 4.0 kHz bands. The spectral characteristics of the two- octave noise band were measured with a Bruel and Kjaer 2113 audio frequency analyzer, and have been published elsewhere (Ryan and Bone, 1978).

To assess the long-term effects of noise damage on evoked neural activity, three animals were exposed to the noise band as above at 110 dB SPL for one hour, and allowed to recover for two months. 2-DG uptake was then assessed during exposure to a probe stimulus: broad band noise at an intensity of 65 dB SPL. At this intensity, broad band noise activates the entire tonotopic extent of auditory nuclei (Sharp et al., 1981). Thus any deficits in neural activity caused by PTS restricted to a narrow frequency band should appear as gaps in 2-DG uptake within those frequency regions. Wide band noise was fed through a graphic equalizer, which was adjusted until equal intensities were measured in each octave band from 250 to 16 kHz using the sound level meter and octave filter set.

2-Deoxyglucose The 2-DG methods have been described in detail

elsewhere (Ryan et al., 1989). Briefly, 2-deoxy-D- IP4C]-glucose (57 mCi/mM, Amersham-Searle)was evaporated and reconstituted in saline. Alert and unanesthetized animals were injected intraperitoneally with 16.7/zCi of 2-DG/100 g body weight, in 100/zl. Acoustic stimulation was provided continuously. Imme- diately following the one hour exposure to noise, subjects were instantaneously decapitated and their brains were rapidly dissected and frozen in isopentane cooled to -30°C. The brains were further cooled to -70°(2 on dry ice, and coated with thin layers of Lipshaw embedding matrix and serially sectioned in the transverse plane on an American Optical cryostat at a section thickness of 20/~m. All sections were mounted on coverslips and rapidly dried on a hotplate at 60°C. Sections were exposed on Kodak SB-5 X-ray film for 7 days, developed in Kodak X-ray film developer for 5 min, washed 2 min, fixed in Kodak rapid-fix for 5 min, washed 20 rain and air-dried.

Data analysis Restricted regions of very high radioactivity (com-

pared to that of the adjacent tissue within the nucleus) were readily apparent in the autoradiographs. This was identified visually as evoked 2-DG uptake.

A pure tone of low-to-moderate intensity (25-65 dB SPL) activates a restricted volume of an auditory nucleus. Based on studies with a series of pure tones spanning the audible range, a tonotopic axis can be defined in an auditory structure as a line running through the centers of such nuclear volumes (Ryan et al., 1989). The tonotopic axis of the dorsal cochlear nucleus (DCN) and of the inferior colliculus (IC) approximately parallels the transverse plane, and the entire axis is visible in single sections through the center of these nuclei. Therefore, these nuclei were used for analysis of results across frequencies.

Autoradiographic images were digitized on a Drexel University image analysis system. The image analyzer was calibrated using optical density standards (Kodak). The densities of images from ~4C standards (New Eng- land Nuclear) were read to assure that the images of brain structures were not saturated. The optical density for each structure was read on six adjacent sections. The following structures had optical densities determined on the left and right sides: DCN, anterior ventral cochlear nucleus (AVCN), posterior ventral cochlear nucleus (PVCN), superior olivary complex (SOC), IC, and medial geniculate nucleus (MGN). As often the case with relatively simple stimuli such as continuous noise, auditory cortex responses were mini- mal and thus were not analyzed. For each nucleus, that portion of the structure which responds to the frequencies of the stimulating noise band at low-to-moderate intensities (30-60% of the tonotopic axis) was measured. For the DCN and IC, nuclei in which the entire tonotopic axis is present in a single coronal section, the frequency regions below (0-30% of the tonotopic axis) and above (60-100%) the noise band were also measured. The optical density of the anterior inferior cere- bellar peduncle (ICP) at the level of the DCN was also measured bilaterally.

Optical density measurements were analyzed as fol- lows. For each section, the background optical density of the film was subtracted from all structure densities. The optical density of each gray matter structure was then divided by the averaged optical density of the ICP, to obtain an optical density ratio. Such ratios of gray matter to white matter were used to help control for small variations in section thickness, exposure and development times, and tracer dose (Sharp et al., 1983). They provide a measure of relative 2-DG uptake which we have used previously to demonstrate stimulus-related auditory neural activity (Ryan et al., 1982; 1989; 1990). The optical densities of auditory nuclei on the two sides of all three subjects in each stimulus condi-

26

tion were measured and then combined for analysis. Optical density ratios were analyzed by the Mann- Whitney U-test for ratios.

Results

Autoradiographs comparing the 2-DG responses of the posterior CN to noise at 100, 110 and 120 dB SPL with 2-DG uptake in silence are presented in Fig. 1. In silence, 2-DO uptake is relatively low and uniform throughout both the PVCN and DCN. This is represented by the uniform, moderate density of the autoradiographic image of each nucleus. At 100 dB SPL, 2-DG uptake in the PVCN was markedly higher than in silence. This was also the case in the DCN, with the exception of the molecular cell layer. Uptake was high-

est in a band of tissue which corresponds tonotopically (Ryan and Woolf, 1988; Ryan c t a l . , 1990) to the 1414-5656 Hz band of the stimulating noise.

At 110 dB SPL, 2-DG uptake was low in a region centered at the frequencies of the noise band, in both DCN and PVCN. This region spanned the frequency representation of the DCN from about 1500 to 12000 Hz. Uptake in regions corresponding to frequencies above or below this band were elevated. At 120 dB SPL, 2-DG uptake was low throughout a broader area of each auditory nucleus. Modest levels of evoked 2-DG uptake were observed in areas representing frequencies below, and to a lesser extent above, the region of low uptake.

Fig. 2 illustrates the response of the IC to intense noise exposure. The results are similar to those observed in the CN. At 100 dB, increased 2-DG uptake

100 d B i

1 1 0 ~ . ~ d B ..,.~.. ,.,,~,,.. ,..~,.~..,-. .... .' " , ' , ' , ~ , . . . . . .'. 120 dB ~ , . . - , , : ~ . . . . . . .... , . , , : .~, ; : . : : , ;,r.~,':, ~ ' , ¢R11~ , "=¢ ' . . . . . ' , ',.,',': .~."..' . . . . . " m , ~ ' , ~ m - ~ ~ : ~ " :' " " . .~.-,~.:~'.~ ~',;~"

,~! ~ ~,~..~.

Fig. 1. Patterns of 2-DG uptake observed in the PVCN and DCN during a one hour expnsure to a 2-~ctave (1414-5656 Itz) band of noise at intensities of 100, 110 or 120 dB SPL, compared m those seen in silence. Low frequencies are represented ventrolaterally and high frequencies dorsomedially in the CN. The 1013 dB SPL stimulus evoked high levels of 2-DG uptake in regions representing all frequencies. The 110 dB stimulus produced a region of very low neural metabolism corresponding the frequencies of the noise band, but high levels for surrounding frequencies. The 1213 dB stimulus produced very low 2-DG uptake in the frequency regions of the noise band, and only slight elevations in

surrounding regions.

27

S i l e n c e ' 1 0 R • ,.:;~ ~.J-,~.:~-:'~.,~

• . . ] ~ [ ~ R Q ~ . ~ ' . ~ . . : " . ' - . v ~ ' . ~ " , . - ~ ,

. ~ , - , . . . -

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:~,,.~ .... ~ ~ , _.,...,~< .- - - . . ";"~"- ~..-.--~.~,~?,~'.:.,,~

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1 1 0 d a . ' "i 120dB ., 'i: '~s:::._.i:::.i,!

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Fig. 2. Patterns of 2-DG uptake induced in the IC by exposure to noise. Low frequencms are represented dorsally and high frequencies ventrally in the IC. Responses were similar to those seen in the CN. At 100 dB uptake was evoked in the central nucleus (CN) of the IC and in the inner portion of the external cortex (ECL Uptake was noticeably higher in regions corresponding to the frequencies of the noise band than at other locations• At 110 dB SPL a central band of slightly higher 2-DG uptake is observed in the region of reduced metabolism corresponding to the

frequencies of the noise band. B = brachium of the IC; DC = dorsal cortex.

was observed in the central nucleus and in the medial portion of the external nucleus of the IC, with the highest uptake in the region corresponding to frequencies of the noise band. At 110 dB, a central band of low 2-DG uptake was observed. However, unlike the CN, a band of slightly elevated 2-DG uptake was present in the center of the region of low uptake. At 120 dB, the region of low 2-DG uptake was slightly broader and uniform. Evoked 2-DG uptake was observed in frequency regions below, and to a lesser extent above, the noise band.

Fig. 3 shows relative 2-DG uptake, expressed as optical density ratios, in the various nuclei of the auditory system in response to noise exposure at 100, 110 or 120 dB SPL. As can be seen from the figure, 100 dB SPL noise greatly increased 2-DG uptake in the region corresponding to the noise band. However, 110

and 120 dB SPL produced no increase in neuronal metabolism above that seen in silence.

Fig. 4 shows relative 2-DG uptake in different frequency regions within the DCN (4-1) and IC (4-2), in response the noise band. While all frequency regions showed elevated 2-DG uptake at 100 dB SPL, only those regions outside of the band showed evoked 2-DG uptake at 110 dB SPL, and to a lesser extent at 120 dB SPL.

Fig. 5 illustrates typical CN and IC responses to a probe stimulus, wide band noise at 65 dB SPL, two months after exposure to the two-octave noise band at 110 dB SPL We have shown in previous behavioral studies that this 110 dB SPL exposure produces an average of 15-20 dB of PTS at 3-6 kHz in the gerbil (Ryan and Bone, 1978). The 65 dB SPL broad-band stimulus, which normally activates the entire tonotopic

28

8

CC 6-

~>" S- t- • 4' a

"~ 3'

0

AVCN PVCN DeN SOC

17 0da [ ] 100dB • 110riB !~ 120dB

IC MGN

Fig. 3. Relative uptake of 2-DG into nuclei of the central auditory system during exposure to three intensities of noise which induce temporary and/or permanent damage to the cochlea. Uptake in each nucleus was measured in the tonotopic region corresponding to

the noise band.

axis, failed to elicit evoked 2-DG uptake from a band of tissue in the 2-4 kHz region of central auditory structures.

D i s c u s s i o n

Our results indicate that intense noise exposure can sharply increase central auditory metabolism or, at higher intensities, suppress the sound-evoked response to the stimulus. The spatial distributions of enhance- ment versus suppression of central auditory metabolism correlate reasonably well with TTS and PTS which we have documented behaviorally using the same noise

stimuli in a previous study (Ryan and Bone, 1978). Thus a one-hour exposure to 100 dB SPL produces a moderate (20-40 dB) TI'S across much of the audible frequency range of the gerbil, but no PTS. The same noise exposure increases 2-DG uptake across the tonotopic axis of central auditory structures in the gerbil. At 110 dB SPL, 40-60 dB (ff TTS is observed across most audible frequencies, but PTS is restricted to a band of frequencies closely related to the exposure frequency. With the same stimulus, 2-DG uptake increased in central auditory regions representing frequencies above and below the noise band, but not in regions representing the noise band frequencies. Fi- nally, the 120 dB SPL noise produces both PTS and lack of evoked metabolic response across a range of frequencies much wider than that observed at 110 dB SPL. Thus lack of evoked 2-DG response to the noise band is correlated with eventual development of PTS.

Perhaps the simplest explanation for the relationship between lack of evoked 2-DG uptake daring noise exposure and eventual PTS is that reduced central 2-DG uptake reflects damage to the end organ; that is, regions of the cochlea which will display PTS are sufficiently damaged that they cannot respond to the stimulus. However, the lack of evoked 2-DG uptake observed in the central auditory system during the 110 dB SPL noise exposure would not be expected from the degree of TTS or PTS induced by the noise. For example, the TTS induced by a 110 dB noise exposure is 40-60 dB, and the eventual PTS is 15-20 dB (Ryan and Bone, 1978). While we did not measure the behavioral thresholds of the animals used in the 2-DG study, if their threshold shifts were comparable then the 110

.o

.>,

a

o

Frequency region: DCN

6' • Noise band 8' [] Above band

A [ ] Below band 5' 0 7'

4. .-2" s.

0 0 dB 100 dB 110 dB 120 dB

Intensity (dB SPL)

Frequency region: IC

• Noise band [ ] Above band

B [ ] Below band

0 dB 100 dB 110 dB 120 dB

Intensity (dB SPL) Fig. 4. Relative uptake of 2-DG into three frequency regions of the DCN and IC: frequency regions corresponding to the noise band (30-60% of

the tonotopic axis), frequencies above the band (60-100%), and frequencies below the band (0-30%).

29

dB stimulus was 50-60 dB above behavioral threshold. The absence of metabolic response to the stimulus in the frequency region corresponding to the noise band at 110 dB can only be e~'~lained on the basis of threshold shift if the 2-DG animals experienced much more T r s than we have previously observed. While noise exposure effects are notoriously variable, it seems unlikely that a large difference occurred in all three of the 110 dB subjects in the 2-DG study.

Alternatively, a central auditory mechanism may be responsible. Many neurons in the central auditory system display nonmonotonic responses to increases in stimulus intensity, such that very intense stimuli produce a suppression of neuronal activity back to or even below the spontaneous discharge rate (e.g. Rose et al., 1963). It is therefore possible that the normal response to very intense stimuli is a depression of central auditory metabolism. Arguing against this interpretation is the fact that many auditory neurons do respond mono- tonically to intensity. Moreover, we have shown that 2-DG responses to both narrow-band and broad-band acoustic stimuli are monotonic in the CN up to 105 dB SPL (Sharp et al., 1981; Ryan et al., 1989). However, this possibility cannot be ruled out.

A second possible central auditory mechanism is that some central auditory neurons may be affected by acoustic overexposure to a greater extent than behavioral thresholds. Physiological experiments (Lonsburv-

7"..

'ON

Martin and Meikle, 1978; Salvi et al., 1979; Popelar and Syka, 1982) have shown that the acoustic thresholds of many single units in the central auditory system can be depressed to a greater extent than behavioral thresholds in response to noise exposure. Our data support these physiological results, and suggest that many auditory neurons may display noise-induced deficits in their ability to sustain responses to continuous stimulation. These deficits appear to exceed what would be predicted ori the basis of behavioral threshold shifts. This interpretation requires that behavioral thresholds be mediated by neurons exhibiting the smallest amount of threshold shift, a n d / o r by unit responses to signal onsets. Onset responses might have lower thresholds than the continuous discharge which presumably mediates increases in 2-DG uptake during a one-hour~ continuous stimulus.

The nature of any possible central auditory changes induced by noise cannot be determined from our data. The uptake of 2-DG has been shown to be closely related to neuronal actMty (Sokoloff, 1977). However, exactly what aspect of activity is reflected by 2-DG uptake is a subject of some controversy. Studies which correlate evoked spike activity and 2-DG uptake have typically observed a close relationship (e.g. Theurich et al., 1984). Stimulus-evoked increases 2-DG uptake ,~,'~ also observed in fiber tracts which lack ne~0na l so- mata or syna0ses (Ryan and Sharp, 1982), further

Fig. 5. Patterns of 2-DG uptake evoked by exposure to 65 dB SPL wide band (0.1-20.0 Id-lz) noise, which would normally stimulate all acoustically responsive regions of central auditory nuclei, two months after a one hour exposure to a noise band (1414-5656 I-Iz) at 110 dB SPL. In the PVCN, DCN and IC, a gap in 2-DG uptake is observed which corresponds tonotopically to the representation of an approximately 3 kHz

laura tone .

3O

suggesting a link between spike discharge and local metabolism. However, while spike rates often correlate with 2-DG uptake, it cannot be assumed that increased uptake is a marker for neural excitation. Activation of a purely inhibitory system can also lead to increased 2-DG uptake (Ackerman, !984; Nudo and Masterton, 1986), suggesting that activation of synapses without resultant spike generation increases local metabolism. However, it seems reasonable to conclude that changes in evoked metabolism in the central auditory pathway are closely related to changes in overall neuronal activity.

The metabolic unresponsiveness observed ia the mid-frequencies during exposure to 110 dB SPL noise appeared to recover over time. At two months post-exposure, a much less intense stimulus (65 dB SPL broad, band noise) activated more of the tonotopic axis of the CN and IC than did the 110 dB SPL noise. However, the 65 dB SPL stimulus did not produce increased 2-DG uptake in a narrow band of tissue related to the frequenc~v region of the noise e~posure. This occurred in spite of the fact that the stimulus intensity was well above the expected PTS (15-20 riB) in these animals. As with the results observed during intense noise exposure, this suggests a possible deficit in central auditory responsiveness which exceeds the expected behavioral threshold shift.

The gap in the central representation of the broad band signal also offered an opportunity to study the response of the auditory system to missing information in an auditory signal. In the visual system, 2-DG studies have shown that spatial gaps in a visual stimulus can be 'filled in' at the higher levels of the central visual pathway. In striate cortex, a gap in a visual grating pattern of high spatial frequency is not represented in 2-DG responses, while a gap in a grating pattern of low spatial frequency will be represented in some cortical layers but not in others (Tootell et al., 1988). This phenomenon appears to reflect spread of activity from active into inactive cortical regions. Our data suggest that the auditory system does not similarly reconstitute missing information, at least up to the level of the IC. The gap observed in the representation of the noise stimulus in the IC was similar in extent to that observed in the CN. The lack of 2-DG responses in auditory cortex prevented us from determining whether spatial reconstruction of the signal might occur at the cortical level of the auditory system.

Acknowledgements

Supported by the Research Service of the US Veter- ans Administration, by US NIH/NIDCD grant DC00139 and by the Swedish Work Environment Fund.

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Central auditory metabolic activity induced by intense noise exposure

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