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Receptor and neural responses in auditory masking of low frequency tones
Electroencephalographyand ClinicalNeurophysiology Elsevier PublishingCompany,Amsterdam- Printed in The Netherlands
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RECEPTOR AND NEURAL RESPONSES IN AUDITORY MASKING OF LOW FREQUENCY TONES J. T. MARSH, J. C. SMITH AND F. G. WORDEN1 Department of Psychiatry and Brain Research Institute, University of California, Los Angeles, Calif 90024 and Neurosciences Research Program, 280 Newton Street, Brookline, Mass. 02146 (U.S.A.) (Accepted for publication: July 14, 1971)
The threshold for theperceptionofapure tone is elevated in the presence of noise presented at the same ear. This perceptual phenomenon, known as monaural masking, has been studied extensively (Licklider 1951 ; Ward 1963 ; Jeffress 1970), but the mechanisms underlying it are not completely understood. To explore these mechanisms, electrophysiological data were recorded from the round window of the cochlea, and the first brain relay (cochlear nucleus) of cat. In order to establish that the stimulus conditions used for the cat qualified in terms of the known psychophysics pertaining to masking, the stimuli were first tested on human subjects,
the subjects who were tested using a 20 dB increase in noise level, threshold elevation averaged 21.2+3.9 dB. This one-to-one relationship of increase in masker intensity to increase in tone detection threshold has been widely reported in the psychophysical literature. Similar stimulus conditions were then presented to cats, using the same earphone fitted with an aural cannula containing a probe microphone (B & K, Model 4133) to monitor sound pressure levels near the ear drum. Ten cats with electrodes chronically implanted on the round window (to record the cochlear microphonic response), and in the cochlear nucleus (CN), were used. With the subjects anesthetized EXPERIMENT I (sodium pentobarbital, 35 mg/kg, intraperitoneal), electrophysiological responses were amMethods plified, monitored on an oscilloscope and recordFor each ear of five human subjects, detection ed on FM magnetic tape for subsequent analogthresholds for a 1.5 kc/sec tone were determined to-digital conversion and response averaging in the presence ofnarrow-band filtered noise, one (IBM 360-91). Results reported elsewhere critical band in width (1.39-1.61 kc/sec), at two (Worden and Marsh 1968) suggest that anlevels of sound pressure, 70 dB and 80 dB (re esthesia is not a significant complicating variable 0.0002 microbar). Subjects sat in a sound-at- for responses at this level of the auditory system. tenuated room (Industrial Acoustics Corp., The electrodes, recording procedures and equipModel 400), wearing a calibrated earphone ment have been described previously (Marsh and (Grason-Stadler TDH-39), and were presented Worden 1968; Worden and Marsh 1968). with a counterbalanced order of noise condiThe auditory frequency-following response tions ; an ascending order of tone intensities was (FFR) served as the measure of tone-evoked used to determine threshold. For this 10 dB activity in CN. The FFR, as previously reported increase in noise level, the increase in tone detec- (Marsh and Worden 1968, 1969 ; Worden and tion threshold averaged 10.8 + 1.7 dB. In two of Marsh 1968), is a microphonic-like wave form 1 Supported by U.S. Public Health Service Grant MH observed in the auditory pathway which shows 03831-11. Computing assistance was obtained from the varying amounts of harmonic distortion but Health Sciences Computing Facility, U.C.L.A., sponsored always a fundamental frequency equal to that of by N.I.H. Grant RR-3. the stimulus. FFR has a latency or phase shift Electroenceph. clin. Neurophysiol., 1972, 32:63 74
64 appropriate to the level from which it is recorded and is observed to change in amplitude as a function of stimulus intensity. Previous experiments have demonstrated that the F F R is a neural response rather than artifact, or a remote pickup of the cochlear microphonic (CM), which it resembles. The F F R is recordable only within the auditory pathway at and below the level of the inferior colliculus and is distinct from the CM in the following respects : (1) the frequency band over which F F R can be recorded is much narrower than the CM bandwidth; (2) FFR disappears concurrently with other neural activity during asphyxia while CM remains for some time; (3) F F R is totally abolished at and above CN after cutting the eighth nerve or during cooling with a cryoprobe in CN, while, concurrently, CM remains undiminished. In the latter experiment, as CN is allowed to return to normal temperature, F F R reappears and attains its pre-cooling amplitude (Marsh et al. 1970). The effect of noise on tone-evoked FFR was explored in" two ways: Ca) observation of responses displayed on an oscilloscope (CRO) with sweep phase-locked to the tone stimulus; and (b) measurement of the amplitude of the sine wave recovered from the noise background by response averaging (N = 500) with sweep timelocked to the tone stimulus so as to average out the noise. Results Both CRO displays and averaged responses are illustrated in Fig. 1. In the CRO photographs, it can be seen that an 80 dB tone (MIKE, column 1) evokes a sinusoidal pattern in both receptor (CM) and neural responses (LCN). With the addition of noise (column 2), this pattern becomes less distinct, and with a 20 dB increase in noise intensity (column 3), it is completely obscured. It can also be seen in the CRO photographs that noise exerts a differential effect on the amplitude of the response envelope, which increases for CM but not LCN. In this regard, the CM response resembles that of the monitor microphone ( M I K E ) more than does the LCN response, Response averaging (bottom photographs in each row of Fig. 1) demonstrates a further effect of noise on tone-evoked responses. For both the
J.T. MARSHet al. receptor and neural responses, the addition of noise results in a diminution of the averaged sine wave (column 2), and this effect is enhanced by increasing the noise intensity (column 3). As can be seen from the averaged responses, the decrement appears greater in the neural than in the receptor responses. For a 20 dB increase in masker intensity, the mean decrement in averaged response amplitude was49.6~o or approximately 6 dB for CM and 60.4~ or approximately 8 dB for CN. This decrement in neural response is significantly greater than that in the receptor response (P< 0.001). The 6 dB decrement in CM resulting from a 20 dB increase in noise amplitude may be attributed to the interference effect (Covell and Black 1936 ; Wever et al. 1940), and resembles data obtained by Engebretson andEldredge (1968) using interference tones applied to guinea pig cochlea. We have since cornpared their interfering tone stimuli to our filtered noise bursts with regard to interference efficacy and have found the two classes of stimuli to be roughly equivalent psychophysiologically (within +0.5 dBofattenuationatRWofacontinuous 700 c/sec test tone). Our observation, that the reduction in F F R resulting from a 20 dB increase in masker was nearly always significantly greater than the corresponding reduction in CM, suggests that the interference effect discussed by Wever et al. (1940), and the subsequent cochlear non-linearity modeled by Engebretson and Eldredge (1968) do not fully account for the "masking" effect observed at CN following the addition of noise to tone. A parallel can be seen between the masking effect of noise in raising tone detection thresholds and its blurring and amplitude-reducing effects on tone-evoked electrophysiological responses. If the decrements in electrophysiological responses reported here are indeed correlates of psychophysical masking phenomena, then the greater reduction at CN suggests that there is an important neural as well as receptor component in masking. This is consistent with the interpretation ofWever et al. (1940). We have suggested that FFR is the envelope of unit discharges that are phase-locked to the tone stimulus. The large decrement in averaged FFR amplitude with the addition of noise suggests the possibility that the noise pre-empts the activities of units which Electroenceph. clin. Neurophysiol., 1972, 32:63--74
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I MSEC Fig. 1. Receptor and neural responses during masking of a pure tone. The top pictures in each row are CRO photographs (40 superimposed sweeps); the bottom pictures are computer-averaged responses (N = 500) in which the noise has been averaged out. M I K E : responses from a probe microphone near the eardrum. CM : cochlear microphonic responses from an electrode on the left round window. L C N : neural responses from a macro-electrode in left cochlear nucleus. Column T80 : responses to an 80 dB 1.5 kc/sec tone. Column T80 N80 : responses to same tone with the addition of noise (bandwidth 1.391.6t kc/sec) at 80 dB. Column T80 N100: same with noise intensity raised to 100 dB.
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would otherwise be part of the phase-locked neural population contributing to the grossly recorded FFR envelope. This hypothesis is consistent with the earlier conclusion of Derbyshire and Davis (1935) that the apparent reduction which they observed in the electrical response to clicks in the presence of noise was the result of these stimuli "competing" for use of the same fiber tracts, In order to explore this possibility further, a second experiment was performed with microelectrodes to study the activity patterns of single cells or small groups of cells within CN in response to pure tone stimuli and noise maskers,
by the hollow earbarsl calibrations were obtained in advance for all tone and noise stimuli using a B & K 1/4" condensor microphone coupled to the earbar by means of ala artificial ear. The electrode was advanced through the CN in small steps while tone bursts were presented to the ipsilateral ear. Whenever the tone bursts elicited unit activity, the electrode was fixed in place while the following were determined: (a) whether the unit showed phase-locked firing to any stimulus frequency ; (b) the frequency range for which phase-locking was most precise ; and (c) the minimal stimulus intensity at which phaselocked activity could be elicited. The frequency band for best phase-locking was selected while EXPERIMENTII observing the response on the CRO, or, in instances of ambiguity, by using on-line postMethods stimulus, time (PST) histograms produced by Both steeland tungstenmicro-electrodes were a CAT 400 B computer. In some cases, the use used. These were etched to tip diameters ranging of Polaroid photographs of several superimposed from 1 to 2 # and insulated with Epoxylite 6001 CRO sweeps served as a substitute for the latter M resin, method. The frequency at which the most precise Subjects were twenty acute cats. Each animal phase-locking occurred often, but not always, was anesthetized and mounted in a stereotaxic elicited the highest firing rate of the unit under instrument. Electrodes were introduced through observation. a burr hole in the skull. The electrode holder was Having determined the presence of phaseset at a posterior angle of 30° and the electrode locking and its best frequency, the following was advanced through cerebellum to dorsal CN stimulus conditions were presented : (a) a nonand, ultimately, to the antero-ventral portion of stimulus control condition to determine base CN. With sufficient experience, it was possible rates of spontaneous unit activity; (b) a toneto determine from the marked changes in the alone condition usingbursts of previously detercharacter of the unit activity recorded, the point mined frequency and intensity ; (c) a tone-plusat which the electrode tip passed from the floc- noise condition using the same tone burst mixed culus of the cerebellum into CN. Three or four with a noise burst of coincident onset and durapenetrations of each CN were made in a given tion. The noise intensity was first set equal to that experiment. Usually, the best recordings were of the tone. Two additional tone-plus-noise conobtained during initial penetrations, ditions were used in which all parameters remainSound stimuli were tone and noise bursts of ed the same as in condition (c) except for 10 and 20 msec duration with 5 msec rise and fall time. 20 dB increases in noise intensity. In each conTones were generated by an audio oscillator dition, a minimum of 100 stimuli were presented (H-P 200CD), and the frequencies ranged from at a rate of 2/sec. Where prolonged contact with 200 c/sec to 2 kc/sec, depending upon the re- a given unit permitted, conditions (a) and (b) sponse characteristics of the unit under examina- were repeated to determine the stability of the tion. Noise bursts were filtered to a bandwidth recording situation. Noise-alone control samples of one critical band, centered at the frequency were collected where it was suspected that sepaof the particular tone being used. Sound stimuli rate unit populations were responding to the two were delivered via TDH-39 earphones coupled classes of stimuli, or where it was doubtful to the hollow earbars of the stereotaxic instru- whether the unit under study could respond at ment. In order to compensate for acoustic all to the noise. Data from such units were exdistortion and tuning characteristics introduced cluded from the present analysis, as was data Electroenceph. clin. Neurophysiol., 1972, 32:63 74
RECEPTOR AND NEURAL RESPONSES IN MASKING
from units that demonstrated the "chopper" pattern (Pfeiffer 1966) characterized by fixedinterval asynchronous discharges regardless of the frequency of the stimulus or whether it was noise alone, A Transidyne MPA-5 pre-amplifier placed near the cat was used to amplify recorded activity. The electrode-amplifier combination yielded a frequency response from 0.001 to 2 kc/sec ( - 6 dB). All trigger pulses, stimuli and responses from CN were recorded on FM magnetic tape (Ampex FR-1300) for later analysis. Recorded data were later analyzed with the aid of a Schmitt trigger and a CAT 400 B cornputer. While the tape-recorded spike discharges and the Schmitt trigger output were monitored on an oscilloscope, the trigger threshold level was adjusted to fire only to the largest spikes within the range of the electrode and to ignore the smaller background activity. The Schmitt trigger output (a 1 V square wave of 100/asec duration) was led to the signal input of the CAT, the sweep of which was triggered by a synchronizing pulse from the magnetic tape. Since this pulse was phase-locked to the tone burst stimulus, successive stimuli were coherent, i.e., identical in phase at onset. This made it possible to compute PST histograms based on unit responses (transmuted to Schmitt trigger pulses) to 100 or more stimuli, Recordings with poor signal-to-noise ratios (i.e., multiple small spikes riding large FFR waves) presented a particular problem for analysis. Where the response to a low frequency stimulus was being studied (200-500 c/sec) it was possible to interpose a high-pass filter (1-10 kc/sec) between the tape output and the Schmitt trigger, In addition to improving the over-all signal-tonoise ratio, this procedure had the additional great advantage of filtering out the FFR wave which, when present, could result in a false impression of synchrony in unit discharges of nonphase-locking units if the Schmitt trigger were adjusted to accept only spikes that occurred at the apex of the F F R wave form. At higher stimulus frequencies, it was not possible to filter out the F F R wave form without significantly distorting the unit discharges. Such data were discarded. After the termination of recording, steel
67
micro-electrodes were reintroduced to the point of maximal previous penetration in each CN. A small current was passed through each tip, and the electrodes were withdrawn. The animal was then perfused via the internal carotid arteries with formalin in which potassium ferricyanide crystals had been dissolved to form a 1.0~ solution. The resulting Prussian blue reaction served to mark the locus of the electrode tip for subsequent histology.
Results Most but not all ofthe units encountered within CN could be excited by a tone burst stimulus. Among these, fewer than half of the units that could be held long enough for detailed study showed unequivocal phase-locked response patterns to tone burst stimuli at any frequency. Among non-phase-locking units were observed a variety of response patterns previously described by Pfeifffer (1966). These included "on" units, "pausers" and "choppers". Cells that were observed to fire in phase-locked fashion varied widely in precision of phase-locking. In some instances, firing was synchronous only during the first few cycles. Other units were observed which showed great precision of phase-locking every time they fired in response to the stimulus. The precision of phase-locking for any given unit varied with stimulus frequency. This is illustrated in Fig. 2. In this instance, the electrode tip appeared to be recording from several adjacent cells which responded to tone bursts across a frequency band from 200 to 2 kc/sec. Above this frequency, stimuli were inhibitory to the same cells. The upper trace of the photographs in columns B and D of Fig. 2 records the firing of a Schmitt trigger activated by only the largest spikes.As these traces show, synchrony increased across frequency to a band of maximal phaselocking precision between 500 and 1.2 kc/sec, deteriorating progressively above this range. Fig. 3 illustrates the activity of a cell in ventral CN which fired in tightly phase-locked fashion to an 81 dB tone burst. Fig. 3, A shows this to be an active unit with a moderate level of spontaneous activity, which responded to tone burst stimulation with a marked increase in firing rate. The precision of phase-locking is clearly apparent in B (20 superimposed sweeps). The recordElectroenceph. clin. Neurophysiol., 1972, 32:63 74
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Fig. 2. Multiple unit responses from left cochlear nucleus (LCN) evoked by tone bursts of increasing frequency. A and C : CRO photographs; single slow sweep. Upper trace is tone burst; lower is response at LCN. B and D: CRO photographs, 20 superimposed fast sweeps. Upper trace, responses of Schmitt trigger to largest unit spikes occurring to the tone burst ; lower trace, LCN response. The number above each pair of photographs is the frequency (in c/sec for A and B, in kc/sec for C and D) of the tone burst stimulus.
ings obtained with this particular electrode at this locus reflect both the activity of a single cell and, at the same time, the FFR wave form which is presumably a function of the activity of a population of cells. This instance is somewhat unusual in that the two phenomena were of opposite polarity. The wave form of FFR is most clearly apparent in C of Fig. 3, a case in which the unit failed to fire in response to the stimulus, Fig. 3, D illustrates (as does B) the relationship of unit activity to FFR. This unit, when it fired, always fired on the negative peak of the FFR wave. Fig. 4 illustrates the effects of the addition of noise to the tone burst stimulus on the activity of the unit shown in Fig. 3. The photographs and histogram in the top row document the precise phase-locking of this unit to an 885 c/sec tone burst. With the addition of noise at the same intensity of the tone, unit activity became desyn-
chronized and phase-locking to the tone burst was no longer evident. A second form of analysis of these data concerned the number of unit firings elicited during each of the two stimulus conditions. This count was made by summing the contents of each bin of the PST histogram stored in the CAT computer. The total number of spikes occurring during the 20 msec tone burst epoch was 1144 (summed across 130 stimuli). With the addition of noise, the total dropped to 753, a highly significant decrement (P= < 0.01). It is of interest that ifth~epoch of analysis was lengthened to include the 5 msec period immediately following the cessation of each stimulus burst, this result was reversed. The tone-alone spike count increased by 1002 to a total of 1755. This difference is reflected in the two photographs on the right in Fig. 4. The activity of this unit was inhibited in the period immediately following tone stimulation but enhanced in the postElectroenceph. clin. Neurophysiol., 1972, 32:63 -74
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Fig. 3. Responses of unit with best phase-locking response to 885 c/sec tone burst, A : Single sweep C R O photographs of unit response. U p p e r trace, 885 c/sec tone burst ; lower trace, responses of single cell recorded from antero-ventral CN. B : 20 superimposed sweeps ; upper trace : 81 dB, 885 c/sec, 20 msec tone burst ; lower trace : response of unit from C N showing both spikes and FFR. Note tight phase-locking of unit response. C : Single sweep, F F R response to 885 c/sec tone burst, a stimulus presentation to which no spikes occurred, note positive polarity of F F R waves. D: Single sweep, F F R and unit response to 885 c/sec tone burst. The C N unit fired twice to this stimulus, each time phase-locked to the negative peak of the F F R wave. The dots above the spikes are responses of the Schmitt trigger.
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Fig. 4. Responses of unit to tone burst and tone-noise burst. R o w T81 : unit responses to 20 msec, 81 dB tone burst at 885 c/sec. Row T81 + N81 : responses of same unit to combined stimulus ; tone plus noise, both 81 dB and 20 msec duration ; noise filtered to 1 critical band (810-1060 c/sec) centered on tone frequency. C R O : C R O photographs, single sweep (1 swp) and 20 superimposed sweeps (20 swps); upper trace in each photograph is Schmitt trigger response to C N ; lower trace is C N response to stimulus. PST : PST histograms of C N unit generated Schmitt trigger spikes to 130 stimuli ; vertical calibration represents 50 Schmitt trigger pulses. Each dot is one cycle (1.13 msec) of the sine wave tone burst.
Electroenceph. clin. Neurophysiol., 1972, 32:63 74
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Fig. 5. CN unit responses to 450 c/sec tone-noise stimulus with increasing noise intensity. Left column : CRO photographs of stimulus. Tone (T) and noise (N) intensities in dB are indicated above each photograph. Time calibration : 2 msec. Center column : CRO photographs (20 sweeps) of unit responses from CN to combined tone-noise stimulus. Upper trace in each photograph is Schmitt trigger response to CN spikes ; lower trace is CN response. Right column : PST histograms of CN unit generated Schmitt trigger spikes summed for 100 stimuli. Dots (at 2.22 msec intervals) indicate tones.
stimulus period, when noise was added to the same tone. Fig. 5 illustrates the behavior of units whose best phase-locking frequency (450 c/sec), whs considerably below that presented in the two previous figures. In this instance, the electrode appeared to be recording the activity of several adjacent units as judged from the several discrete spike sizes observed. Therefore the Schmitt trigger threshold was carefully adjusted while monitoring to fire only in response to the largest spikes. In this case a filter was utilized (1-10 kc/sec bandpass) in order to minimize FFR and
to improve the signal-to-noise ratio of spikes to background. It is evident that the firing pattern of the unit analyzed in this series was less affected by the addition of noise of increasing intensity than that shown in Fig. 4. Although the precision of phase-locking decreased markedly as a function of the increase in noise intensity, some synchrony was still apparent when the noise intensity exceeded the tone intensity by 20 dB. In this case the addition of noise at equal intensity did not significantly change the over-all spike count (796 as compared to 772). Fig. 6 (upper portion) illustrates the activity Electroenceph. clin. Neurophysiol., 1972, 32:63-74
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RECEPTOR AND NEURAL RESPONSES IN MASKING
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Fig. 6. Response of CN unit to tone and tone plus noise at two frequencics (500 and 700 c/sec). Tone (T) and noise (N) intensities in dB are indicated above each photograph. A and B : CRO photographs single sweep. Upper trace (CN) in each photograph is response of CN unit ; lower trace (S) is stimulus. C : PST histograms of unit activated Schmitt trigger pulses summed over 100 stimulus presentations. Upper half of figure : unit activity in response to 500 c/sec stimuli at 75 dB (top row) and (second row) in response to same tone with noise added (85 dB filtered to pass 445-555 c/sec). Lower half of figure : responses of the same unit to 700 c/sec tone at 87 dB (third row) and the same tone plus 93 dB noise filtered to pass 640-770 c/sec (bottom row).
of a unit which phase-locked well to a 75 dB, 500 c/sec tone pulse. The addition of noise at 85 dB produced a marked desynchrony. Here spike count increased with the addition of noise (from 508 to 782 for 100 stimulus presentations in each condition), presumably as a function of the 10 dB intensity increase represented in the combined tone-noise stimulus, The response of the same unit to a 700 c/sec tone burst at 87 dB is shown in the lower portion of Fig. 6. A comparison of the histograms in rows
1 and 3 makes it clear that synchrony was much less precise to the higher frequency, even though the intensity of the latter was set 12 dB higher. This partial synchrony to the 700 c/sec tone pulse was essentially eliminated by the addition of noise at 93 dB. Evident also in this illustration is the fact that over-all increase in stimulus intensity produced the often observed decrease in latency of unit firing as well as prolongation of the post-stimulus period of inhibition. Electroenceph. clin. Neurophysiol., 1972, 32:63-74
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J.T. MARSHet al.
The evidence presented here suggests that the addition to a tone burst of masking noise at progressively increasing intensities alters the firing patterns of units which fire in phase-locked fashion to the tone. This alteration is in the direction of decreased synchrony, or less precise phase-locking. In most of the instances observed in this study, an intensity difference of 20 to 30 dB between tone and noise is sufficient to desynchronize completely a unit that fires with precise phase-locking to tone alone. The phase-locking units encountered in this study differed in degree of sensitivity to the effects of noise. In some instances (Fig. 4), little or no synchrony was apparent in the presence of noise equal to the tone intensity. In others (Fig. 5), some degree of synchrony was present when noise intensity exceeded tone intensity by 20 dB.
sumed that unit activity is pre-empted by the noise so that the unit fires in response to some parameter of the noise rather than to a specific phase of the sinusoid. An additional possible mechanism suggested by our data is inhibition of synchronous units by the masker so that the total number of discharges of a given unit to 100 masked tone bursts is significantly reduced as compared to the total number of times it fires to 100 unmasked control tone bursts. The net effect of this inhibition across a population of similarly affected cells would be a reduction in the total number of discharges per unit time. Fig. 4 illustrates an instance in which both factors appear to be operating, i.e., the addition of the noise masker at the same intensity as the tone produced both desynchronization and a marked reduction in over-all firing rate. Although our data suggest that some CN units DISCUSSION are inhibited in the presence of noise, we have also observed instances in which the addition of Results presented in part I of this report in- noise at equal intensity to the tone burst either dicated that the addition of masking noise to tone increased or did not significantly alter the oversignificantly reduced the FFR to that tone .re- all firing rate. However, in all instances, regardcorded via gross electrodes in CN. We have less ofits effect on firing rate, the addition ofnoise suggested (Marsh and Worden 1968) that FFR produced desynchrony. is the envelope of phase-locked activity in a Obviously, these results do not bear on the population of units. Supporting this notion is masking of high frequency tones (roughly those recent evidence which indicates that phase-lock- above 5000 c/sec) beyond the upper limits of ing units are encountered in cochlear nucleus phase-locking and FFR. For frequencies in this (Moushegian and Rupert 1970), superior olivary range a "place" rather than "volley" principle is complex (Moushegian et al. 1964, 1967), lateral assumed as the basis of frequency information, lemniscus (Aitkin et al. 1970 ; Brugge et al. 1970) and masking as well as frequency discrimination and some portions of the inferior colliculus may involve different neural mechanisms. (Rose et al. 1966), the same centers from which we have recorded FFR (Worden and Marsh SUMMARY 1968). TO date, neither unit phase-locking nor FFR have unequivocally been observed at higher " Responses from cochlea and cochlear nucleus levels of the auditory pathway. In addition, the were recorded in cats through gross electrodes, upper frequency limits of F F R appear to be using stimulus conditions under which masking roughly comparable to those for phase-locking, effects were demonstrated with human subjects. Part II of this report presents evidence that a With successive intensity increments of the noise masking noise reduces the precision of phase- masker relative to the tone stimulus, the neural locking to a tone stimulus. This finding accords "frequency-following response" (FFR) showed a well with the masking-produced decrement in significantly greater diminution in amplitude FFR described in part I and supports the pos- than did the cochlear microphonic. Results sugsibility that at least one neural mechanism gested masking is mediated neurally in the underlying the masking of low frequency tones cochlear nucleus and is separable from interby noise is the desynchrony of phase-locking ference effects known to occur at the cochlea. units. With respect to this mechanism, it is as- In order to explore further the neural mechanisms Electroenceph. clin. Neurophysiol., 1972, 32:63 74
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RECEPTOR AND NEURAL RESPONSES IN MASKING
involved, experiments were performed to study the activity of single cells in the cochlear nucleus under the same stimulus conditions. Cells that fired in phase-locked fashion to the tone frequency showed progressive desynchronization with increasing intensity of the noise masker. These results support the hypothesis that the noise pre-empts the activities of units which would otherwise be part of the phase-locked neural population contributing to the grossly recorded F F R envelope and suggest at least one neural mechanism involved in the masking of low frequency t o n e s .
RESUME REPONSES RECEPTRICES ET NEURONIQUES DANS LE MASQUAGE AUDITIF DES TONS A BASSE FREQUENCE
Les r6ponses de la cochl6e et du noyau coch16aire sont enregistr6es chez le chat au moyen de grosses 61ectrodes, en utilisant des conditions de stimulation dans lesquelles des effets de masquage existeraient chez l'homme. En augmentant les intensit6s successives du masquage du bruit par rapport au stimulus auditif, la
r6ponse neuronique en fr6quence (FFR) m o n t r e diminution significativement plus grande que ne le fait la r6ponse microphonique cochl6aire, une
Ces r6sultats sugg6rent que le masquage est transmis de faqon neuronique dans le noyau cochl6aire et peut &re s6par6 des effets d'interf6rence connus au niveau de la cochl6e. Afin d'aller plus loin dans l'exploration des m6canismes nerveux impliqu6s, des exp6riences ont 6t6 imagin6es pour 6tudier l'activit6 de cellules isol6es du noyau cochl6aire dans ,les m~mes conditions de stimulation. Les cellules qui d6chargent en relation de phase avec la fr6quence du bruit montrent une d6synchronisation progressive avec l'intensit6 progressive d u mRsquage du bruit. Ces r6sultats confirment l'hypoth6se suivant laquelle le bruit prend le pas sur les activit6s des unit6s cellulaires qui feraient autrement partie de la population nerveuse en liaison de phase contribuant/l l'enveloppe de la FUR enregistr6e avec des macro-61ectrodes, e t sugg6rent qu'un m6canisme nerveux au moins est impliqu6 dans le masquage des sons/t basse fr6quence.
We are pleased to acknowledge the technical assistance of Mr. James L. Martin III, Mr. Roger Barnes and Mr. Claude Finn, and the assistance of Mrs. S. Crozier in the preparation of the manuscript.
REFERENCES
AITKIN,L. M., ANDERSON,D. J. and BRUGGE,J. F. Tonotopic organization and discharge characteristics of single neurons in nuclei of the lateral lemniscus of the cat. J. Neurophysiol., 1970, 33:421-440. BRUGGE,J. F., ANDERSON,D. J. and AITKIN, L. M. Responses of neurons in the dorsal nucleus of the lateral lemniscus of cat to binaural tonal stimulation. J. Neurophysiol., 1970, 33: 441-458. COVELL,W. P. and BLACK,L. J. The cochlear response as an index to hearing. Amer. J. Physiol., 1936, 116: 524-530. DERBYSHIRE,A. J. and DAVlS,H. The action potentials of the auditory nerve. Amer. J. Physiol., 1935, 113:476 504. ENGEBRETSON, A. M. and ELDREDGE, D. H. Model for the nonlinear characteristics of cochlear potentials. J. acoust. Soc. Amer., 1968, 44: 548-554.
JEFFREss,L.A. Masking. InJ. V. ToBIAs(Ed.),Foundationst~f modern auditory theory. Vol. I. Academic Press, New York, 1970: 85-114. LICKLIDER,J. C. R. Basic correlates of the auditory stimulus. InS. S. STEVENS(Ed.), Handbook ofexperimentalpsychology. Wiley and Sons, New York. 1951: 985-1039. MARSH,J. T. and WORDEN, F. G. Sound evoked frequencyfollowing responses in the central auditory pathway. Laryngoscope (St Louis), 1968, 78:1149 1163. MARSH,J. T. and WORDEN,F. G. Some factors modulating neural activities in peripheral auditory centers. Brain Res., 1969, 12: 99-111. MARSH,J. Z., WORDEN,F. G. and SMITH,J. C. Auditory frequency-following response: neural or artifact? Science, 1970, 169: 1222-1223. MOUSHEGIAN,G. and RUPERT, A. L. Response diversity of neurons in ventral cochlear nucleus of kangaroo rat to low frequency tones. J. Neurophysiol., 1970,33: 351-364. MOUSHE6IAN,G., RUPERT, A. L. and LANGEORD, T. L. Stimulus coding by medial superior olivary neurons. J. Neurophysiol., 1967, 30: 1239-1261. MOUSHEGIAN,G., RUPERT, A. L. and WHITCOMB, M. A. Brain-stem neuronal response patterns to monaural
andbinauraltones. J. Neurophysiol.,1964,27:l174-1191.
PFEIFFER,R. R. Classification of response patterns of spike discharges for units in the cochlear nucleus: tone burst stimulation. Exp. Brain Res., 1966, 1 : 220-235. ROSE,J. E., GROSS,N. B., GEISLER,C. D. and HIND, J. E. Some neural mechanisms in the inferior colliculus of the cat which may be related to the localization of a sound source. J. Neurophysiol., 1966, 29: 288-314. WARD, W. D. Auditory fatigue and masking. In J. JERGER (Ed.), Modern developmentsin audiology. Academic Press, New York, 1963: 241-284.
Electroenceph. clin. Neurophysiol., 1972, 32:63 74
74 WEVER, E. G., BRAY, C. W. and LAWRENCE, M. The interference of tones in the cochlea. J. acoust. Soc. Amer., 1940, 12: 268-280.
J.T. MARSH e t al. WORDEN, F. G. and MARSH, J. T. Frequency-following (microphonic-like) neural responses evoked by sound. Electroenceph. clin. Neurophysiol., 1968, d.~5:42-52.
R~{l~'rence : MARStt,J. T.. SMITH,J. C. and WORDEN,F. G. Receptor and neural responses in auditory masking of low frequency tones. Electroenceph. clin. Neurophysiol., 1972, 32: 63-74.
63
RECEPTOR AND NEURAL RESPONSES IN AUDITORY MASKING OF LOW FREQUENCY TONES J. T. MARSH, J. C. SMITH AND F. G. WORDEN1 Department of Psychiatry and Brain Research Institute, University of California, Los Angeles, Calif 90024 and Neurosciences Research Program, 280 Newton Street, Brookline, Mass. 02146 (U.S.A.) (Accepted for publication: July 14, 1971)
The threshold for theperceptionofapure tone is elevated in the presence of noise presented at the same ear. This perceptual phenomenon, known as monaural masking, has been studied extensively (Licklider 1951 ; Ward 1963 ; Jeffress 1970), but the mechanisms underlying it are not completely understood. To explore these mechanisms, electrophysiological data were recorded from the round window of the cochlea, and the first brain relay (cochlear nucleus) of cat. In order to establish that the stimulus conditions used for the cat qualified in terms of the known psychophysics pertaining to masking, the stimuli were first tested on human subjects,
the subjects who were tested using a 20 dB increase in noise level, threshold elevation averaged 21.2+3.9 dB. This one-to-one relationship of increase in masker intensity to increase in tone detection threshold has been widely reported in the psychophysical literature. Similar stimulus conditions were then presented to cats, using the same earphone fitted with an aural cannula containing a probe microphone (B & K, Model 4133) to monitor sound pressure levels near the ear drum. Ten cats with electrodes chronically implanted on the round window (to record the cochlear microphonic response), and in the cochlear nucleus (CN), were used. With the subjects anesthetized EXPERIMENT I (sodium pentobarbital, 35 mg/kg, intraperitoneal), electrophysiological responses were amMethods plified, monitored on an oscilloscope and recordFor each ear of five human subjects, detection ed on FM magnetic tape for subsequent analogthresholds for a 1.5 kc/sec tone were determined to-digital conversion and response averaging in the presence ofnarrow-band filtered noise, one (IBM 360-91). Results reported elsewhere critical band in width (1.39-1.61 kc/sec), at two (Worden and Marsh 1968) suggest that anlevels of sound pressure, 70 dB and 80 dB (re esthesia is not a significant complicating variable 0.0002 microbar). Subjects sat in a sound-at- for responses at this level of the auditory system. tenuated room (Industrial Acoustics Corp., The electrodes, recording procedures and equipModel 400), wearing a calibrated earphone ment have been described previously (Marsh and (Grason-Stadler TDH-39), and were presented Worden 1968; Worden and Marsh 1968). with a counterbalanced order of noise condiThe auditory frequency-following response tions ; an ascending order of tone intensities was (FFR) served as the measure of tone-evoked used to determine threshold. For this 10 dB activity in CN. The FFR, as previously reported increase in noise level, the increase in tone detec- (Marsh and Worden 1968, 1969 ; Worden and tion threshold averaged 10.8 + 1.7 dB. In two of Marsh 1968), is a microphonic-like wave form 1 Supported by U.S. Public Health Service Grant MH observed in the auditory pathway which shows 03831-11. Computing assistance was obtained from the varying amounts of harmonic distortion but Health Sciences Computing Facility, U.C.L.A., sponsored always a fundamental frequency equal to that of by N.I.H. Grant RR-3. the stimulus. FFR has a latency or phase shift Electroenceph. clin. Neurophysiol., 1972, 32:63 74
64 appropriate to the level from which it is recorded and is observed to change in amplitude as a function of stimulus intensity. Previous experiments have demonstrated that the F F R is a neural response rather than artifact, or a remote pickup of the cochlear microphonic (CM), which it resembles. The F F R is recordable only within the auditory pathway at and below the level of the inferior colliculus and is distinct from the CM in the following respects : (1) the frequency band over which F F R can be recorded is much narrower than the CM bandwidth; (2) FFR disappears concurrently with other neural activity during asphyxia while CM remains for some time; (3) F F R is totally abolished at and above CN after cutting the eighth nerve or during cooling with a cryoprobe in CN, while, concurrently, CM remains undiminished. In the latter experiment, as CN is allowed to return to normal temperature, F F R reappears and attains its pre-cooling amplitude (Marsh et al. 1970). The effect of noise on tone-evoked FFR was explored in" two ways: Ca) observation of responses displayed on an oscilloscope (CRO) with sweep phase-locked to the tone stimulus; and (b) measurement of the amplitude of the sine wave recovered from the noise background by response averaging (N = 500) with sweep timelocked to the tone stimulus so as to average out the noise. Results Both CRO displays and averaged responses are illustrated in Fig. 1. In the CRO photographs, it can be seen that an 80 dB tone (MIKE, column 1) evokes a sinusoidal pattern in both receptor (CM) and neural responses (LCN). With the addition of noise (column 2), this pattern becomes less distinct, and with a 20 dB increase in noise intensity (column 3), it is completely obscured. It can also be seen in the CRO photographs that noise exerts a differential effect on the amplitude of the response envelope, which increases for CM but not LCN. In this regard, the CM response resembles that of the monitor microphone ( M I K E ) more than does the LCN response, Response averaging (bottom photographs in each row of Fig. 1) demonstrates a further effect of noise on tone-evoked responses. For both the
J.T. MARSHet al. receptor and neural responses, the addition of noise results in a diminution of the averaged sine wave (column 2), and this effect is enhanced by increasing the noise intensity (column 3). As can be seen from the averaged responses, the decrement appears greater in the neural than in the receptor responses. For a 20 dB increase in masker intensity, the mean decrement in averaged response amplitude was49.6~o or approximately 6 dB for CM and 60.4~ or approximately 8 dB for CN. This decrement in neural response is significantly greater than that in the receptor response (P< 0.001). The 6 dB decrement in CM resulting from a 20 dB increase in noise amplitude may be attributed to the interference effect (Covell and Black 1936 ; Wever et al. 1940), and resembles data obtained by Engebretson andEldredge (1968) using interference tones applied to guinea pig cochlea. We have since cornpared their interfering tone stimuli to our filtered noise bursts with regard to interference efficacy and have found the two classes of stimuli to be roughly equivalent psychophysiologically (within +0.5 dBofattenuationatRWofacontinuous 700 c/sec test tone). Our observation, that the reduction in F F R resulting from a 20 dB increase in masker was nearly always significantly greater than the corresponding reduction in CM, suggests that the interference effect discussed by Wever et al. (1940), and the subsequent cochlear non-linearity modeled by Engebretson and Eldredge (1968) do not fully account for the "masking" effect observed at CN following the addition of noise to tone. A parallel can be seen between the masking effect of noise in raising tone detection thresholds and its blurring and amplitude-reducing effects on tone-evoked electrophysiological responses. If the decrements in electrophysiological responses reported here are indeed correlates of psychophysical masking phenomena, then the greater reduction at CN suggests that there is an important neural as well as receptor component in masking. This is consistent with the interpretation ofWever et al. (1940). We have suggested that FFR is the envelope of unit discharges that are phase-locked to the tone stimulus. The large decrement in averaged FFR amplitude with the addition of noise suggests the possibility that the noise pre-empts the activities of units which Electroenceph. clin. Neurophysiol., 1972, 32:63--74
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I MSEC Fig. 1. Receptor and neural responses during masking of a pure tone. The top pictures in each row are CRO photographs (40 superimposed sweeps); the bottom pictures are computer-averaged responses (N = 500) in which the noise has been averaged out. M I K E : responses from a probe microphone near the eardrum. CM : cochlear microphonic responses from an electrode on the left round window. L C N : neural responses from a macro-electrode in left cochlear nucleus. Column T80 : responses to an 80 dB 1.5 kc/sec tone. Column T80 N80 : responses to same tone with the addition of noise (bandwidth 1.391.6t kc/sec) at 80 dB. Column T80 N100: same with noise intensity raised to 100 dB.
66
J.T. MARSHel al.
would otherwise be part of the phase-locked neural population contributing to the grossly recorded FFR envelope. This hypothesis is consistent with the earlier conclusion of Derbyshire and Davis (1935) that the apparent reduction which they observed in the electrical response to clicks in the presence of noise was the result of these stimuli "competing" for use of the same fiber tracts, In order to explore this possibility further, a second experiment was performed with microelectrodes to study the activity patterns of single cells or small groups of cells within CN in response to pure tone stimuli and noise maskers,
by the hollow earbarsl calibrations were obtained in advance for all tone and noise stimuli using a B & K 1/4" condensor microphone coupled to the earbar by means of ala artificial ear. The electrode was advanced through the CN in small steps while tone bursts were presented to the ipsilateral ear. Whenever the tone bursts elicited unit activity, the electrode was fixed in place while the following were determined: (a) whether the unit showed phase-locked firing to any stimulus frequency ; (b) the frequency range for which phase-locking was most precise ; and (c) the minimal stimulus intensity at which phaselocked activity could be elicited. The frequency band for best phase-locking was selected while EXPERIMENTII observing the response on the CRO, or, in instances of ambiguity, by using on-line postMethods stimulus, time (PST) histograms produced by Both steeland tungstenmicro-electrodes were a CAT 400 B computer. In some cases, the use used. These were etched to tip diameters ranging of Polaroid photographs of several superimposed from 1 to 2 # and insulated with Epoxylite 6001 CRO sweeps served as a substitute for the latter M resin, method. The frequency at which the most precise Subjects were twenty acute cats. Each animal phase-locking occurred often, but not always, was anesthetized and mounted in a stereotaxic elicited the highest firing rate of the unit under instrument. Electrodes were introduced through observation. a burr hole in the skull. The electrode holder was Having determined the presence of phaseset at a posterior angle of 30° and the electrode locking and its best frequency, the following was advanced through cerebellum to dorsal CN stimulus conditions were presented : (a) a nonand, ultimately, to the antero-ventral portion of stimulus control condition to determine base CN. With sufficient experience, it was possible rates of spontaneous unit activity; (b) a toneto determine from the marked changes in the alone condition usingbursts of previously detercharacter of the unit activity recorded, the point mined frequency and intensity ; (c) a tone-plusat which the electrode tip passed from the floc- noise condition using the same tone burst mixed culus of the cerebellum into CN. Three or four with a noise burst of coincident onset and durapenetrations of each CN were made in a given tion. The noise intensity was first set equal to that experiment. Usually, the best recordings were of the tone. Two additional tone-plus-noise conobtained during initial penetrations, ditions were used in which all parameters remainSound stimuli were tone and noise bursts of ed the same as in condition (c) except for 10 and 20 msec duration with 5 msec rise and fall time. 20 dB increases in noise intensity. In each conTones were generated by an audio oscillator dition, a minimum of 100 stimuli were presented (H-P 200CD), and the frequencies ranged from at a rate of 2/sec. Where prolonged contact with 200 c/sec to 2 kc/sec, depending upon the re- a given unit permitted, conditions (a) and (b) sponse characteristics of the unit under examina- were repeated to determine the stability of the tion. Noise bursts were filtered to a bandwidth recording situation. Noise-alone control samples of one critical band, centered at the frequency were collected where it was suspected that sepaof the particular tone being used. Sound stimuli rate unit populations were responding to the two were delivered via TDH-39 earphones coupled classes of stimuli, or where it was doubtful to the hollow earbars of the stereotaxic instru- whether the unit under study could respond at ment. In order to compensate for acoustic all to the noise. Data from such units were exdistortion and tuning characteristics introduced cluded from the present analysis, as was data Electroenceph. clin. Neurophysiol., 1972, 32:63 74
RECEPTOR AND NEURAL RESPONSES IN MASKING
from units that demonstrated the "chopper" pattern (Pfeiffer 1966) characterized by fixedinterval asynchronous discharges regardless of the frequency of the stimulus or whether it was noise alone, A Transidyne MPA-5 pre-amplifier placed near the cat was used to amplify recorded activity. The electrode-amplifier combination yielded a frequency response from 0.001 to 2 kc/sec ( - 6 dB). All trigger pulses, stimuli and responses from CN were recorded on FM magnetic tape (Ampex FR-1300) for later analysis. Recorded data were later analyzed with the aid of a Schmitt trigger and a CAT 400 B cornputer. While the tape-recorded spike discharges and the Schmitt trigger output were monitored on an oscilloscope, the trigger threshold level was adjusted to fire only to the largest spikes within the range of the electrode and to ignore the smaller background activity. The Schmitt trigger output (a 1 V square wave of 100/asec duration) was led to the signal input of the CAT, the sweep of which was triggered by a synchronizing pulse from the magnetic tape. Since this pulse was phase-locked to the tone burst stimulus, successive stimuli were coherent, i.e., identical in phase at onset. This made it possible to compute PST histograms based on unit responses (transmuted to Schmitt trigger pulses) to 100 or more stimuli, Recordings with poor signal-to-noise ratios (i.e., multiple small spikes riding large FFR waves) presented a particular problem for analysis. Where the response to a low frequency stimulus was being studied (200-500 c/sec) it was possible to interpose a high-pass filter (1-10 kc/sec) between the tape output and the Schmitt trigger, In addition to improving the over-all signal-tonoise ratio, this procedure had the additional great advantage of filtering out the FFR wave which, when present, could result in a false impression of synchrony in unit discharges of nonphase-locking units if the Schmitt trigger were adjusted to accept only spikes that occurred at the apex of the F F R wave form. At higher stimulus frequencies, it was not possible to filter out the F F R wave form without significantly distorting the unit discharges. Such data were discarded. After the termination of recording, steel
67
micro-electrodes were reintroduced to the point of maximal previous penetration in each CN. A small current was passed through each tip, and the electrodes were withdrawn. The animal was then perfused via the internal carotid arteries with formalin in which potassium ferricyanide crystals had been dissolved to form a 1.0~ solution. The resulting Prussian blue reaction served to mark the locus of the electrode tip for subsequent histology.
Results Most but not all ofthe units encountered within CN could be excited by a tone burst stimulus. Among these, fewer than half of the units that could be held long enough for detailed study showed unequivocal phase-locked response patterns to tone burst stimuli at any frequency. Among non-phase-locking units were observed a variety of response patterns previously described by Pfeifffer (1966). These included "on" units, "pausers" and "choppers". Cells that were observed to fire in phase-locked fashion varied widely in precision of phase-locking. In some instances, firing was synchronous only during the first few cycles. Other units were observed which showed great precision of phase-locking every time they fired in response to the stimulus. The precision of phase-locking for any given unit varied with stimulus frequency. This is illustrated in Fig. 2. In this instance, the electrode tip appeared to be recording from several adjacent cells which responded to tone bursts across a frequency band from 200 to 2 kc/sec. Above this frequency, stimuli were inhibitory to the same cells. The upper trace of the photographs in columns B and D of Fig. 2 records the firing of a Schmitt trigger activated by only the largest spikes.As these traces show, synchrony increased across frequency to a band of maximal phaselocking precision between 500 and 1.2 kc/sec, deteriorating progressively above this range. Fig. 3 illustrates the activity of a cell in ventral CN which fired in tightly phase-locked fashion to an 81 dB tone burst. Fig. 3, A shows this to be an active unit with a moderate level of spontaneous activity, which responded to tone burst stimulation with a marked increase in firing rate. The precision of phase-locking is clearly apparent in B (20 superimposed sweeps). The recordElectroenceph. clin. Neurophysiol., 1972, 32:63 74
68
J.T. MARSHet al. A
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Fig. 2. Multiple unit responses from left cochlear nucleus (LCN) evoked by tone bursts of increasing frequency. A and C : CRO photographs; single slow sweep. Upper trace is tone burst; lower is response at LCN. B and D: CRO photographs, 20 superimposed fast sweeps. Upper trace, responses of Schmitt trigger to largest unit spikes occurring to the tone burst ; lower trace, LCN response. The number above each pair of photographs is the frequency (in c/sec for A and B, in kc/sec for C and D) of the tone burst stimulus.
ings obtained with this particular electrode at this locus reflect both the activity of a single cell and, at the same time, the FFR wave form which is presumably a function of the activity of a population of cells. This instance is somewhat unusual in that the two phenomena were of opposite polarity. The wave form of FFR is most clearly apparent in C of Fig. 3, a case in which the unit failed to fire in response to the stimulus, Fig. 3, D illustrates (as does B) the relationship of unit activity to FFR. This unit, when it fired, always fired on the negative peak of the FFR wave. Fig. 4 illustrates the effects of the addition of noise to the tone burst stimulus on the activity of the unit shown in Fig. 3. The photographs and histogram in the top row document the precise phase-locking of this unit to an 885 c/sec tone burst. With the addition of noise at the same intensity of the tone, unit activity became desyn-
chronized and phase-locking to the tone burst was no longer evident. A second form of analysis of these data concerned the number of unit firings elicited during each of the two stimulus conditions. This count was made by summing the contents of each bin of the PST histogram stored in the CAT computer. The total number of spikes occurring during the 20 msec tone burst epoch was 1144 (summed across 130 stimuli). With the addition of noise, the total dropped to 753, a highly significant decrement (P= < 0.01). It is of interest that ifth~epoch of analysis was lengthened to include the 5 msec period immediately following the cessation of each stimulus burst, this result was reversed. The tone-alone spike count increased by 1002 to a total of 1755. This difference is reflected in the two photographs on the right in Fig. 4. The activity of this unit was inhibited in the period immediately following tone stimulation but enhanced in the postElectroenceph. clin. Neurophysiol., 1972, 32:63 -74
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Fig. 3. Responses of unit with best phase-locking response to 885 c/sec tone burst, A : Single sweep C R O photographs of unit response. U p p e r trace, 885 c/sec tone burst ; lower trace, responses of single cell recorded from antero-ventral CN. B : 20 superimposed sweeps ; upper trace : 81 dB, 885 c/sec, 20 msec tone burst ; lower trace : response of unit from C N showing both spikes and FFR. Note tight phase-locking of unit response. C : Single sweep, F F R response to 885 c/sec tone burst, a stimulus presentation to which no spikes occurred, note positive polarity of F F R waves. D: Single sweep, F F R and unit response to 885 c/sec tone burst. The C N unit fired twice to this stimulus, each time phase-locked to the negative peak of the F F R wave. The dots above the spikes are responses of the Schmitt trigger.
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Fig. 4. Responses of unit to tone burst and tone-noise burst. R o w T81 : unit responses to 20 msec, 81 dB tone burst at 885 c/sec. Row T81 + N81 : responses of same unit to combined stimulus ; tone plus noise, both 81 dB and 20 msec duration ; noise filtered to 1 critical band (810-1060 c/sec) centered on tone frequency. C R O : C R O photographs, single sweep (1 swp) and 20 superimposed sweeps (20 swps); upper trace in each photograph is Schmitt trigger response to C N ; lower trace is C N response to stimulus. PST : PST histograms of C N unit generated Schmitt trigger spikes to 130 stimuli ; vertical calibration represents 50 Schmitt trigger pulses. Each dot is one cycle (1.13 msec) of the sine wave tone burst.
Electroenceph. clin. Neurophysiol., 1972, 32:63 74
70
J.T. MARSHet al.
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Fig. 5. CN unit responses to 450 c/sec tone-noise stimulus with increasing noise intensity. Left column : CRO photographs of stimulus. Tone (T) and noise (N) intensities in dB are indicated above each photograph. Time calibration : 2 msec. Center column : CRO photographs (20 sweeps) of unit responses from CN to combined tone-noise stimulus. Upper trace in each photograph is Schmitt trigger response to CN spikes ; lower trace is CN response. Right column : PST histograms of CN unit generated Schmitt trigger spikes summed for 100 stimuli. Dots (at 2.22 msec intervals) indicate tones.
stimulus period, when noise was added to the same tone. Fig. 5 illustrates the behavior of units whose best phase-locking frequency (450 c/sec), whs considerably below that presented in the two previous figures. In this instance, the electrode appeared to be recording the activity of several adjacent units as judged from the several discrete spike sizes observed. Therefore the Schmitt trigger threshold was carefully adjusted while monitoring to fire only in response to the largest spikes. In this case a filter was utilized (1-10 kc/sec bandpass) in order to minimize FFR and
to improve the signal-to-noise ratio of spikes to background. It is evident that the firing pattern of the unit analyzed in this series was less affected by the addition of noise of increasing intensity than that shown in Fig. 4. Although the precision of phase-locking decreased markedly as a function of the increase in noise intensity, some synchrony was still apparent when the noise intensity exceeded the tone intensity by 20 dB. In this case the addition of noise at equal intensity did not significantly change the over-all spike count (796 as compared to 772). Fig. 6 (upper portion) illustrates the activity Electroenceph. clin. Neurophysiol., 1972, 32:63-74
71
RECEPTOR AND NEURAL RESPONSES IN MASKING
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Fig. 6. Response of CN unit to tone and tone plus noise at two frequencics (500 and 700 c/sec). Tone (T) and noise (N) intensities in dB are indicated above each photograph. A and B : CRO photographs single sweep. Upper trace (CN) in each photograph is response of CN unit ; lower trace (S) is stimulus. C : PST histograms of unit activated Schmitt trigger pulses summed over 100 stimulus presentations. Upper half of figure : unit activity in response to 500 c/sec stimuli at 75 dB (top row) and (second row) in response to same tone with noise added (85 dB filtered to pass 445-555 c/sec). Lower half of figure : responses of the same unit to 700 c/sec tone at 87 dB (third row) and the same tone plus 93 dB noise filtered to pass 640-770 c/sec (bottom row).
of a unit which phase-locked well to a 75 dB, 500 c/sec tone pulse. The addition of noise at 85 dB produced a marked desynchrony. Here spike count increased with the addition of noise (from 508 to 782 for 100 stimulus presentations in each condition), presumably as a function of the 10 dB intensity increase represented in the combined tone-noise stimulus, The response of the same unit to a 700 c/sec tone burst at 87 dB is shown in the lower portion of Fig. 6. A comparison of the histograms in rows
1 and 3 makes it clear that synchrony was much less precise to the higher frequency, even though the intensity of the latter was set 12 dB higher. This partial synchrony to the 700 c/sec tone pulse was essentially eliminated by the addition of noise at 93 dB. Evident also in this illustration is the fact that over-all increase in stimulus intensity produced the often observed decrease in latency of unit firing as well as prolongation of the post-stimulus period of inhibition. Electroenceph. clin. Neurophysiol., 1972, 32:63-74
n-50
72
J.T. MARSHet al.
The evidence presented here suggests that the addition to a tone burst of masking noise at progressively increasing intensities alters the firing patterns of units which fire in phase-locked fashion to the tone. This alteration is in the direction of decreased synchrony, or less precise phase-locking. In most of the instances observed in this study, an intensity difference of 20 to 30 dB between tone and noise is sufficient to desynchronize completely a unit that fires with precise phase-locking to tone alone. The phase-locking units encountered in this study differed in degree of sensitivity to the effects of noise. In some instances (Fig. 4), little or no synchrony was apparent in the presence of noise equal to the tone intensity. In others (Fig. 5), some degree of synchrony was present when noise intensity exceeded tone intensity by 20 dB.
sumed that unit activity is pre-empted by the noise so that the unit fires in response to some parameter of the noise rather than to a specific phase of the sinusoid. An additional possible mechanism suggested by our data is inhibition of synchronous units by the masker so that the total number of discharges of a given unit to 100 masked tone bursts is significantly reduced as compared to the total number of times it fires to 100 unmasked control tone bursts. The net effect of this inhibition across a population of similarly affected cells would be a reduction in the total number of discharges per unit time. Fig. 4 illustrates an instance in which both factors appear to be operating, i.e., the addition of the noise masker at the same intensity as the tone produced both desynchronization and a marked reduction in over-all firing rate. Although our data suggest that some CN units DISCUSSION are inhibited in the presence of noise, we have also observed instances in which the addition of Results presented in part I of this report in- noise at equal intensity to the tone burst either dicated that the addition of masking noise to tone increased or did not significantly alter the oversignificantly reduced the FFR to that tone .re- all firing rate. However, in all instances, regardcorded via gross electrodes in CN. We have less ofits effect on firing rate, the addition ofnoise suggested (Marsh and Worden 1968) that FFR produced desynchrony. is the envelope of phase-locked activity in a Obviously, these results do not bear on the population of units. Supporting this notion is masking of high frequency tones (roughly those recent evidence which indicates that phase-lock- above 5000 c/sec) beyond the upper limits of ing units are encountered in cochlear nucleus phase-locking and FFR. For frequencies in this (Moushegian and Rupert 1970), superior olivary range a "place" rather than "volley" principle is complex (Moushegian et al. 1964, 1967), lateral assumed as the basis of frequency information, lemniscus (Aitkin et al. 1970 ; Brugge et al. 1970) and masking as well as frequency discrimination and some portions of the inferior colliculus may involve different neural mechanisms. (Rose et al. 1966), the same centers from which we have recorded FFR (Worden and Marsh SUMMARY 1968). TO date, neither unit phase-locking nor FFR have unequivocally been observed at higher " Responses from cochlea and cochlear nucleus levels of the auditory pathway. In addition, the were recorded in cats through gross electrodes, upper frequency limits of F F R appear to be using stimulus conditions under which masking roughly comparable to those for phase-locking, effects were demonstrated with human subjects. Part II of this report presents evidence that a With successive intensity increments of the noise masking noise reduces the precision of phase- masker relative to the tone stimulus, the neural locking to a tone stimulus. This finding accords "frequency-following response" (FFR) showed a well with the masking-produced decrement in significantly greater diminution in amplitude FFR described in part I and supports the pos- than did the cochlear microphonic. Results sugsibility that at least one neural mechanism gested masking is mediated neurally in the underlying the masking of low frequency tones cochlear nucleus and is separable from interby noise is the desynchrony of phase-locking ference effects known to occur at the cochlea. units. With respect to this mechanism, it is as- In order to explore further the neural mechanisms Electroenceph. clin. Neurophysiol., 1972, 32:63 74
73
RECEPTOR AND NEURAL RESPONSES IN MASKING
involved, experiments were performed to study the activity of single cells in the cochlear nucleus under the same stimulus conditions. Cells that fired in phase-locked fashion to the tone frequency showed progressive desynchronization with increasing intensity of the noise masker. These results support the hypothesis that the noise pre-empts the activities of units which would otherwise be part of the phase-locked neural population contributing to the grossly recorded F F R envelope and suggest at least one neural mechanism involved in the masking of low frequency t o n e s .
RESUME REPONSES RECEPTRICES ET NEURONIQUES DANS LE MASQUAGE AUDITIF DES TONS A BASSE FREQUENCE
Les r6ponses de la cochl6e et du noyau coch16aire sont enregistr6es chez le chat au moyen de grosses 61ectrodes, en utilisant des conditions de stimulation dans lesquelles des effets de masquage existeraient chez l'homme. En augmentant les intensit6s successives du masquage du bruit par rapport au stimulus auditif, la
r6ponse neuronique en fr6quence (FFR) m o n t r e diminution significativement plus grande que ne le fait la r6ponse microphonique cochl6aire, une
Ces r6sultats sugg6rent que le masquage est transmis de faqon neuronique dans le noyau cochl6aire et peut &re s6par6 des effets d'interf6rence connus au niveau de la cochl6e. Afin d'aller plus loin dans l'exploration des m6canismes nerveux impliqu6s, des exp6riences ont 6t6 imagin6es pour 6tudier l'activit6 de cellules isol6es du noyau cochl6aire dans ,les m~mes conditions de stimulation. Les cellules qui d6chargent en relation de phase avec la fr6quence du bruit montrent une d6synchronisation progressive avec l'intensit6 progressive d u mRsquage du bruit. Ces r6sultats confirment l'hypoth6se suivant laquelle le bruit prend le pas sur les activit6s des unit6s cellulaires qui feraient autrement partie de la population nerveuse en liaison de phase contribuant/l l'enveloppe de la FUR enregistr6e avec des macro-61ectrodes, e t sugg6rent qu'un m6canisme nerveux au moins est impliqu6 dans le masquage des sons/t basse fr6quence.
We are pleased to acknowledge the technical assistance of Mr. James L. Martin III, Mr. Roger Barnes and Mr. Claude Finn, and the assistance of Mrs. S. Crozier in the preparation of the manuscript.
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R~{l~'rence : MARStt,J. T.. SMITH,J. C. and WORDEN,F. G. Receptor and neural responses in auditory masking of low frequency tones. Electroenceph. clin. Neurophysiol., 1972, 32: 63-74.