Psychiatry Research 113 (2002) 115–125
Auditory masking experiments in schizophrenia ¨ ´ ¨ ´ Olle Olsson* Johan Kallstrand, Peter Montnemery, Soren Nielzen, Clinical Psychoacoustic Laboratory, Division of Psychiatry, Department of Clinical Neuroscience, University Hospital, SE-221 85 Lund, Sweden Received 5 June 2001; received in revised form 11 November 2001; accepted 2 June 2002
Abstract Twelve schizophrenic subjects with acoustic hallucinations in their case histories were compared with 12 healthy reference subjects and eight subjects with panic disorder in a test of three auditory masking tasks, simultaneous masking (SM), forward masking (FM) and backward masking (BM). The schizophrenic subjects showed no differences from reference subjects on SM but had higher thresholds for the two other conditions (FM and BM). Schizophrenics with very increased thresholds (ns6) had a significantly higher need for residential treatment. Thresholds for SM and BM were not, as for reference subjects, related to age for schizophrenics. No statistically significant differences regarding any masking experiments were found between the panic disorder subjects and the reference subjects. Simultaneous masking, reflecting functions of the basilar membrane and those of elementary brainstem processing, showed no signs of dysfunction in schizophrenic subjects. Schizophrenics showed aberrations in FM and BM, possibly influenced by more central (cortical) processes. 䊚 2002 Elsevier Science Ireland Ltd. All rights reserved. Keywords: Schizophrenia; Simultaneous masking; Forward masking; Backward masking; Psychoacoustics
1. Introduction 1.1. The schizophrenic context A great variety of symptoms characterize schizophrenia illness. They emanate from different networks of the nervous system, namely those that handle motor, sensory, hearing, visual, thinking and talking functions, i.e. higher mental activities. Acoustic hallucinations and sound events experienced as inadequate in relation to the auditory scene are common, a fact that underlines the need *Corresponding author. Tel.: q46-46-1738-88; fax: q4646-1738-84. E-mail address:
[email protected] (O. Olsson).
for further investigations of psychoacoustic processes in this disorder. Indirect evidence for the existence of the schizophrenic disorder may be drawn from cognitive testing (Hentschel and Smith, 1980; Heinrichs et al., 1997). A few neurophysiological measures have been found to be typical for the diagnosis. The best known is perhaps the dishabituation of the sensory-motor system, a general deficit of function that may be related to some other findings: retarded orienting response, unchanged startle reflex and lessened accuracy of smooth pursuit eye movements. Abnormalities in EEG measures such as P300, P50 and pre-pulse inhibition have been assessed as typical for the diagnosis (Freedman et
0165-1781/02/$ - see front matter 䊚 2002 Elsevier Science Ireland Ltd. All rights reserved. PII: S 0 1 6 5 - 1 7 8 1 Ž 0 2 . 0 0 2 4 8 - 2
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al., 1996; Romani et al., 1987). An important finding regarding hearing and schizophrenia was ¨ et al. (1987), who demonreported by Lindstrom strated an aberration of the auditory pathway in schizophrenics by means of ABR (auditory brainstem response). Several perceptual deficits have been discovered it this laboratory regarding psychoacoustical functioning in schizophrenics. These regard streaming (sorting into frequency layers depending on amplitude relations), restoration of missing sounds and abnormal final percepts after complex sound stimulation (Olsson, 2000). The brainstem and subcortical structures together with cortical networks are at work in auditory processing. McKay et al. (2000) found differences between reference subjects and schizophrenics on tests of filtered speech perception and dichotic speech tests. They argued that the deficits might be associated with central auditory processing in the right hemisphere. Rainowicz et al. (2000) found an impaired delayed tone-matching performance in schizophrenia. They further showed that schizophrenic subjects had no increased susceptibility to auditory distraction and concluded that the dysfunction originates in temporal rather than prefrontal cortex. Green et al. (1999) found visual backward masking deficits in schizophrenia. These dysfunctions inspired us to look into masking processes in the auditory field. 1.2. Auditory masking Auditory masking refers to the increase in detection threshold of a certain stimulus, when presented in the presence of another distracting sound (Kohlrausch and Houtsma, 1989). Qualitative similarities and temporal relations between the stimulus and the masker determine the potency of masking effect. The masker is presented at the same time as the target tone (simultaneous masking, SM), preceding the target tone (forward masking, FM) or presented after the target tone (backward masking, BM). Usually the stimulus consists of a sinewave tone and the masker either of a sine-wave tone or a filtered noise. For SM it has been concluded that suppression in the cochlea accounts for most of the effect (Moore, 1997; Delgutte, 1990), although regions
more centrally located in the auditory system might be involved (Nieder and Klump, 1999). Furthermore, dendritic filtering mechanisms intrinsic to the dorsal cochlear nucleus (DCN) might contribute to the facilitation of stimulus detection in noise (Frisina et al., 1994). FM has been explained by ringing of the basilar membrane (Carlyon, 1988), but the large discrepancy between spike counts in single auditory nerve neurons and behavioral thresholds (Relkin and Turner, 1988) suggests a role for more centrally located functions. One such mechanism could be echo-suppression in the DCN, wherein spectral and temporal properties of auditory information are modulated (Kaltenbach et al., 1993). FM is present for ISIs (interstimulus intervals) up to 200 ms (Scharf, 1970). The distracting effect of BM is less potent than for FM and is generally thought to reflect cortical functions (Soderquist et al., 1981). Elliot (1962) suggested that the effect of BM is achieved when the masker catches the stimulus tone up, because the higher energetic masker is more rapidly and dominantly coded than the target tone. This is supposed to happen at some place central to the cochlea (Elliot 1962). The BM effect is present for ISIs up to 25 ms (Scharf, 1970). Backward and simultaneous masking abilities deteriorate with age (Gehr and Sommers, 1999; Moore, 1997). This study was undertaken as a consequence of earlier studies involving processes basically resting on masking as a fundamental component. Especially, the role of aberrations in perception of restoration of missing sounds, where schizophrenics have altered thresholds, pointed to the need for further investigations on masking and schizophre´ 1999; Nielzen ´ and Olsnia (Olsson and Nielzen, son, 1997; Warren et al., 1972). 1.3. Aims of study This study aims at investigating several aspects of auditory masking in schizophrenia. It is assumed that schizophrenic subjects may show impairments of masking functions, as they have earlier shown aberrations in experiments where masking plays an integrated role. Comparisons with reference
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subjects are carried out, and the influence of anxiety is controlled. 2. Methods 2.1. Stimuli and masker In all experiments a 1000-Hz sine-wave tone with 0.010 s impulse length and 0.002 s rise and fall time was used as the target stimulus. A 1500Hz low pass filtered noise (Butterworth filter) was used as the masker. The duration of the masking noise was 0.750 s with 0.005 s rise and fall time (cf. Fig. 1). The duration of the masking noise was chosen to avoid effects of temporal integration, which are present at durations shorter than 0.53 s (Brahe-Pedersen and Elberling, 1972). The stimuli and noise were constructed using MATLAB (5.1), Signal Processing Toolbox and a Silicon Graphics (O2) workstation. In the simultaneous masking (SM) experiments the stimuli and masker were presented simultaneously with the stimuli tone placed in the center of the masking noise. In the forward masking (FM) and backward masking (BM) experiments, the ISIs were 0.020 s. The test material was presented with the use of the software SoundEdit 16 (44.1 kHz sampling rate) on a Macintosh Powerbook G3. The output of the Powerbook was connected to headphones (TDH 39) with cushions (MX41yAR). Presentations were made binaurally with the stimuli in phase over headphones. In all tests the level of the masking noise was kept constant at 83 dB SPL. The amplitude level of the sine-wave tone was varied (cf. Section 2.2). Calibration of the sound ¨ & Kjaer 2203 levels was performed using a Bruel ¨ & Kjaer 4152 sound-level meter with a Bruel artificial ear. 2.2. Procedure All tests were performed in a satisfactorily soundproofed room. Before the presentations the subjects were verbally informed of the nature of the experiments, and the sine-wave tone they should respond to was presented to them. The subjects were tested one at a time. A positive
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response to each stimulus was verbally indicated by the subjects and transformed to the test protocol by the test leader. Thus, a staircase method was used rather than forced-choice paradigm commonly used in masking experiments (Penner, 1995). One reason was the inclusion of schizophrenic subjects who may not tolerate long-duration and monotonous procedures. However, the testing was done by means of two staircases going up and down, in order that the subjects could learn the test. Only the second staircase was used for subsequent analysis in the study. At the start of each experiment the level of the stimuli was kept well below the level of detection w73 dB SPL (hearing level) for SM; 46 dB SPL for FM; and 46 dB SPL for BMx and increased in steps of 3 dB to a level well above detection (91 dB SPL for SM; 91 dB SPL for FM; and 91 dB SPL for BM). This sequence was then repeated in a descending order. Each test was repeated twice, because the first part of the test was suspected to become biased by unwanted differences in learning and cognition. As indicated above, the second part of the presentations (SM presentations no. 15–28, FM and BM no. 33–64) is referred to as ‘stabilized thresholds’ and in the analyses these are defined as the mean of the ascending and the descending ones. 2.3. Subjects Twelve hallucinating schizophrenic outpatients participated in the experiments, six females and six males. The diagnosis of schizophrenia was established by a senior psychiatric physician according to DSM-IV (American Psychiatric Association, 1994, pp. 285–286). The hallucinations were anamnestically documented by chief physicians, and during the test the subjects neither subjectively reported nor objectively displayed any signs of ongoing hallucinations. Patients with a history of organic brain disease, alcoholic or drug abuse, or the presence of additional psychiatric diagnosis were excluded. All subjects were tested to exclude hearing impairment (Peter Montne´ mery). The medication given is the only one and not confounded with other pharmaceutical substances. A formal consent was ascertained in accor-
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Fig. 1. Experimental design. Grey areas represent the masking noise. White squares indicate the sine-wave tone and broken lines indicate the variations of the amplitude of the target tone.
dance with the requirements of the ethical committee at the University of Lund (171–94). An equal number of healthy individuals matched for age (cf. Table 1) and gender were also investigated and used as reference subjects. Furthermore, eight subjects with the diagnosis panic disorder, four males and four females (mean ages
44.24 and S.D.s14.43), were recruited to control for a possible influence of anxiety. 3. Results As can be seen in Figs. 2–4, no difference between schizophrenics and reference subjects
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Table 1 Some identifying and background variables of the subjects with schizophrenic symptoms Ind. no.
Age
Sex
Medication mgyweek
No. of admissions
Duration of illness (years)
DSM-IV diagnosis
No. of months as inpatient
1 2 3 4
44 42 38 61
M F F M
13 1 5 15
20 14 3 25
295.30 295.30 295.30 295.30
26 1 5 36
5 6 7 8 9 10 11 12
45 53 32 37 57 43 33 43
M M M M F F F F
Roxiam 2450 mg Perphenazine 900 mg Haloperidol 28 mg Flupenthixol 3.5 mg Clozapine 1400 mg Risperidone 35 mg Perphenazine 28 mg Flupenthixol 28 mg Haloperidol 28 mg Risperidone 35 mg Zuclopenthixol 250 mg Clozapine 4200 mg —
7 1 5 5 3 1 3
15 25 3 11 29 24 17 11
295.30 295.10 295.30 295.20 295.30 295.30 295.10 295.10
8 25 1 31 15 11 54 1.5
MsMale, FsFemale.
emerged for SM, while there were differences between schizophrenics and reference subjects regarding FM and BM. As mentioned earlier, the results are based on the values of the second staircase. No statistically significant differences were observed regarding SM. Schizophrenics showed significantly raised thresholds compared to reference subjects regarding FM (Mann–Whitney U-test, Zsy3.38, P0.001). Likewise, in the BM experiment, the schizophrenics were less sensitive to the target tone; they needed a higher sound level to detect it (Mann–Whitney U-test, Zsy2.40, P-0.05) Table 2. In Table 3 a division of the reports of the schizophrenics in the FM experiment was made. Those who did not hear the target tone when all reference subjects did (exposition 40) were categorized into one group (very increased threshold, VIT; ns6) and the rest of the schizophrenics into another (increased threshold, IT; ns6) (cf. Fig. 3). The comparison IT schizophrenics (ns6) and the references (Ns12) were significantly different regarding FM (Mann–Whitney U-test, Zsy2.10, P-0.05). Still more significant was the difference between the VIT schizophrenics and the reference subjects (Mann–Whitney U-test, Zsy3,41, P0.001). The comparison between the VIT and IT schizophrenic subgroups was significant regarding FM (Mann–Whitney U-test, Zsy2.90, P-
0.005). A comparison between the IT and VIT subgroups concerning months as inpatients showed a significant difference (Mann–Whitney U-test, Zsy2.25, P-0.05). For BM the only significant difference was revealed when references were compared with schizophrenics with VIT (Mann– Whitney U-test, Zsy2.30, P-0.05). In the reference group, simultaneous and backward masking thresholds were positively correlated with age (Spearman, simultaneous masking; rs 0.67, P-0.05: backward masking; rs0.81, P0.01). No significant correlations with age were present for the schizophrenic group. Neither were there any significant differences between patients medicated with high dose neuroleptics vs. those medicated with low dose neuroleptics. Comparisons between reference subjects, schizophrenics and panic disorder subjects showed the following results: panic disorderyreferences, SM Mann–Whitney U-test, Zsy0.12, Ps0.91; FM, Mann–Whitney U-test, Zsy0.50, Ps0.61; BM, Mann–Whitney U-test, Zsy0.08, Ps0.94. Between panic disorder and schizophrenics the following values resulted: SM, Mann–Whitney Utest, Zsy0.27, Ps0.79; FM, Mann–Whitney Utest, Zsy2.12, Ps0.03; BM, Mann–Whitney U-test, Zsy1.50, Ps0.13. These results indicate that no specific differences may be related to the influence of anxiety as it is manifested in panic disorder and in schizophrenia as well.
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Fig. 2. Simultaneous masking condition: Frequency distribution of the number of individuals who heard the sine-wave tone for each presentation (abscissa). Unfilled squaressreference subjects (Ns12) and filled squaressschizophrenics (Ns12).
4. Discussion Before mentioning the main findings, a brief comment will be made on matters of design and rating. Data from tests on schizophrenics often ´ 1982). However, show great variability (Nielzen,
when experiments are constructed in series of events in regular patterns, aberrations in schizophrenics may emerge due to their specific perceptual and behavioral characteristics. That is why such a design was used in this study. It may also explain why recent studies have failed to demon-
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Fig. 3. Forward masking condition: Frequency distribution of the number of individuals who have heard sine-wave tone for each presentation (abscissa). Unfilled squaressreference subjects (Ns12) and filled squaressschizophrenics (Ns12).
strate auditory masking aberrations in schizophrenics (March et al., 1999). Another problem is that schizophrenics often are said to be unable to understand or perform experimental testing. Therefore, their ratings are claimed to be invalid or not reliable in many contexts (Steinberg, 1986). How-
ever, in a circumscribed experimental situation, these arguments have been shown to be misleading because it even happens that schizophrenics may be more reliable in their reports than reference subjects (Hemsley, 1993). Psychotic processes influence the former group, but these effects may
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Fig. 4. Backward masking condition: Frequency distribution of the number of individuals who have heard the sine-wave tone for each presentation (abscissa). Unfilled squaressreference subjects (Ns12) and filled squaressschizophrenics (Ns12).
be counterbalanced by dishabituation, which is combined with rigidity and resistance against swiftly changing circumstances. The latter group is influenced by environmental and perhaps personally upsetting factors, which lead to uncertainty of ratings. With the design of this study the ratings on simultaneous masking by the schizophrenics
were very close to those of the reference group (cf. Table 2), which strengthens validity and reliability. The first of the main findings is that schizophrenic and reference subjects responded in the same manner regarding simultaneous masking. Most researchers (Moore, 1997) are convinced
¨ J. Kallstrand et al. / Psychiatry Research 113 (2002) 115–125 Table 2 Group differences for thresholds between reference subjects and schizophrenic subjects References
SM FM BM
P-value
Schizophrenics
Means
S.D.
Means
S.D.
5.0 4.5 3.1
1.1 1.5 2.1
4.7 8.0 7.9
1.0 2.8 5.1
0.58 (n.s.) 0.001*** 0.02*
SMsSimultaneous masking (8 stimulus steps); FMsforward masking (16 stimulus steps); BMsbackward masking (16 stimulus steps). *sSignificance below 0.05; ***sSignificance below 0.005. Reference subjects, Ns12; schizophrenic subjects, Ns12.
that simultaneous masking mainly depends on mechanical functions of the basilar membrane and low brainstem functions, but this process may also be influenced by central modulation. Our finding is in concordance with those by McKay et al. (2000), who observed several aberrations at cortical levels in schizophrenics but not at low brainstem levels. The second main finding consists of a significant difference between schizophrenic and reference subjects regarding forward masking. Schizophrenics detected the target tone at a higher signal to noise ratio in comparison with the reference subjects. A mechanistic interpretation may be introduced as an explanation for the forward masking phenomenon (Carlyon, 1988). According to this,
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ringing of the basilar membrane would hamper the later detection of the target tone. However, an argument that schizophrenics should have a deficient function of the basilar membrane is not upheld in any context. It has been shown that the signal to noise ratio (now in terms of spike counts) in the auditory nerve is well-preserved (Relkin and Turner, 1988). It is equally unlikely that schizophrenics should display any aberrations of the auditory nerve. Kaltenbach et al. (1993) argues that the main mechanisms for forward masking consists of shaping of the acoustical input by mainly DCN in line with evolutionary demands for suppression of redundant information, especially of successive more or less insignificant elements (echoes). The difference of FM between the studied groups could be explained by the assumption that the disintegration of the schizophrenic nervous system extends even to low regions of brainstem nuclei. However, as it is known that schizophrenics often have cortical dysfunctions in the temporal and frontal lobes, it is more reasonable to postulate that FM is regulated by cortical activity to a substantial extent. The third important finding was discovered in connection with backward masking. The schizophrenics detected the sine-wave tone later than the reference subjects. Although the view has been advanced that backward masking does not exist (Moore, 1997; Miyazaki and Sasaki, 1984), but
Table 3 Group comparisons between reference subjects and schizophrenic subjects with increased and very increased thresholds, regarding forward masking References
Schizophrenics IT
SM FM BM No. of admissions Duration of illness (years) Inpatient (months) Age
Group comparisons VIT
5.0 (1.1) 4.5 (1.5) 3.1 (2.1) — —
5.0 5.8 6.6 2.8 14.7
(0.9) (1.1) (4.9) (1.8) (10.6)
— 42.0 (14.2)
6.8 (5.6) 42.8 (8.3)
4.4 10.4 9.3 7.3 18.2
(1.2) (1.3) (5.3) (5.6) (6.3)
28.9 (17.1) 45.2 (10.3)
Ref.y schiz. IT
Ref.yschiz. VIT
Schiz. ITy schiz. VIT
n.s. 0.036* n.s. — —
n.s. 0.0006**** 0.021* — —
n.s. 0.0038*** n.s. n.s. n.s.
— n.s.
— n.s.
0.025* n.s.
SMsSimultaneous masking; FMsforward masking; BMsbackward masking. ITsIncreased threshold; VITsvery increased threshold. References, Ns12; schizophrenics IT, ns6; schizophrenics VIT, ns6. *sSignificance below 0.05; ***sSignificance below 0.005, ****sSignificance below 0.001. The three left-handed columns refer to means and S.D.
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much effort has been made by others to explain the phenomenon, whose existence they convincingly demonstrate (Scharf, 1970; Crawley et al., 1994). According to the mainstream of theories, backward masking necessarily involves handling of the auditory input by high central nervous network systems, notably those represented by temporal and frontal cortical areas. Schizophrenics surely have deficits in these systems (Kuperberg and Heckers, 2000), a fact which is further supported by the present findings. The group with very increased thresholds showed the highest impact of illness, as measured by months of inpatient care and, therefore, the deficient functioning may be related to the degree of illness. There were no significant differences related to age, sex and the other background factors including medication between subgroups of schizophrenics. Reference subjects showed a significant correlation between SM and BM thresholds and age. The age effect is attributed to successively deteriorating brain processes (Gehr and Sommers, 1999; Moore, 1997). A possible explanation for the lack of this in schizophrenics could be that schizophrenic adaptation aims at compensating attentive deficits of the illness while reference subjects might become more suppressive with regard to unimportant stimuli with age. Another possibility is that impairment with age causes the correlation while in schizophrenics the impact of the already existing illness plays the main role— and there may be other explanations. The normal auditory masking pattern was not influenced by panic disorder or the anxiety related to this illness. This, together with the lack of major influences from studied background factors among the schizophrenics and the increasing deterioration of forward masking threshold with greater need of inpatient care speaks for the likelihood that the results here dealt with are related to the schizophrenic disease. While SM may be considered to reflect mechanical cochlear mechanisms and neural processes at low levels, FM may be seen as a more elaborate functional mechanism involving mainly the cochlear nucleus and probably cortical areas. Contrary to this and according to experimental
assessment, BM involves higher structures, the temporal lobe and frontal cortical structures. The importance of the findings in this study is that they reveal varying degrees of dysfunction in essential processes of auditory function in schizophrenics. However, a more basic function such as simultaneous masking is not affected here. In the present sample of schizophrenics, the impaired performance connected to the forward masking experiment hints at the possibility that dysfunctions exist not only in cortical networks but in brainstem networks as well. Acknowledgments This study was supported by grants from the ¨ Sjobring Foundation at the Division of Psychiatry of the Lund University, The Royal Swedish Academy of Sciences, The Royal Physiographic Society of Lund and Pfannenstill Foundation of Lund. References American Psychiatric Association, 1994. Diagnostic and Statistical Manual of Mental Disorders, 4th ed. Washington, DC. Brahe-Pedersen, C., Elberling, C., 1972. Temporal integration of acoustic energy in normal hearing persons. Acta Otolaryngologica (Stockholm) 74, 398–402. Carlyon, R.P., 1988. The development and decline of forward masking. Hearing Research 32, 65–79. Crawley, E.J., Kallman, H.J., Neely, J.H., 1994. A test of an interruptionytemporal-uncertainty theory of auditory backward recognition masking of target duration. Acta Psychologica (Amsterdam) 87, 1–18. Delgutte, B., 1990. Physiological mechanisms of psychophysical masking: observations from auditory-nerve fibers. Journal of the Acoustical Society of America 87, 791–809. Elliot, L.L., 1962. Backward and forward masking of probe tones of different frequencies. Journal of the Acoustical Society of America 34, 1116–1118. Freedman, R., Adler, L.E., Worsley-Myles, M., Nagamoto, H.T., Miller, C., Kilsy, M., McRae, K., Cawthra, E., Waldo, M., 1996. Inhibitory gating of an evoked response to repeated auditory stimuli in schizophrenic and normal subjects. Archives of General Psychiatry 53, 1114–1121. Frisina, R.D., Walton, J.P., Karcich, K.J., 1994. Dorsal cochlear nucleus single neurons can enhance temporal processing capabilities in background noise. Experimental Brain Research 102, 160–164. Gehr, S.E., Sommers, M.S., 1999. Age differences in backward masking. Journal of the Acoustical Society of America 106, 2793–2799.
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