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2019, Volume 10, Issue 4, pages: 01-13 | doi:10.18662/brain/01

Auditory Brainstem
Response
Abnormalities in
Schizophrenic
Patients with
Auditory
Hallucinations

Mohammad SAYADNASIRI¹,
Omid REZAEI2,
Raheleh KOMAR3

1 Psychosis Research Center, University of
Social Welfare and Rehabilitation sciences,

Tehran, Iran. Nasiri115@yahoo.com

2 Psychosis Research Center, University of
Social Welfare and Rehabilitation sciences,
Tehran, Iran.
Dr_omid_rezaee@yahoo.com

3 Islamic Azad University, Science and
Research Branch, Tehran, Iran.
Raheleh_komar@yahoo.com

Abstract: Background: although the exact pathogenesis of auditory
hallucinations is not yet known, some suggested the impairment of
perception and processing of auditory information as a possible
explanation. So, the aim of this study is to evaluate auditory pathways of
schizophrenic patients using auditory brainstem responses (ABR).
Methods: schizophrenic patients with auditory hallucinations and age and
sex matched healthy non-relative controls were recruited in this case-
control study. Scale for assessment of positive symptoms (SAPS) was
used for rating the severity of hallucinations. Then, ABR recorded from
all participants and the latencies of waves I, II, III, IV, V and inter-
peak latencies (IPL) of waves I-III, III-V were analyzed on both sides.
Chi squire and independent t tests were applied for statistical analysis. P-
value≤0.05 was considered significant.
Results: 39 patients and 35 controls were included. Latencies of waves
III and V and IPL of III-V were significantly prolonged on the left side.
Disease duration had no influence on the results.
Conclusion: there is a link between abnormal ABRs and auditory
hallucinations in schizophrenic patients that indicates dysfunction and
abnormal asymmetry of auditory pathways in these patients.

Keywords: schizophrenia; auditory brainstem response; auditory
hallucination.

How to cite: Sayadnasiri, M., Rezaei, O., & Komar, R. (2019).
Auditory Brainstem Response Abnormalities in Schizophrenic
Patients with Auditory Hallucinations. BRAIN. Broad Research
in Artificial Intelligence and Neuroscience, 10(4), 01-13.
doi:10.18662/brain/01

mailto:Nasiri115@yahoo.com
mailto:Dr_omid_rezaee@yahoo.com
mailto:Raheleh_komar@yahoo.com

Auditory Brainstem Response Abnormalities in Schizophrenic Patients with …
Mohammad SAYADNASIRI et al.

1. Introduction

Schizophrenia is a chronic mental illness that affects about 1% of the
population (Patel et al., 2014). Signs and symptoms of this disease are
classified into three major categories of positive, negative, and cognitive
signs. Abnormal sensory experiences such as hallucinations are among the
most common positive signs of the disease with 70% of schizophrenic
patients experiencing auditory hallucinations (Waters et al., 2012). The exact
mechanism of auditory hallucination in schizophrenic patients is still not
well understood. However, recent studies have revealed certain aspects of it
(Kumar et al., 2009; Tracy and Shergill, 2013), some of the most important
of which focused on changes in brain lateralization of these patients.
Reduction of right ear processing ability in the dichotic listening test
(Hugdahl et al., 2008), decreased right-handedness (Hirnstein and Hugdahl,
2014), and changes in language lateralization (Ocklenburg et al., 2013) are
among the findings of studies conducted on schizophrenic patients.
Meanwhile, the decreased volume of Heschl’s gyri, especially in the left
hemisphere and smaller size of right inferior colliculus are recent findings in
the brain of schizophrenic patients that can be associated with auditory
hallucinations (Kasai et al., 2003; Kang et al., 2008). Interestingly, this
decrease in the nervous system volume occurs mainly in areas related to the
central auditory system. Therefore, it seems that the prevalence of auditory
hallucinations in schizophrenia is associated with structural changes in the
brain.

Some researchers investigating the mechanisms of auditory
hallucinations have studied central auditory pathways through
electrophysiological recording methods, and since the brainstem is the main
transmission route of auditory information, recording of auditory evoked
potentials (AEP) in the brainstem is considered an optimal
electrophysiological method for studying this sign (Wahlstrom et al., 2015).

Auditory brainstem response (ABR) is an exogenous response that is
recorded in the first 10 milliseconds (ms) of an auditory stimulation in the
auditory pathways and is a sign of simultaneous neuronal activity from the
auditory nerve through the brainstem (Wahlstrom et al., 2015). Few studies
evaluating ABR in schizophrenic patients with or without auditory
hallucinations yielded inconsistent results; the abnormal findings of these
studies included the absence of one or more waves, an increase in the waves’
latency, and a decrease in waves’ amplitude (Harrel et al., 1986; Hayashida et
al., 1986; Igata et al., 1994; Lindstrom et al., 1987; Siegel et al., 1984).

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Artificial Intelligence and Neuroscience Volume 10, Issue 4

Although there is no agreement on abnormal ABR findings in schizophrenic
patients, these changes indicate a brainstem dysfunction and possibly a
defect in the processing of auditory perceptions in its early stages. This
means that auditory signals undergo abnormal changes before they reach the
auditory cortex.

Therefore, we designed a case-control study to investigate changes in
the brain AEPs in schizophrenic patients with auditory hallucinations to
help better understand the abnormalities of the central auditory pathways of
these patients.

2. Materials and methods

2.1. Participants

This is a cross-sectional descriptive-analytic study that was
conducted from August to December 2017 at Razi Psychiatric Center
(Tehran, Iran). Patients aged 18 to 60 years admitted to this center with a
diagnosis of schizophrenia were considered to be included in the study.
Inclusion criteria were schizophrenia confirmed by a psychiatrist (OR)
according to DSM-5 criteria and presence of active auditory hallucinations.
Patients with hearing impairment, known central nervous system (CNS)
diseases (history of stroke, head trauma in the last 3 months, history of
epilepsy or seizure in the last 6 months, multiple sclerosis or other CNS
inflammatory diseases and history of brain tumors) and systemic diseases
(such as diabetes) that affect the auditory pathways were excluded. Healthy
ones, non-relatives of patients with no history of psychotic disorders in their
first degree relatives, were selected as controls.

2.2. Ethical considerations

The study was approved by the Ethical Review Board, University of
Social Welfare and Rehabilitation Sciences (1395.158). Informed consent
was obtained from all participants or their first degree relatives; they were
able to withdraw the study at any time.

2.3. Data collection

Demographic data including age, gender, duration of illness, and
drug use were recorded. The Scale for the Assessment of Positive Symptoms
(SAPS) was used to record and determine the intensity of hallucinations.
This scoring system provided by Andreasen in 1984 evaluates four domains
of schizophrenia, including hallucination, delusion, bizarre behavior, and
positive formal thought disorder. The hallucination domain consists of

Auditory Brainstem Response Abnormalities in Schizophrenic Patients with …
Mohammad SAYADNASIRI et al.

seven items, including auditory hallucinations, voices commenting, voices
conversing, somatic or tactile hallucinations, olfactory hallucinations, visual
hallucinations, and global rating of hallucinations, ranging from zero to five
in severity. This test has good validity and inter-rater reliability for the
screening of positive signs (Andreasen, 1984). Then, ABR of all participants
was recorded with an EMG/NC/EP device (Negarandishegan Co., model
5000Q). This test, which lasts about 20 minutes, is non-invasive and does
not require active collaboration of the patient. The patient sits in a relaxed
position on a chair in a dimly lit room. Two active electrodes are placed on
both mastoids, a reference electrode on the vertex, and an earth electrode on
the forehead using a special gel, and then a headphone is placed on the
participant’s ears. Before starting the test, the impedance of the electrodes is
measured to ensure their proper connection. First, the test method is fully
explained to the participant and a short-sequence click is sent to the patient’s
ears to become familiar with the test. The device then sends 1000 audio
clicks (not more than 80 dB) separately to each ear. The duration and
frequency of each click are 1 ms and 5 Hz, respectively. The device records
the signals of neuronal activity in the auditory nerve and brainstem 10 ms
after each click. These potentials include five waveforms named I to V, and
the five-wave latency and the inter-peak latency (IPL) of the I-III, III-V
waves are determined individually for each ear and recorded in ms. The
results of ABR are analyzed by a neurologist (MS) who is blind to the
participants.

2.4. Statistical analysis

Data were analyzed in SPSS 20 through chi-square and independent
t-test for single-variable data. P-values of 0.05 or less were considered
significant.

3. Results

A total of 39 schizophrenic patients (20 male) and 35 healthy
controls (20 male) were recruited for the study. The median age was 37.5
years for the patients and 34.5 years for the controls. Twenty-three patients
(59%) had disease duration more than 2 years.

In the hallucinations domain of SAPS, the mean severity of auditory
hallucinations, voices commenting, voices conversing, and global rating of
hallucinations were 3.8±0.02, 3.7±0.04, 2.2±0.02, and 3.9±0.03, respectively.

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Artificial Intelligence and Neuroscience Volume 10, Issue 4

Figure 1. Severity of auditory hallucinations according to the Scale for the
Assessment of Positive Symptoms.

Comparison of latencies of ABR waves recorded from the right ear
showed no significant changes between patients and controls (Table 1).

Table 1. Comparison of right sided ABR waveform latencies between
patient and control groups.

Latency (±SD)

Waves Patients
(n=39)

Controls
(n=35)

P value

I 1.78±0.02 1.77±0.02 0.27

II 2.87±0.04 2.87±0.04 0.53

III 3.95±0.02 2.96±0.02 0.06

IV 5.25±0.02 5.25±0.03 0.74

V 5.80±0.01 5.80±0.03 0.35

I-III 2.24±0.02 2.21±0.19 0.34

III-V 1.85±0.01 1.83±0.04 0.13

0,5

1,5

2,5

3,5

Auditory
hallucinations

Voices commenting

Voices conversing

Global rating of
hallucinations

Auditory Brainstem Response Abnormalities in Schizophrenic Patients with …
Mohammad SAYADNASIRI et al.

Table 2. Comparison of left sided ABR waveform latencies between patient
and control groups.

Latency (±SD)

Waves Patients
(n=39)

Controls
(n=35)

P value

I 1.78±0.02 1.77±0.02 0.52

II 2.85±0.03 2.86±0.04 0.30

III 3.95±0.03 2.97±0.04 0.03

IV 5.24±0.03 5.23±0.05 0.47

V 5.81±0.02 5.77±0.08 0.03

I-III 2.23±0.02 2.25±0.04 0.23

III-V 1.86±0.01 1.82±0.03 0.001

Table 3. Comparison of right sided ABR waveform latencies between
patients with different disease duration. (DD: disease duration)

Latency (±SD)

Waves DD<2 yr
(n=16)

DD>2yr
(n=23)

P value

I 1.78±0.02 1.78±0.02 0.34

II 2.87±0.04 2.87±0.03 0.47

III 3.95±0.02 3.94±0.04 0.62

IV 5.25±0.02 5.25±0.03 0.24

V 5.80±0.01 5.81±0.03 0.32

I-III 2.24±0.02 2.23±0.03 0.51

III-V 1.85±0.02 1.83±0.04 0.27

Table 4. Comparison of left sided ABR waveform latencies between
patients with different disease duration. (DD: disease duration)

Latency (±SD)

Waves DD<2 yr
(n=16)

DD>2yr
(n=23)

P value

I 1.78±0.02 1.78±0.01 0.54

II 2.85±0.02 2.85±0.04 0.37

III 3.95±0.03 2.97±0.04 0.33

IV 5.24±0.03 5.23±0.05 0.47

V 5.81±0.02 5.77±0.08 0.64

I-III 2.23±0.02 2.25±0.04 0.23

III-V 1.86±0.01 1.82±0.03 0.45

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Comparison of latency of ABR waves recorded from left ear
between patients and controls showed a significant difference in the waves
III, V, and III-V, so that the latency was longer in the patient group (Table
2).

To evaluate the effect of the duration of the disease on the ABR
findings, patients were divided into two groups of disease duration of less
than two years and more than two years, and the latency of their waves was
compared, showing no significant difference (Tables 3 and 4).

4. Discussion

Our study showed that the presence of auditory hallucinations in
schizophrenic patients was associated with changes in AEPs; i.e., the
prolonged latencies of the waves III, V and III-V IPL on the left side was
significantly correlated with auditory hallucinations.

Study of auditory, visual, and somatosensory evoked potentials in
schizophrenia has been of interest to researchers since the 1980s, although it
has not yet found its place as a biomarker in the diagnosis of these patients.
Kubiszewski et al. (1993) reviewed the findings of evoked potentials in
schizophrenic patients and presented the most common changes as 1)
higher sensory evoked potentials (SEP) amplitude during first 0.1 seconds in
chronic schizophrenic patients with severe psychotic signs, 2) reduced
amplitude and latency of ABR waves and increased waveform variability of
visual evoked potentials (VEP) in schizophrenic patients with active
hallucinations, 3) N2 latency prolongation in motor responses to simple and
complex stimuli, 4) abnormal P300 and 5) increased waveforms variability
in all modalities in chronic schizophrenics (Kubiszewski et al., 1993).

Although attempts to record changes in the evoked potentials in
schizophrenic patients have contributed to the understanding of structural
abnormalities in the central and peripheral nervous system of these patients,
there are still contradictions in these findings. According to researchers,
impaired ABR indicates abnormal processing of auditory information and
impairment in sensory inhibitory gating in schizophrenic patients, which can
lead to auditory hallucinations (Freedman et al., 1996; Siegel et al., 1984).

Siegel et al. (1984) evaluated sensory gating in schizophrenic patients
by recording ABR and found that, compared to normal subjects,
schizophrenic patients (and some of their first-degree relatives) had deficits
in inhibition of second auditory stimuli. The researchers interpreted these
findings in favor of gating impairment or the inability to filter auditory
stimuli, meaning that the influx of sensory information into the brain of

Auditory Brainstem Response Abnormalities in Schizophrenic Patients with …
Mohammad SAYADNASIRI et al.

these patients (in the absence of appropriate and effective filtering) leads to
misinterpretation and the occurrence of psychotic signs (Siegel et al., 1984).

In one of the first studies in this regard, Lindstrom et al. (1987)
reviewed changes in ABR waves in patients with auditory hallucinations and
recorded abnormal ABR waves in half of the 20 patients. These abnormal
changes did not correlate with severity of signs, age, and gender, but the
association of abnormal ABR with auditory hallucinations was statistically
significant; so that 9 out of 11 patients reporting auditory hallucinations had
abnormal ABR. The researchers concluded that the brainstem dysfunction
was involved in the psychopathology of schizophrenia, and impaired
auditory pathways in the brainstem could lead to hallucinations in these
patients (Lindstrom et al., 1987). In our study, as in the above research,
abnormal changes were recorded in ABR, which could be in favor of an
organic basis for the production of auditory hallucinations in schizophrenic
patients. These researchers suggested mechanisms, such as denervation
hypersensitivity for auditory hallucinations which can result in spontaneous
impulse generation in the presence of neuronal injury (Lindstrom et al.,
1987).

Lindstrom et al. (1990) investigated the relationship between
impaired ABR and monoamine metabolites (HVA, 5-HIVV) in the
cerebrospinal fluid of schizophrenic patients. Patients with abnormal ABR
had a lower level of HVA. These findings suggest that brainstem
dysfunction is associated with decreased levels of dopaminergic and possibly
serotonergic activity in schizophrenia (Lindstrom et al., 1990).

In another study, Igata et al. (1994) recorded ABR in 30
schizophrenic patients. In 27% of patients, at least one of the waves I, II or
III was missed on either side. The authors interpreted these changes in favor
of impaired auditory transmission in the inferior brainstem. In this study,
ABR changes were associated with negative signs of patients (not
hallucinations) (Igata et al., 1994). In our study, the pattern of ABR
involvement was in favor of auditory pathways impairment in the superior
brainstem, and these contradictions indicate that impaired ABR in
schizophrenia is not specific and fixed, especially with regard to patient’s
symptoms.

Various neurophysiologic hypotheses have been proposed for the
occurrence of hallucinations in schizophrenia including auditory
hallucinations (Chen et al., 2019; Cho and Wu, 2013; Kumar et al., 2009;
Tracy and Shergill, 2013; Zhang et al., 2018). In the neurophysiologic
dissociation theory, the occurrence of hallucination arises from dissociation
of the primary sensory cortex from the cortical association areas (Kumar et

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Artificial Intelligence and Neuroscience Volume 10, Issue 4

al., 2009). In the present study, prolonged latency of the recorded waves can
lead to dissociation of the auditory cortex from the pathways ending to it,
indicating the reduced regulatory effect of cortical areas on lower pathways,
which can lead to hallucinations. Another theory in this approach is the
perceptual release, based on which a censorship mechanism in the brain can
actively keep away most of the sensory information that continually reaches
the brain from the conscious level (Aleman & Laroi, 2008; Kumar et al.,
2009). However, the censorship mechanism has the best performance when
there is a continuous flow of sensory inputs. Impairment in recorded ABRs
in the present study will also lead to disintegration of the auditory
information input to the brain; so, this impaired censorship mechanism is
another mechanism that is suggested for the auditory hallucinations in the
patients of this study. However, it should be emphasized that none of the
above mechanisms alone can justify hallucinations in these patients (Aleman
& Laroi, 2008). For example, impaired ABR waves can be secondary to a
defect in the superior brainstem that can simultaneously cause
neurotransmitter disorders which role in the occurrence of auditory
hallucinations has been proven (Jardri et al., 2016).

Asymmetry of abnormal ABR changes with a leftward focus was
another remarkable point in this study. Although the auditory pathways in
the brainstem can establish bilateral hemispheric connections, these findings
reconfirm the abnormal asymmetry of brain connectivity in schizophrenic
patients (Ribolsi et al., 2014). In recent years, several pieces of evidence have
been obtained regarding the decrease in normal asymmetry and the
occurrence of both structural and functional abnormal asymmetry in
schizophrenic patients (Ribolsi et al., 2014; Sun et al., 2017). For example,
patients with significant positive signs have shown leftward asymmetry in
the brain functional connectivity confirmed by fMRI (Andreou et al., 2015;
Ke et al., 2010; Xie et al., 2018). In contrast, patients with more severe
negative signs showed a rise in rightward asymmetry of functional
connectivity (Ke et al., 2010). This asymmetry in the central pathways
(including the brainstem auditory pathways in our study) can be of a
developmental nature and confirm the neurodevelopmental hypothesis in
schizophrenic patients. The ineffectiveness of the disease duration on the
findings of ABR also suggests that these changes are likely to occur before
the onset of clinical disease.

The present study had some limitations. In this study, the traditional
method for recording auditory-evoked activity was employed which detects
mainly the subcortical (brainstem) auditory pathways. So, this method would
not completely elucidate the cortical contribution of auditory processing and

Auditory Brainstem Response Abnormalities in Schizophrenic Patients with …
Mohammad SAYADNASIRI et al.

for this reason, limits our study. New methods for concurrent brainstem and
cortical AEP measurements may be more useful to analyze disturbed neural
pathways of hallucinating patients (Slugocki et al., 2017). In addition, our
findings were based on monaural stimulation but some studies emphasizes
on the binaural testing in evaluation of central auditory pathways which
represents signal detection in a noisy environment. Assessment of binaural
interaction may reveal additional abnormalities in patients with auditory
hallucinations. For this assessment, some studies used artificial intelligence
such as a hybrid machine learning approach for the objective detection of
the central auditory pathway disorders and showed promising results
(Strauss et al., 2004).

For further research, evaluation of AEPs of healthy first degree
relatives of the patients, applying new methods of AEP recording and
simultaneous study of AEP-functional brain imaging would be practically
useful for elucidating the neural dynamics involved in auditory
hallucinations. Also, repeating ABR after attenuation of hallucinations can
help evaluate the relationship between ABR impairment and auditory
hallucinations more accurately.

5. Conclusion

The present study showed a relationship between the impaired ABR
in schizophrenic patients and their auditory hallucinations. This relationship,
which was mainly observed in the left side waves III, V and III-V IPL,
indicates that this dysfunction was in the superior half of the brainstem
(pons and above). So, disturbance in the auditory input processing in cortical
areas contribute to the occurrence of hallucinations. These findings
demonstrate the organic basis of auditory hallucinations in this disease and
may confirm the neurodevelopmental theory of schizophrenia.

Author’s contribution:

OR: design of the study, interpretation of data and revision of the article
critically
MS: the conception and design of the study, interpretation of data, drafting
and final approval of the article
RK: acquisition and analysis of data
Conflict of interest: none

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Artificial Intelligence and Neuroscience Volume 10, Issue 4

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