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International Journal of Audiology 2013; 52: 3–13
Discussion Paper
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Evolving concepts of developmental auditory processing
disorder (APD): A British Society of Audiology
APD Special Interest Group ‘white paper’
David R. Moore*, Stuart Rosen†, Doris-Eva Bamiou‡, Nicole G. Campbell§ & Tony Sirimanna#
*MRC Institute of Hearing Research, Nottingham, UK, †UCL Speech, Hearing & Phonetic Sciences, London, UK, ‡UCL Ear Institute and
Neuro-otology Department, National Hospital for Neurology and Neurosurgery, London, UK, §Institute of Sound and Vibration Research,
University of Southampton, Southampton, UK, #Department of Audiology & Audiological Medicine, Great Ormond Street Hospital, London, UK
Abstract
Children with listening difficulties, but normal audiometry, may be diagnosed with APD. The diagnosis is typically based on poor performance on tests of perception of both
non-speech and speech stimuli. However, non-speech test results correlate only weakly with evaluations of speech-in-noise processing, cognitive skills, and caregiver evaluations
of listening ability. The interpretation of speech test results is confounded by the involvement of language processing mechanisms. Overall, listening ability is associated more
with higher-level, cognitive and analytic processing than with lower-level sensory processing. Current diagnosis of a child with APD, rather than another problem (e.g. language
impairment, LI), is determined more by the referral route than by the symptoms. Co-occurrence with other learning problems suggests that APD may be a symptom of a more varied
neurodevelopmental disorder. Alternately, APD has been proposed as a cause of language-based disorders, but there is no one-to-one mapping between listening and language among
individuals. Screening for APD may be most appropriately based on a well-validated, caregiver questionnaire that captures the fundamental problem of listening difficulties and identifies areas for further assessment and management. This approach has proved successful for LI, and may in future serve as a metric to help assess other, objective testing methods.
Foreword
Auditory processing disorder (APD) has a long (⬎ 30 years) and controversial history. The controversies concern absolutely fundamental issues: the definition of APD, its neural
basis, test validity and standardization, differentiation from other disorders, and even whether it exists as an independent disorder (Jerger, 2009). To evaluate and interpret the
scientific evidence on APD, and to advise the audiology profession, the British Society of Audiology (BSA) established a Special Interest Group (BSA SIG) on APD in 2003. That
group has recently published two key documents, a ‘Position Statement’ and a ‘Management Overview’ (BSA, 2011, a,b. See www.thebsa.org.uk ‘Procedures and Publications’).
In formulating the new position statement, it became clear to the group that several significant differences were developing between their interpretation of the evidence concerning
APD and that of the American Academy of Audiology (AAA), as stated in their recently published ‘Guidelines for the diagnosis, treatment and management of children and adults
with central auditory processing disorder’ (AAA, 2010). To address these differences, and borrowing from British Parliamentary procedure, the BSA SIG decided to develop a ‘white
paper’, a discussion document that could then receive an international set of commentaries from other research groups working on APD. An approach was made to the editor of the
International Journal of Audiology who agreed to this suggestion. This paper, and the associated commentaries that follow, are the result.
Key Words: Behavioral measures; paediatric; speech perception; psychoacoustics/hearing science
Introduction
Some people who report listening difficulties in everyday situations
are found to have normal pure-tone thresholds (Hind et al, 2011).
Often, these people are simply told that nothing is amiss and sent on
their way. However, in many audiology services around the world,
they are invited to complete additional tests to investigate the possibility of an ‘auditory processing disorder’ (APD). Based on the
results of these tests, APD may be diagnosed and a management
regimen recommended (AAA, 2010). There is no doubt that auditory processing disorders can arise from frank lesions in the central
auditory system or may co-exist with, and/or be linked to peripheral
hearing loss (BSA, 2011a). Our focus here, however, is on the type
of APD that appears to be a developmental disorder, and is of most
concern in children, not least because of the impact it may have on
social development and on academic performance.
APD diagnosis is typically based, in North America, Europe
and Australasia, on poor performance on at least one core test of
‘auditory processing’ (AP). Core AP tests include both speech- and
non-speech-based tasks, the most commonly used of which are
duration and frequency patterns, dichotic words or sentences, and
Correspondence: David R. Moore, MRC Institute of Hearing Research, Nottingham, UK. E-mail: [email protected]
(Received 14 March 2012; accepted 15 August 2012)
ISSN 1499-2027 print/ISSN 1708-8186 online © 2013 British Society of Audiology, International Society of Audiology, and Nordic Audiological Society
DOI: 10.3109/14992027.2012.723143
4
D. R. Moore et al.
Abbreviations
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AAA
APD
ASHA
BSA
CANS
SLI
American Academy of Audiology
Auditory processing disorder
American Speech-Language-Hearing Association
British Society of Audiology
Central auditory nervous system
Specific language impairment
speech which has either been degraded by low-pass filtering, or
put in a background of noise (AAA, 2010; Emanuel et al, 2011).
Management strategies tend to focus on improving listening skills,
on the acoustic environment, on electronic delivery of enhanced
signal-to-noise ratios, and on auditory training (BSA, 2011b).
the cerebral cortex should be considered part of an extended CANS
(Moore, 2012). These cortical regions show evoked responses
to acoustic stimulation (Poremba et al, 2003), damage to them
produces auditory perceptual difficulties (Griffiths et al, 2010),
and they subserve the transition between coding simple and more
complex auditory attributes of sounds including speech (Scott &
Johnsrude, 2003; Scott, 2012). These and other regions (e.g. the
cerebellum; Callan et al, 2006) also mediate the cortical processing
of, and integration with, the higher-order cognitive components of
sound perception. They have strong reciprocal connections with
classical auditory cortical areas and, through the auditory cortex,
descending connections down to the entire sub-cortical auditory
system. They are thus able to influence the neural processing of
sound on its way up from the ear (Moore, 2012).
Attention and memory
Difficulties defining APD
No one has developed a satisfactory definition of APD, but we
now know more about what it is not (Burkard, 2009). Successive
position statements from ASHA, AAA, and BSA have suggested
that APD arises from deficiencies in the central auditory nervous
system (CANS; the brain pathway from cochlear nerve to auditory
cortex) leading to impaired performance on basic psychoacoustic
tasks (e.g. temporal processing and binaural interaction). Complex
hearing tasks (sound localization, pattern recognition, performance
with degraded signals or competing sounds) are also listed (ASHA,
1996). However, a number of studies (Watson & Kidd, 2009; Moore
et al, 2010) have failed to find any close or consistent correlation
between performance on non-speech psychoacoustic tasks and
indicators of listening and learning problems, including academic
ability, cognitive skills, speech-in-noise perception, and caregiver
ratings of communication and listening skills. These findings suggest that psychoacoustic performance is not a good indicator of the
reasons that people get referred for APD (the ‘clinical presentation’).
Insofar as electrophysiologic responses like the complex (speech)
auditory brainstem response (cABR) also reflect the fidelity of lowlevel sensory encoding, even if tuned by top-down influences over
the long term (Krishnan et al, 2005; Kraus & Chandrasekaran, 2010),
it seems unlikely that such measures will prove any more useful than
direct behavioural measures of low-level sensory processes.
Some speech-based hearing tasks may be better predictors (e.g.
LiSN-S; Cameron & Dillon, 2008), but these involve substantial
processing beyond the CANS, specifically in systems that are specialized for language. More generally, all auditory tests, whether
language-based or not, involve varying levels of cognitive engagement, so impaired attention or memory can and does contribute to
impaired auditory perception (see below). In an attempt to retain the
specificity of APD distinct from other developmental disorders, definitions have included clauses that exclude broad cognitive deficits,
particularly problems in attention. However, attention, as reflected
in variable performance on tests of AP, correlates far more with
clinical presentation measures of APD than does test threshold, the
usual index of performance (Moore et al, 2010).
Lessons from auditory neuroscience
Impaired auditory perception has traditionally been thought to
be caused by innate or acquired malfunction of the ear, nerve or
the CANS, excluding other brain regions. Only recently has it
become clear that the anterior lateral, frontal, and parietal lobes of
It is a matter of everyday experience that we must attend to sounds to
hear them properly (i.e. to listen). In addition, because sound stimuli
evolve across time, we need to remember what has gone before, and
integrate sound information across time. Finally, we need to act on
the sound we hear, for example by rehearsing the acoustic image,
moving it into longer term memory (Ronnberg et al, 2011), or by
making some other response such as (more prosaically) pushing a
button to show that we have heard the sound. The act of processing what is heard is thus complex and involves the intertwining of
auditory, cognitive (including attention and memory), and language
mechanisms (Medwetsky, 2011).
Attention and memory are inextricably linked with all forms of
sensory perception. It thus makes little sense to exclude the possibility that they contribute to APD. Psychologists have an elaborate
set of terms to describe various aspects of attention and memory,
but the important things for listening are that we can detect, discriminate, remember, understand, and act on a given pattern of auditory stimulation. For this reason, the most informative measures of
auditory cognition related to attention and memory are likely to be
those that are closely related to, and integrated with the auditory task
being performed. For instance, while detection and discrimination
thresholds are the standard measures of auditory performance, the
variability of threshold across time appears to be a useful indicator
of auditory attention, on the reasonable assumption that the sensory
coding of a sound is relatively invariant over the course of a testing
session. In fact, auditory threshold variability in children has been
shown to be related to parental evaluations of everyday listening
skills. It therefore follows that impaired everyday listening will be
associated with more variable performance arising from inattention
(Moore et al, 2008, 2010).
Speech perception and APD
Although general auditory problems may be an important aspect
of APD, the vast majority of concerns centre around aspects of
language, particularly speech perception. For example, of 13
behavioural manifestations said to be common among people
referred for APD in the AAA Clinical Practice Guidelines, nine
directly involve speech perception and one other the development
of literacy (AAA, 2010).
Speech is a highly redundant stimulus, meaning that it is only
under challenging listening conditions (but ones that occur often in
everyday life) that a speech processing difficulty may become apparent. This leads to a fundamental question about the nature of APD.
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Developmental auditory processing disorder
Is it a problem with the processing of all auditory signals, or is it
specific to speech signals? We do not currently know the answer to
this question, since it is possible that performance of other complex,
but non-speech tasks, either auditory or non-auditory, is also deficient in those having the clinical presentation of APD. Although it is
possible to construct nonspeech auditory discrimination tasks which
incorporate the kind of spectro-temporal complexity found in speech
and are essential for its perception, such stimuli have not been used
in investigations of APD. If the problem is specific to speech, it may
involve a very low, perhaps phonetic, level of linguistic processing,
since performance of low redundancy speech tasks (e.g. identification of VCV nonsense syllables against a nonsense speech masker)
by children is also related to parental reports of poor listening and
communication (Moore et al, 2010). This is not to say that higher
levels of linguistic processing could not also be compromised.
Almost all test batteries for APD incorporate speech-based test
material. Poor performance on these tests could mean a problem
with the processing of basic sounds by the CANS, or problems in
memory and/or attention, or it could mean a problem decoding the
more abstract aspects of speech—phonetics, syntax, semantics, and
vocabulary. For example, the commonly used SCAN-C (Keith,
2000) and more recent SCAN-3 (Keith, 2009) have a variety of difficulties when it comes to interpreting poor performance. Two of the
subtests use a dichotic presentation of competing words or sentences.
Such paradigms have long been used in experimental psychology
(Broadbent, 1958), and are more-often considered assessments of
attention and memory than auditory processing. An added complication is that the competing sentences subtest requires the participant to
repeat back a sentence played to one ear while ignoring a different
sentence in the other. However, performance on a sentence repetition
task in quiet was found to be the best predictor (of four) of language
impairment (Conti-Ramsden et al, 2001). Children with language
impairment may thus do poorly on this test for reasons unrelated to
an auditory processing problem. Consider finally the filtered words
subtest, in which low-pass filtered monosyllabic words are presented
for identification. What kind of auditory processing deficit could
possibly impair performance for stimuli like this, when there is less
information to process? How can this test be anything more than
a test of linguistic competence, in guessing a whole from limited
information? (Loo et al, 2012).
Testing and diagnosing APD
How then should we screen for and diagnose APD? For screening, it
seems to make sense to return to the clinical presentation. The most
common reason for APD referrals is listening problems, associated
with a wide variety of scenarios including difficulty in noisy environments, inability to follow conversations and, for children, concerns
about speech production, hearing in class, inattention (Hind et al,
2011) and poor academic performance. Clinicians presented with
these problems almost always take a clinical history. This may be
a checklist of commonly reported problems (a ‘structured history’)
or a more eclectic and individualized assessment. Such assessments,
however, are subject to the particular views and knowledge of the
interviewer. Importantly, it is difficult to recommend clear, mutually
agreed guidelines to practitioners, especially those unfamiliar with
all the various forms of presentation.
We suggest that a better way to capture and characterize the
nature of the children’s problems is to give them, or their caregiver, a well-validated questionnaire. For screening and diagnosis
of language and attention difficulties such questionnaires are already
5
available: the Children’s Communication Checklist (CCC-2; Bishop,
2003) and the Conners Rating Scales (Conners, 1996), respectively.
Currently available questionnaires of listening difficulties, such as the
Children’s Auditory Processing Performance Scale (the CHAPPS;
Smoski et al, 1992) lack such validation. A secondary reason for
developing such a questionnaire is as an index of the clinical presentation against which research evaluations of other methods of
testing may be compared. The need for this cannot be overstated; a
recent study identified nine different sets of diagnostic criteria for
APD (including BSA, AAA, and ASHA guidelines) and the resulting rates of diagnosis of APD ranged from 7.3% to 96% (Wilson
et al, 2012). Unsurprisingly, in light of this evidence, the validity
and reliability of APD diagnosis continues to be questioned, with
serious implications for access to appropriate educational support
and management of those affected.
Co-occurrence of APD with other learning difficulties
Children with listening difficulties often have other problems consistent with alternative and more recognized diagnoses. The clinical
presentation of APD has much in common with the most common
developmental language disorders—specific language impairment
(SLI) and dyslexia. Children diagnosed with any one of these conditions score similarly on a wide range of auditory, cognitive, and
communication evaluations, at least on the group level (Dawes et al,
2009; Dawes & Bishop, 2010; Miller & Wagstaff, 2011; Sharma
et al, 2009; Ferguson et al, 2011). There is also some evidence of a
higher incidence of symptoms related to autism spectrum disorders
in children diagnosed with APD but not, importantly, in children
diagnosed with dyslexia (Dawes & Bishop, 2010).
These overlaps could arise for a number of reasons. First is the
possibility that not all of these disorders are, in fact, distinct from
one another. Given that the methods currently used to diagnose APD
largely lack an evidence base, and are often based on tests like the
SCAN which would be expected to be difficult for children with
language impairment, it is hardly surprising that there is a lot of
comorbidity between APD and SLI. In this view, the diagnosis of
any particular child with APD is determined more by the referral
route than by the symptoms.
Second is the rather more interesting theoretical position that language disorders like SLI and dyslexia are in fact caused by an APD.
This idea has been promulgated most extensively by Tallal and her
colleagues, identifying a deficit in rapid auditory temporal processing as key (Tallal, 2004). Although there is still much controversy
about this hypothesis (see Rosen, 2003 for a review), only some children with language and reading difficulties have impaired auditory
processing and, even in those cases, the impairment is not restricted
to temporal processing. Furthermore, many children identified with
an APD do not develop a language disorder, although this may
be because they compensate for their APD. In short, there is no oneto-one mapping between listening and language difficulties.
Third is the possibility that all these features are symptomatic
of a more general neurodevelopmental delay. This hypothesis
is attractive because it allows both for the co-occurrence of
symptoms across disorders and for the considerable differences
observed between children receiving a single diagnosis. There
are, however, two major objections to this idea, one theoretical,
and one practical. Theoretically, it is crucial to note that the close
similarities between children with dyslexia or SLI and APD are
only true on the group level. There are many children with APD
who are not language impaired and vice versa. The evidence on
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6
D. R. Moore et al.
this issue is very clear, even for the closely related disorders of
dyslexia and SLI. For these it is known that there is quite a high
degree of comorbidity, but they are still known to be distinct disorders, with good evidence for different genetic bases to the two
(Pennington & Bishop, 2009). Practically, it would be a major
challenge for care services to be able to manage a single, more
broadly-ranging diagnosis. While parallel, multi-disciplinary
intervention may be the best solution, efficiency suggests that
a more hierarchical referral and management process, in which
audiologists and other relevant single-specialist professionals
(e.g. speech-language therapists/pathologists) could be trained
and involved, would be more realistic. More complex models
of comorbidity, involving multiple overlapping risk factors
(Pennington & Bishop, 2009), might be more suitable, insofar as the
focus is on the identification of the crucial risk factors and how they
interact to produce any particular developmental disorder.
Conclusions
• Developmental APD is considered as a diagnosis when people
referred to audiology services with concerns about ‘listening’
are found not to have a peripheral hearing problem or a neurological lesion.
• There is currently no clear evidence that auditory sensory processing is the core problem underlying developmental APD.
• Impaired listening is associated with poor attention and
working memory.
• APD often co-occurs with other learning and language
disorders, so may indicate a broader and more varied
neurodevelopmental disorder.
• A high-quality and validated questionnaire aimed at screening
for APD could pave the way for the development of more
sensitive diagnostic measures.
Acknowledgements
Written on behalf of the BSA APD Special Interest Group.
David R. Moore and Stuart Rosen contributed equally to writing
the paper.
Declaration of interest: The authors report no conflicts of interest.
The authors alone are responsible for the content and writing of
the paper.
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The following groups agreed to provide
comments on the preceding paper
Teri James Bellis, The University of South Dakota
Gail Chermak, Washington State University
Jeff Weihing, University of Louisville
Frank Musiek, University of Connecticut
As Moore et al note, there are significant differences in the evaluation and interpretation of evidence on APD (or central auditory processing disorder (CAPD) as the disorder is referred to in the United
States to emphasize its origins in the central nervous system), as
reflected in recent position statements and guidelines (AAA, 2010;
ASHA, 2005a, b; BSA, 2011a, b). We address our primary concerns
with their interpretation of the evidence here.
Moore et al state “There is no doubt that auditory processing disorders can arise from frank lesions in the central auditory system…
Our focus here, however, is on the type of APD that appears to be
a developmental disorder, and is of most concern in children...”
The implication of the distinction they construct is that CAPD
in children is not neurobiological. In fact, whether the source of
central auditory nervous system (CANS) dysfunction is benign
(maturational or neuroanatomical) or the result of frank neurological lesion or compromise, the underlying source of the resulting
central auditory deficits and CAPD originate in the central nervous
system (Chermak & Musiek, 2011). We also strongly disagree with
their statement “That the methods currently used to diagnose APD
largely lack an evidence base…”, and their conclusion that “There
is currently no clear evidence that auditory sensory processing is the
core problem underlying APD.” There are, in fact, multiple lines
of evidence confirming a core sensory processing deficit in CAPD,
including literature documenting CAPD in adults with confirmed
CANS lesions (see Musiek et al, 1994, for a representative example),
7
reports demonstrating the neuroanatomic source of CAPD in some
children (Boscariol and colleagues, 2009, 2010, 2011), similar
central auditory test performance across children diagnosed with
CAPD with and without confirmed neurologic lesions of the CANS
(Jerger et al, 1988), and, as importantly, similar central auditory
test performance patterns across children and adults with CAPD
(e.g. as in dichotic deficits (Musiek & Weihing, 2011)). Moreover,
there are plausible mechanisms explaining what would cause this
similarity to arise between neurologic patients and pediatric populations. For instance, when one considers the course of neuromaturation in the brain, it becomes clear that areas critical to auditory
processing (e.g. corpus callosum) are often affected by delayed
neuromaturation. Therefore, these areas are often found to be deficient in cases of CAPD (Musiek et al, 1984; Bellis & Wilber, 2001,
Musiek & Weihing, 2011).
Moore et al question the utility of using both speech and nonspeech test stimuli for diagnosis stating that “...non-speech test
results correlate only weakly with ... speech-in-noise processing,
cognitive skills and caregiver evaluations of listening ability”, and
that “Speech test interpretation is confounded by the involvement
of brain language processing mechanisms.” While we agree that
there is potential for language and cognitive (e.g. memory, attention) confounds, this is true of any task that requires cooperation and
behavioral response on the part of the child being tested. As with
any psychophysical measure (including pure-tone threshold testing), experienced clinicians must be on the lookout for test-related
indicators of attention and related confounds. In CAPD testing,
these confounds can be minimized by using simple speech stimuli
(e.g. digits), minimizing memory loading, utilizing intra-test measures which control, in part, for non-auditory factors (e.g. left vs. right
ear performance; see Bellis et al, 2011), and by employing a multidisciplinary team approach through which information regarding
attention, memory, language, and other functions is available. Additional controls in cases in which the possible presence of a linguistic
or memory confound exists may include assessing performance in
the non-manipulated condition (e.g. monaural versus dichotic, nonfiltered versus filtered, etc.) to ensure that performance deficits seen
on CAPD tests are due to the acoustic manipulations rather than to
lack of familiarity with the language and/or significantly reduced
memory skills. Inclusion of speech stimuli allows the audiologist
to obtain information regarding speech processing mechanisms in
the CANS which are not necessarily revealed through non-speech
stimuli (Grossman et al, 2010). Further, these stimuli have ecological
value, and because the degree of temporal processing required for
accurate perception of spoken language is significantly greater than
required for perception of non-speech sounds, processing of speech
signals may be more vulnerable to disruption by CANS dysfunction
(e.g. Fitch et al, 1997; Griffiths et al, 1999; Shannon et al, 1995;
Zatorre & Belin, 2001); therefore, in some cases central auditory
processing deficits may only be revealed using speech tasks
(e.g. Benavidez et al, 1999; Johnson et al, 2005; Russo et al, 2005).
Moore et al’s concern that non-speech test results correlate weakly
with speech-in-noise processing, deficiencies of which are a hallmark of central auditory processing disorder, argues for the inclusion
of speech tests in the test battery used to identify CAPD.
Regarding Moore et al’s concern about poor correlations between
non-speech test results and cognitive skills, academic and learning
abilities, caregiver evaluations of listening ability, and even some
(language-loaded) speech-in-noise tasks, we would note that there is
no reason to expect or demand strong correlations between measures
of CANS function and these indicators of higher-order functions.
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8
D. R. Moore et al.
While auditory perceptual difficulties are sometimes seen in children
with other primary diagnoses, including language impairment, attention deficits, and autism (Chermak et al, 1998; Rinker et al, 2007;
O’Connor, 2012), neither speech nor non-speech behavioral central
auditory perceptual tests are designed to be sensitive to these higher-order deficits (Musiek et al, 2005). Further, we would note that
there is generally little agreement between caregiver/informant subjective reports of listening skills and children’s actual performance
on central auditory measures (Drake et al, 2006; Lam & Sanchez,
2007; Wilson et al, 2011). Hence, the weak correlation between nonspeech diagnostic measures and subjective questionnaires does not
throw into question the utility of non-speech tests, but rather leads to
questions regarding the appropriate use of caregiver rating scales.
Moore et al dismiss electrophysiological measures that use speech
stimuli stating “... it seems unlikely that such measures will prove
any more useful than direct behavioural measures of low-level sensory processes.” There is accumulating evidence that a wide range
of electrophysiological measures provide an objective look at the
CANS and that some of these measures correlate with many of the
skills and abilities which Moore et al find lacking for non-speech
tests. Thus, not only do we find this evidence in the ABR to complex stimuli (cABR)(e.g. Banai et al, 2009, 2005; Billiet & Bellis,
2011; Kraus et al, 1996), but in the auditory middle latency response
(e.g. Purdy et al, 2002; Schochat et al, 2010), the auditory late
response (e.g. McArthur et al, 2009), and event related potentials,
such as the P300 & mismatch-negativity (e.g. Sharma et al, 2006;
Jirsa & Clontz, 1990) as well.
Moore et al correctly note that impaired listening can be associated with poor attention and working memory; however, their
assertion that “Overall, listening ability is associated more with
higher-level, cognitive and analytic processing than with lower-level
sensory processing” does not logically follow. There is no question
that working memory supports listening skills such as localization
ability (Martinkauppi et al, 2000) and speech recognition in noise
(Akeroyd, 2008; Wong et al, 2009). However, lower-level sensory
processes also have a profound impact on these skills, as even moderate declines in peripheral auditory acuity lead to a systematic down
regulation of neural activity during the processing of higher-level
aspects of speech (e.g. sentence comprehension) (Peele et al, 2011).
These interactions arise from brain organization and the nature
of information processing and they do not, therefore, negate what
we learn about lower-level sensory processing from sensitized
(i.e. efficient) behavioral and electrophysiological measures of
CANS dysfunction.
Moore et al state that the “The current diagnosis of a child with
CAPD, rather than another learning problem is often determined
more by the referral route than by the symptoms.” First, we must
emphasize that CAPD is not a learning problem. Second, the use of
teacher/parent report, as recommended by Moore et al, can lead to
inaccurate diagnosis. As shown by Wilson (2012), many children
perform well on performance-based measures of central auditory
processing despite caregiver-reports of these children encountering
listening difficulties. It is likely that using caregiver-report to diagnosis CAPD, as in Ferguson et al (2011), has contributed to the
observed overlap between CAPD and SLI noted by Moore et al.
Nonetheless, we are sensitive to Moore et al’s concern that diagnoses given to children often are influenced by the professional seeing
the child perhaps more so than guided by the symptoms. We would
argue that multidisciplinary teams working in cooperation rather
than competition, using measures with documented sensitivity and
validity for CAPD (as well as language, learning, listening, reading,
etc.) would address their concern. Contrary to Moore et al’s position
that the co-occurrence of CAPD with other learning problems “...
suggests that APD may be considered a symptom of a more varied
neurodevelopmental disorder,” we would argue that co-morbidity
does not invalidate a sensory-perceptual diagnosis, if such diagnosis
is based on an efficient test battery.
Finally, we are concerned about the potential adverse impact for
treatment and management of children with CAPD were Moore
et al’s recommendation adopted that “Assessment of APD may be
most appropriately based on a well-validated, caregiver questionnaire that captures the fundamental presenting problem of listening
difficulties.” There is no question that questionnaires have value;
however, employing a questionnaire to assess CAPD would suggest to professionals and insurers that evaluating children who
demonstrate behaviors consistent with ‘listening’ or auditory problems need not include a controlled battery of central auditory (and
peripheral auditory) tests. Given the limitations of questionnaires, as
noted above, their exclusive use for diagnosis of CAPD would lead
to uncertain diagnoses, less precise information to guide intervention, and certainly less well targeted and therefore less effective and
efficient intervention.
In closing, we commend our colleagues for their work in this
area and for providing an opportunity for discussion of a range of
issues which must be resolved to ensure delivery of the best clinical
services to children with CAPD.
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Comments from:
Harvey Dillon, National Acoustic Laboratories, Sydney, Australia
Sharon Cameron, National Acoustic Laboratories, Chatswood,
Australia
The White Paper raises some very relevant issues regarding concepts
related to APD. It is helpful that the authors have specified the disorder under discussion as being developmental in nature which is
indeed the most common form of APD to be encountered clinically.
This is not to say that all forms of APD are developmental, or that
developmental problems will self-resolve with time.
However, in the first of their concluding statements the authors
refer to developmental APD as being considered a ‘diagnosis’
when “… people referred to auditory services with concerns about
‘listening’ are found not to have a peripheral hearing problem or
a neurological lesion”. This statement suggests that anyone with
normal hearing thresholds and no identified brain lesion who has
concerns regarding their ability to ‘listen’ has developmental APD.
We assume that this definition of developmental APD is derived
from the authors’ belief that there are no assessment tools—
either behavioural or electrophysiological—that can accurately and
unequivocally diagnose such a ‘disorder’.
To this end, the authors conclude that performance on nonspeech tests is only weakly correlated with indicators of listening
and learning problems (such as speech-in-noise perception and
academic performance) which they term the ‘clinical presentation’. Whereas the authors acknowledge that some speech-based
assessments tools—such as the Listening in Spatialized Noise–
Sentences test (LiSN-S)—may be better predictors of clinical
presentation, performance on such tests may be too strongly
influenced by higher-order processes such as language ability,
attention, and memory to be valid indicators of basic auditory
processing abilities. Degree of variability across performance on
a range of AP tests is suggested as correlating better with clinical presentation than the threshold achieved on any one test. Our
interpretation of the White Paper is that, based on the abovementioned problems that the authors consider are inherent within
the currently available APD test battery, the best AP diagnosis
is achieved via parental report, preferably using a well validated
questionnaire.
10
D. R. Moore et al.
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Whereas we agree with many of the opinions expressed in this
paper, we would like to take this opportunity to expand and challenge some of the conclusion drawn as follows:
1. The term APD, be it developmental or otherwise, is a largely
useless descriptor for clinicians and parents alike, akin to a doctor providing a diagnosis of a “sore leg” when a patient has a
fractured patella. In order for appropriate management to be
effective—be it deficit-specific remediation or some form of
compensation—the clinician must be aware of the exact nature
of the deficit they are required to manage. It is unlikely that such
a diagnosis can be achieved from examining a questionnaire. We
suggest that specific sub-types of auditory processing disorders
be defined that can be diagnosed using sensitive and specific,
ecologically valid, behavioural, or electrophysiological tests
(incorporating speech or non-speech stimuli) that have extensive, age-specific normative data and have been rigorously evaluated in the target population.
2. We agree that higher-order cognitive abilities can impact on
the performance of many tests currently used to assess AP disorders. This fact was extremely influential in the development
of the LiSN-S (Cameron & Dillon, 2007). The target stimuli
were specifically developed for children from four years of age.
The rule of measuring performance as the difference in dB
between various test conditions was specifically adopted to
minimize the effect of language and other cognitive functions
on test performance (if the performance of the client was
impacted by such issues the difference between two test conditions that differed only in one aspect—e.g. spatial location of
the maskers—would be minimally impacted). Intermittent
variations in attention can, however, occur with any test battery, be it auditory or cognitive, and must be managed by the
professional administering the tests.
3. The statement that “attention, as reflected in variable performance on tests of AP, correlates far more with clinical presentation measures of APD than does test threshold” appears to arise
from performance on a long and repetitive test battery reported
by Moore et al 2010. It is not surprising that the children who
most quickly gave up on trying their hardest at some or all tests
(and hence had variable performance) tended to be those most
likely to exhibit the type of problems that cause their teachers
or parents to seek an APD assessment. Moore et al have labelled
the underlying attribute as attention. It could equally be labelled
as motivation, vigilance, or perseverance. Irrespective of the
label applied, the impact of such an attribute on some test
scores does not logically mean that the symptoms thought to
be associated with APD cannot also be associated with the
scores obtained on other tests where the attention/motivation/
vigilance/perseverance of the child has been maintained
through suitably short tests or suitably interesting test design
and administration.
4. We agree that short term and/or working memory deficits or
attention problems can have a negative impact on AP test
performance; however this issue should not deter the clinician
from performing an AP assessment. The clinician can include in
the battery a test of auditory memory, or perhaps even auditory
continuous performance, and evaluate overall AP performance
in light of these test results.
5. In respect to the authors’ conclusion that there is “...currently
no clear evidence that auditory sensory processing is the core
problem underlying APD”, we assume that the authors believe
that attention, memory, and higher order language skills account
for all instances of (developmental) APD published to date in
the literature. One reason for this belief may be that many
studies have specifically targeted children with conditions such
as language impairment or dyslexia. These higher order conditions may have impacted on the AP test results. In our studies
with the LiSN-S we took great care to separate groups based
on presenting profile and to examine test results accordingly.
As such, Cameron & Dillon (2008) found that nine children,
recruited with a presenting profile of difficulty understanding
speech in the classroom with IQ results within normal limits
and no other diagnosed disorder, were all outside normal limits
on the spatially-separated conditions of the LiSN-S, whereas
eleven children with a cognitive deficit of some type all performed within normal limits on all LiSN-S conditions. These
results provide evidence of a specific auditory sensory processing
deficit (which we termed spatial processing disorder or SPD)
as the core problem in these particular children who presented
with listening deficits in the absence of any other condition.
The fact that the children with SPD were all within normal
limits on the conditions of the LiSN-S where the target and
masker stimuli were collocated (i.e. where no spatial processing
was required) further strengthens the argument for a specific
form of auditory sensory processing being the core problem for
these children. Studies have also shown (individual and group
results) that SPD is totally reversible in children with SPD
(Cameron & Dillon 2011), that the remediation occurs only
with deficit-specific training, and that the improvement posttraining is reflected in patient, parent, and teacher questionnaires concerning real-life listening (Cameron et al, submitted).
So while we do not doubt that a proportion of children have a
deficit in auditory vigilance or attention, our own studies have
shown that at least one auditory sensory deficit does indeed
exist and can be remediated, thereby improving quality of life.
We are not suggesting that SPD will be the only auditory
deficit that can be identified, and for which the effects of
remediation will generalize to real life.
6. In respect to the authors’ concluding point, we support the need
for a high-quality and validated questionnaire and agree with the
importance that the paper places on establishing the degree
of difficulties experienced in real life. Such a measure could
provide the gold standard used to assess whether a particular
type of remediation has actually helped a child, rather than
simply made the child more skilful in some test, the results of
which caused the child to be diagnosed as “having APD”.
Thank you for the opportunity to comment on this important and
challenging topic. It will only be when we as a field have identified
a set of auditory skills, each of which can be improved by an appropriate remediation, and when that remediation results in improved
listening in daily life, demonstrated through suitable questionnaires, that we will have a meaningful idea of the scope of auditory
processing abilities and disorders. Such a focus is more likely to
be productive than a search for a single method of diagnosing a
disorder that that we already know has different underlying deficits
in different children.
Comments from:
James Jerger and Jeffrey Martin, The University of Texas at
Dallas/Callier Center for Communication Disorders, Dallas, USA
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Developmental auditory processing disorder
We congratulate the Special Interest Group (SIG) of the
British Society of Audiology (BSA), and the authors of this
important “white paper”, for their willingness to attempt to make
some sense of a substantial collection of very murky concepts,
historical missteps, and contradictory data. In particular, they have
highlighted the importance of cognitive and linguistic factors in
understanding the nature of developmental listening problems. There
can be no doubt that attention, memory, and language disorder are
the elephants in the room. One can view them either as confounds
in traditional behavioral tests of an assumed sensory disorder or,
indeed, as key factors underlying the very nature of a “more general
neurodevelopmental delay”. The important point made by the authors
is that the situation is far more complicated than many clinicians and
researchers, in a variety of disciplines, would have us believe.
It would be a mistake to minimize efforts to document how (and
when) genuine dysfunction in auditory processing leads to selective
impairments in auditory perception, including the development of
techniques for purposes of validation. Not incorporating evidence
from neuropsychology and auditory neuroscience, highlighting the
importance of cognition in APD research and clinical practice, would
constitute a larger mistake. In fact, it is difficult to dismiss that such
(cognitive) mechanisms could be equally responsible for some of our
own past APD findings. Such is the path of science.
We find ourselves in essential agreement with all of the authors’
conclusions, with the possible exception of reliance on questionnaires for diagnosis: surely we can do better than that. Can we not
benefit, as so many other fields have, from decades of advances in
neuropsychological evaluation, electroencephalographic averaging,
and brain-imaging techniques to guide us?
It is perhaps not premature to suggest that this paper serve as an
impetus for the implementation of an international consensus conference on APD under the auspices of BSA-SIG.
Response to the Reviewers' Comments
from Moore, et al:
We, the members of the BSA Special Interest Group on APD, would
like to thank the three groups of reviewers for taking the trouble
to comment on this ‘white paper’, and also the editor-in-chief of
TIJA, Dr Ross Roeser, for organizing its appearance. We believe
that all members of the international community want to achieve a
shared understanding of APD, based on the highest level of scientific
evidence and reasoning. As suggested by Drs. Jerger and Martin, an
important goal is an international consensus, and we are delighted
that the American Academy of Audiology now plans to make an
APD symposium a regular (two-yearly) part of their annual meeting (Audiology Now!), following the successful symposium “Global
Perspectives on (C)APD” which was held in Boston in March 2012.
Because of some overlap in the points made by each group of
reviewers, we have elected to organize our response in terms of the
general issues raised by them, rather than dealing with each set of
comments in turn.
11
no other known etiology and presumably present from birth),
acquired (associated with a known peri- or post-natal event such
as neurological trauma or infection), and secondary (occurring
in association with a known genetic cause1 or peripheral hearing impairment). In the white paper, we deal only with the most
common category, developmental APD. There is currently no
evidence that developmental APD is caused by or associated
with a specific neurological disorder. The evidence that some
behaviours associated with developmental APD (e.g. atypical
ear advantage) resemble those of patients with acquired APD
does not mean that developmental APD is due to a recognized
neurological disorder. Current understanding of other developmental disorders is also instructive in this respect. For example,
the study of acquired dyslexia in adults, usually as the result of
stroke, has provided few or no useful lessons for understanding
developmental dyslexia in children. Studies of the sequelae of
damage to a fully developed adult brain encourage the notion of
either impaired or spared systems. By contrast, in a child without
neurological damage, the development of various cognitive skills
is highly interdependent, so separate skills cannot be considered
in isolation (see Karmiloff-Smith, 1997; Karmiloff-Smith et al,
in press).
Sensory, perceptual, and cognitive aspects of hearing
It is practically impossible fully to dissociate these different
aspects of auditory processing because of the highly interconnected
and recurrent nature of auditory system functional connectivity.
Nevertheless, the ‘sensory’ part of hearing we take to be processing
along the classic, ascending auditory system from the ear to primary
auditory cortex. This is, of course, the main highway for delivery
of auditory information. It is essentially the same in humans and
other mammals, and functions fairly similarly during wakefulness,
sleep, and under general anaesthesia. In contrast, ‘perception’ is the
conscious interpretation of sensory signals, based on innate biology, experience and ‘cognition’ which includes attention, memory,
language, and understanding. The growing recognition that cortical
areas beyond the auditory cortex (anterior temporal, frontal, inferior parietal) are necessarily involved in perception, and should be
regarded as part of the ‘central auditory nervous system’ (CANS),
also makes categorical distinctions difficult. Similarly, descending pathways having their origins in the cortex and, relaying back
down through the midbrain and the brainstem to the cochlea and
middle ear, can transmit cognitively and perceptually relevant
information to the very earliest stages of sensation, modulating
and gating the input to the brain. That seems a good reason to drop
the ‘C’ from (C)APD, the indisputable neuroscience showing that
the ear, the recognized CANS, and much of the cerebral cortex are
all necessary for normal hearing. It is universally recognized that
the pure-tone audiogram does not provide a comprehensive assessment of auditory perception. But a finding of normal audiometry
remains a strong indicator of normal peripheral function. In this
sense, we can therefore agree that ‘auditory processing’ begins at
the cochlear nerve.
The neurobiological origin of APD
and our focus on development
It is an axiom of psychology and neuroscience that all behavior,
whether normal or disordered, is biological in origin, although
clearly formed by interaction with the environment. We have
proposed elsewhere (BSA, 2011a) that APD should be divided
into three categories: developmental (normal audiometry with
Tests of auditory perception
Two issues identified by the reviewers were the use of speech
vs. non-speech tests, and the impact of cognition, specifically language difficulties, on speech-based test performance. These are,
of course, related issues. We (BSA, 2011a) had proposed that, to
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12
D. R. Moore et al.
eliminate the influence of specifically language skills, it is necessary to use non-speech stimuli to demonstrate specifically auditory processing problems. We have never suggested that speech
perception is unimportant, only that tests using speech necessarily
engage language mechanisms that are not traditionally considered
part of hearing. In fact, we argue strongly for the central role of
speech perception in thinking about APD. The ‘clinical presentation’, the reason children are referred for APD assessment, is
always related to listening and related communication difficulties,
but never based on ‘auditory processing’ in the sense of basic
psychoacoustic skills.
In the white paper we noted that speech-based hearing tasks
may be better predictors of the clinical presentation, but that these
involve substantial processing beyond the CANS. Reviewers point
to attempts made to limit involvement of higher level processing
by, for example, comparing performance in two different conditions (e.g. monaural vs. dichotic, unfiltered vs. filtered, front vs.
side sound delivery). These attempts limit cognitive involvement to
different degrees: monaural vs. dichotic hardly at all, since different
signals to each ear clearly pose a different cognitive challenge than
the same signals to one ear. However, comparing target signals presented from different directions relative to a masking signal (spatial
release from masking, SRM), as used in the LiSN-S (Cameron &
Dillon, 2008), is a more subtle issue. A speech target in a speech
masker is a highly complex acoustic signal involving both energetic
and informational masking (Shinn-Cunningham, 2008). This means
that while some of the SRM is due to binaural processing, presumably in the brainstem, some is due to language-based analysis of the
signals, the informational content of which would differ in the two
spatial conditions. So this example, which is cited by the reviewers
as one in which care was taken to minimize cognitive processing,
is one in which cognitive processing could account for a significant
portion of the measured effect. Further research could help determine the size of that portion but, in simple terms, this means that spatial processing disorder (SPD), considered to be a ‘specific auditory
sensory processing deficit’, may be at least somewhat dependent on
language processing. This does not mean that the LiSN-S is a poor
test of APD, or of SPD, only that it is extremely difficult to separate
sensory and cognitive contributions to perception, especially when
using speech-based tests.
If APD is primarily a core sensory processing deficit, as argued
by reviewers, then nonspeech tests should be sufficient to detect
those deficits. Take, for example, sensitivity to amplitude modulation (AM), a key component of temporal processing ability on the
scale of a few ms to hundreds of ms. Obtaining low AM thresholds,
from say 2 to 1000 Hz in a temporal modulation transfer function
(Viemeister, 1979), requires a much better ability to detect AM than
understanding noise-vocoded speech (Shannon et al, 1995) which
requires sensitivity only to modulation rates below about 20–50 Hz,
and AM that is well above threshold. In short, the degree of temporal
processing required for the accurate perception of spoken language
is not significantly greater than that required for good performance
in non-speech tasks, and is typically less.
Questionnaires
All three reviews expressed some reservations as well as some support for the use of questionnaires. We reinforce here the argument
presented in the white paper that a well-validated questionnaire can
serve two important purposes. First, it could serve as a standardised
screening tool now and, probably, into the foreseeable future. We
recognize that a questionnaire is not an end in itself, and is only
one element of a potential diagnostic battery. However, it could
replace or supplement clinical histories that vary in construct and
interpretation with the skills and knowledge of the attending clinician2. Second, we urgently need a benchmark against which other
potentially useful developments of sensitive and appropriate tests
of auditory processing, including behavioural, electrophysiological,
and molecular metrics, may be assessed. Our message is clear: unless
a test is sensitive to the symptom (in this case, a listening problem)
it is not diagnostic.
Electrophysiology
A claim often made about human electrophysiology is that it
is somehow more objective than behavioural measures. We are
tempted to make the opposite claim. Unless supported by behavioural evidence, electrophysiology is uninterpretable. Also, because
electrophysiology, like behaviour, is an index of neural function, it
will be generated by the same mechanisms and subject to the same
influences as behaviour. Consider the complex auditory brainstem
response (cABR). Recent work cited in the reviews has shown
that various aspects of cABR waveform and timing are related
to auditory performance (e.g. speech-in-noise perception) and
influenced by experience (e.g. music and language training). But
those findings provide potentially important research evidence on
mechanisms of auditory function and dysfunction only because of
their association with the relevant behaviour. How or where neural
generators shape the cABR remains an almost completely open
question. Recent studies (e.g. de Boer & Thornton, 2008; Bajo
et al, 2010; Irving et al, 2011) suggest that descending pathways
from the cortex modulate subtle aspects of auditory learning. In
each case, however, those relationships are drawn on the basis
of behaviour. It is clear that electrophysiology is clinically useful
when behavioural measures are difficult or impossible to obtain
(e.g. in infants) and where there is a relatively well understood
relationship between a particular function and the site of generation
of the electrical response (e.g. electrocochleography). The finding that central electrophysiological measures among individuals
correlate better with higher level skills such as speech-in-noise
perception than do simple non-speech behavioural measures only
serves to reinforce our underlying hypothesis: Perceptual variation
between individuals with normal peripheral hearing is more a topdown than a bottom-up phenomenon.
A final practical and fundamental problem is that there are currently no available electrophysiological measures of sufficient utility and reliability to be useful in the clinical assessment of APD
(McFarland & Cacace, 2012; Hornickel et al, 2012). A plethora of
measures and stimuli is used inconsistently from study to study, with
no clear evidence of replicability across studies.
Epilogue
Our hope is that the debate captured in our white paper and the
following discussion will stimulate further, hypothesis-led research,
culminating in evidence-based diagnosis and intervention. For clinicians, the question of what to do now about APD is probably best
summarized in the recent paper of Dillon and colleagues (2012):
“Patients will be best served by focusing on whether they have difficulty understanding speech, identifying the specific characteristics
of this difficulty, and specifically remediating and/or managing those
characteristics” (p. 97).
Developmental auditory processing disorder
Notes
Int J Audiol Downloaded from informahealthcare.com by Hadassah college - Library on 04/23/13
For personal use only.
1. A ‘known genetic cause’ was not part of the proposal in BSA
(2011a), but represents a potentially important omission that we
would wish to add here. An example might be an association
with Downs Syndrome.
2. It is worth making a general point here. Many clinicians are
undoubtedly highly skilled at guiding a consultation towards the
particular needs of a client, and that role will continue. However,
evidence-based medicine also requires, where possible, the utilization of appropriate and well conducted research findings. Part
of that process means that objectively derived test measures are
usually preferable to measures that depend heavily on individual
clinical skills.
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