Neurocase
The Neural Basis of Cognition

ISSN: 1355-4794 (Print) 1465-3656 (Online) Journal homepage: https://www.tandfonline.com/loi/nncs20

Aprosodia and prosoplegia with right frontal
neurodegeneration
James R. Bateman, Christopher M. Filley, Elliott D. Ross, Brianne M. Bettcher,
H. Isabel Hubbard, Miranda Babiak & Peter S. Pressman
To cite this article: James R. Bateman, Christopher M. Filley, Elliott D. Ross, Brianne M. Bettcher,
H. Isabel Hubbard, Miranda Babiak & Peter S. Pressman (2019): Aprosodia and prosoplegia with
right frontal neurodegeneration, Neurocase, DOI: 10.1080/13554794.2019.1646291
To link to this article: https://doi.org/10.1080/13554794.2019.1646291

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NEUROCASE
https://doi.org/10.1080/13554794.2019.1646291

Aprosodia and prosoplegia with right frontal neurodegeneration
James R. Bateman a, Christopher M. Filleyb,c, Elliott D. Rossd,e, Brianne M. Bettcherf, H. Isabel Hubbardg,
Miranda Babiakh and Peter S. Pressmani
a
Department of Neurology, Wake Forest School of Medicine, Winston-Salem, VISN 6 Mental Illness Research, Education, and Clinical Center (MIRECC),
Salisbury, NC, USA; bBehavioral Neurology Section, Departments of Neurology and Psychiatry, University of Colorado School of Medicine, Aurora, CO,
USA; cRocky Mountain Alzheimer’s Disease Center, Marcus Institute for Brain Health, Aurora, CO, USA; dDepartment of Neurology, University of Oklahoma
Health Sciences Center, Oklahoma City, OK, USA; eBehavioral Neurology Section, Department of Neurology, University of Colorado Anschutz Medical
Campus, Denver, CO, USA; fDepartments of Neurology and Neurosurgery, Behavioral Neurology Section, Rocky Mountain Alzheimer’s Disease Center,
University of Colorado Anschutz Medical Campus, Aurora, CO, USA; gCommunication Sciences and Disorders, University of Kentucky, Lexington, KY, USA;
h
Audiology and Speech-Language Sciences, University of Northern Colorado, Greeley, CO, USA; iBehavioral Neurology Section, Department of Neurology,
University of Colorado School of Medicine; Rocky Mountain Alzheimer’s Disease Center, Aurora, CO, USA

ABSTRACT

ARTICLE HISTORY

Affective prosody and facial expression are essential components of human communication. Aprosodic
syndromes are associated with focal right cerebral lesions that impair the affective-prosodic aspects of
language, but are rarely identified because affective prosody is not routinely assessed by clinicians.
Inability to produce emotional faces (affective prosoplegia) is a related and important aspect of affective
communication has overlapping neuroanatomic substrates with affective prosody. We describe
a patient with progressive aprosodia and prosoplegia who had right greater than left perisylvian and
temporal atrophy with an anterior predominance. We discuss the importance of assessing affective
prosody and facial expression to arrive at an accurate clinical diagnosis.

Received 28 February 2019
Accepted 15 July 2019

Introduction
Human communication involves both what a person says and
how that person says it. The same words can have very
different implications if uttered with sincerity versus sarcasm,
or with a smile versus a grimace. Research over the last 150
years has established that various aspects of propositional
language may be disrupted by focal lesions of the left hemisphere, giving rise to aphasic syndromes. In contrast, focal
lesions of the right hemisphere do not cause aphasic syndromes, but do cause deficits in the affective aspects of language and communication, including facial expressions.
Prosody is a paralinguistic aspect of language that is realized acoustically through variations in pitch, loudness, syllable
and word duration, pauses, stress, tempo, and timbre. There
are two major subcategories of prosody, linguistic and affective, each having a different neuroanatomical substrate (Ross,
Shayya, & Rousseau, 2013). Linguistic prosody often clarifies
the literal aspects of speech. Linguistic stress may emphasize
part of a phrase or word to convey the correct semantic intent;
for example, compare the semantic difference between “hotdog” versus “hot dog,” or “object” (noun) versus “object”
(verb). In contrast, prosodic stress and pausing may be used
to clarify potentially ambiguous syntax and emphasize the
most important word in a sentence (pragmatic intent). For

KEYWORDS

Aprosodia; prosody;
neurodegeneration; aphasia

example, compare the following sentences with the exact
same word order, “John e-mailed . . . his friend from Denver”
versus “John e-mailed his friend . . . from Denver.” Affective
prosody, on the other hand, layers emotional and/or attitudinal meaning on top of linguistic information (Ross & Monnot,
2008; Ross et al., 2013), which may alter communicative intent.
For example, if the sentence “He is smart” is strongly stressed
on “is”, it acknowledges the person’s ability. A strong stress on
“smart” with a terminal rise in intonation, however, indicates
sarcasm. In addition, affective prosody can convey emotions
such as anger, happiness, fear, or surprise. In non-tone languages, such as English, the manipulation of pitch over time
(intonation) appears to be the most salient acoustic correlate
of affective prosody (Ross, Edmondson, & Seibert, 1986).
The neuroanatomic substrate of prosody is complex.
Affective prosody is disrupted by focal lesions of the right
hemisphere that give rise to various clinical syndromes, called
aprosodias, which are analogous to the aphasic syndromes
observed after focal left hemisphere damage (Ross, 1981).
The Aprosodia Battery (ApBat; Ross & Monnot, 2008; Ross,
Thompson, & Yenkosky, 1997) was developed specifically to
detect patterns of deficits in affective prosody associated with
left versus right brain damage under incrementally reduced
verbal-articulatory demands. In patients with left brain

CONTACT James R. Bateman
jrbatema@wakehealth.edu
James R Bateman was involved in the interpretation of data and drafting/review of the manuscript.Christopher M. Filley was involved in the interpretation of data
and drafting/review of manuscript.Elliott D. Ross was involved in the interpretation of data and drafting/review of manuscript.Brianne M. Bettcher was involved in
the interpretation of data and drafting/review of manuscript.H. Isabel Hubbard was involved in the interpretation of data and drafting/review of manuscript.Miranda
Babiak was involved in the interpretation of data and drafting/review of manuscript.Peter S. Pressman was involved in the interpretation of data and drafting/review
of manuscript.
This article has been republished with minor changes. These changes do not impact the academic content of the article.
© 2019 Informa UK Limited, trading as Taylor & Francis Group

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J. R. BATEMAN ET AL.

damage, reducing the verbal-articulatory demands results in
near-normal improvement for both affective-prosodic repetition and comprehension. In contrast, in right brain damage
reducing verbal-articulatory demands does not result in
improvement for either affective-prosodic repetition and comprehension. The neurology of linguistic prosody is more complex than affective prosody. The most studied aspect of
linguistic prosody is production of prosodic stress in patients
with focal brain lesions (Ross et al., 2013). Both left and right
brain lesions disrupt prosodic stress equally. However, disruption of prosodic stress is not closely related to lesion location
within the right hemisphere or the presence of aprosodias. In
contrast, disruption of prosodic stress is highly correlated with
aphasic non-fluency and lesions injuring the basal ganglia in
the left hemisphere.
Neurodegeneration involving the left frontal operculum
causes the non-fluent variant of primary progressive aphasia
(nfvPPA; Gorno-Tempini et al., 2011; Pressman & GornoTempini, 2015), characterized by progressive motor speech
deficits that have been labeled “apraxia of speech.” Apraxia
of speech is characterized by several speech errors, including
what has been commonly described as a “loss of prosody”.
This loss of prosody, however, has not been specified as being
linguistic or affective. Furthermore, almost all of the acoustic
studies involving “loss of prosody” associated with nfvPPA
(Ballard et al., 2014; Duffy et al., 2017) have measured pauses
and speech rate but not pitch variation, thus assessing linguistic rather than affective prosody.
Focal lesions that acutely damage the right frontal operculum are associated with the syndrome of motor aprosodia (loss of spontaneous affective prosody and affectiveprosodic repetition with preserved comprehension of
affective prosody; Ross & Monnot, 2008). In addition, right
hemispheric damage, including in patients with neurodegenerative disease, has been associated with impaired
ability to intentionally make or imitate facial expressions
of emotion (“affective prosoplegia”; Ghacibeh & Heilman,
2003; Gola et al., 2017) that overlaps with the syndrome of
motor aprosodia. In contrast, buccofacial apraxia tends to
lateralize to the left hemisphere (Kwon, Lee, Oh, & Koh,
2013) and often overlaps with speech apraxia (Botha et al.,
2014; Graff-Radford et al., 2014).
In this case report, we describe a strongly right-handed
patient who presented with progressive language deficits
characterized as a moderate apraxia of speech with “loss of
prosody” consistent with the diagnosis of nfvPPA (GornoTempini et al., 2011). On imaging, he was expected to have
predominantly left fronto-opercular and anterior-superior
atrophy. Instead, his imaging showed predominantly right
frontal atrophy. We initially thought this patient may represent a case of “crossed aphasia” (Spinelli et al., 2015).
However, further history from his wife suggested that his
initial deficits involved emotional expression, and formal
assessment demonstrated severe deficits involving spontaneous affective prosody and affective-prosodic repetition
with relative sparing of affective prosodic comprehension.
He was also unable to intentionally produce facial expressions. Thus, these findings are consistent with his predominantly right-sided atrophy.

Case history
AP is a 58-year-old right-handed man with 18 years of education who was evaluated at the University of Colorado
Neurobehavior Clinic for progressive impairment of speech.
Although his wife reported that he had had a life-long tendency to avoid emotional displays, she stated that over the
previous several years he had become more emotionally flat in
his verbal expression. Because of his increasing emotional
flatness, she had wondered whether he was depressed.
Approximately 1 year before his evaluation, he developed
deficits in speech articulation, especially when pronouncing
multi-syllabic words. This problem led to an evaluation of
bulbar-onset motor neuron disease. However, electrodiagnostic studies were normal. The patient reported no difficulties
with memory, attention, visuospatial processes, or manual
praxis. He continued to work in a high-level technical position
and had not received any complaints about his performance
at work. His written communication remained excellent. Both
the patient and his wife denied mood disturbances or personality changes other than flattening of emotional expression.
On neurologic examination, the patient had stereotypic
random rapid tightening of the corners of his lips, and mild
paratonia in the distal extremities. His posture was somewhat
stooped and there was mild hypomimia. His overall Unified
Parkinson’s Disease Rating Scale (Fahn, Elton, & Committee,
1987) score was 14. The remainder of his neurological examination was normal. On neurobehavioral testing, AP’s language was characterized as nonfluent with impaired
confrontation naming, and impaired verbal agility in the context of intact single-word comprehension and relatively preserved syntactic comprehension. His performance on a brief
sentence repetition task was also impaired, primarily because
of distorted sounds consistent with apraxia of speech. His
score on the Montreal Cognitive Assessment (Nasreddine
et al., 2005) was 24. A brain MRI demonstrated predominant
right frontal atrophy (discussed below). Routine blood tests for
reversible dementia were unremarkable.
To further analyze the neurobehavioral deficits specific to
AP, a comparison case was identified who had nfvPPA and left
greater than right frontoinsular atrophy. This individual is a 68year-old right-handed man with a Mini-Mental State
Examination (Folstein, Folstein, & McHugh, 1975) score of 26,
and 24 years of education. On the Western Aphasia Battery
(WAB; Kertesz, 2007), his fluency score was 5 and his information content score was 9. He was diagnosed with pronounced
apraxia of speech, featuring slow and halting articulation, and
several revisions of phrases (perhaps to help with initiation),
and many instances of poor initiation and groping. His speech
was sometimes unintelligible, and both speech and writing
were agrammatic.

Neuropsychological evaluation
Neuropsychological testing was completed in both patients
(Table 1). AP had impaired abstract thinking, simple attention,
and verbally mediated processing speed, with lesser (but still
mild) impairment in visually mediated processing speed. All
measures of fluency (including nonverbal measures) were at

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Table 1. Neuropsychological results.
Patient ID
Memory
California Verbal Learning Task – Short Form
Learning trial 1 (9)
Learning trial 2 (9)
Learning trial 3 (9)
Learning trial 4 (9)
30-second recall (9)
10-minute recall (9)
Recognition (9)
Benson recall (17)
Benson recognition (Y/N)
Visuospatial
Benson copy (17)
Calculations (5)
Attention, Speed, and Executive Function
Digit span forward
Digit span backward
FAS fluency
Category (animals) fluency

AP

nfvPPA

5 (−2.1)
7 (−0.2)
6 (−4.0)
7 (−3.2)
7 (−1.5)
7 (−0.6)
9 (0.5)
8 (−1.7)
Correct

3 (−4.1)
6 (−1.2)
7 (−2.3)
8 (−1.2)
8 (−0.3)
7 (−0.6)
9 (0.5)
11 (−0.5)
NA

15 (−0.5)
5 (0.3)

14 (−1.5)
3 (−2.6)

4 (−2.7)
3 (−1.8)
12 (−2.9)
16 (−1.1)

3 (−3.5)
2 (−2.6)
1 (−3.9)
4 (−3.1)

FAS = letters F, A, and S; NA = not available. z-Scores in parentheses calculated
from normative data from the University of California San Francisco Memory
and Aging Center (Kramer et al., 2003).

least mildly impaired, and he had mild retrieval deficits in
visual memory. Verbal memory and visuospatial functions
were normal. He also scored well on a face perception task
(12/12) and on a task involving the naming of affective facial
expressions (13/16). The patient with nfvPPA performed similarly on all tasks of abstract thinking and simple attention,
though he performed markedly worse on tasks of lexical and
semantic fluency.

Language evaluation
Speech and language evaluation was completed on both
patients, and included a modified WAB (Kertesz, 2007), a shortform of the Boston Naming Task (Mack, Freed, Williams, &
Henderson, 1992), a syntax comprehension task (Wilson
et al., 2010), and a thorough motor speech evaluation
(Table 2).
Verbal output was recorded and evaluated independently
by two speech-language pathologists (HIH, MB). For patient
AP, both HIH and MB noted the presence of moderate apraxia
of speech, with distorted phonemic substitutions and transpositions, distorted vowels, marked additions, substitutions,
omissions, multiple attempts at words with inconsistent production across attempts, increasing difficulty with phonemic

3

complexity and word length, and abnormal prosody
(described as monopitch). Speech output was diminished,
and short sentences were interspersed with long pauses.
Speech was also mildly dysarthric and characterized by
reduced breath support with monopitch and monoloudness,
errors in speech sound production, and mildly reduced voice
quality. The Apraxia of Speech Rating Scale – Version 1 (ASRS)
(Strand, Duffy, Clark, & Josephs, 2014) score was 30 with 15
items rated. As quantified by performance on the WAB
(Kertesz, 2007), the information content of language output
was intact and fluency was reduced. Structure was simplified
and generally grammatically correct, but there were some
instances of mild agrammatism due to exclusion of function
words such as “to.” The ability to comprehend and produce
both active and passive grammatical statements was preserved. Repetition was impacted by motor speech errors but
appeared to be relatively intact with respect to phonological
short-term memory. He had no evidence of surface dyslexia or
surface dysgraphia, and a modified Pyramids and Palm Trees
task assessing for semantic knowledge was normal (15/15).
In comparison, the nfvPPA patient performed similarly on
the ASRS, scoring 26 with 13 items rated. His fluency was
intact, and his information content was similarly reduced
(see Table 2). In contrast to AP, whose syntactic comprehension was intact, the nfvPPA patient performed worse on this
task, indicating a greater degree of agrammatism.

Communication evaluation: acoustic analysis
Computer-assisted acoustic analysis was performed on speech
samples from AP and the patient with nfvPPA. In addition to
standard linguistic tasks including a motor speech evaluation,
assessment of spontaneous speech, and reading from
a standardized passage (the Grandfather passage), affective
prosodic expression was assessed using the ApBat repetition
task (Ross & Monnot, 2008; Ross et al., 1997). The task calls for
the repetition of a presented series of sounds under three
conditions: sentential, monosyllabic, and asyllabic (i.e.,
decreasing the verbal-articulatory demands). An assessment
of affective-prosodic comprehension using sentential, monosyllabic, and asyllabic utterances was also performed over the
telephone, 8 months after the production and repetition tasks
were done, due to limitations of clinical care.
AP was recorded using the internal microphone on an
encrypted 2015 MacBook Pro using version 2.0.5 of

Table 2. Speech and language tasks.
Patient ID
WAB Spontaneous Speech: Information (10)
WAB Spontaneous Speech: Fluency (10)
WAB Recognition Subtest (60)
WAB Command Comprehension Subtest (80)
WAB Repetition Composite Score (100)
Abbreviated Boston Naming Task (15)
Syntax Comprehension
Apraxia of Speech Rating Scale (ASRS)
Oral Apraxia (Imitation) (14)

AP
9
5
60
80
100
15
22c
30e
11

nfvPPA
9
6
59
80
80
15
17d
26f
7

Norms
10(0)a
10(0)a
NA
NA
NA
14.3 (1.1)a
NA
NA
NA

nfvPPA cohortb
NA
6.24 (2.59)
58.40 (4.49)
66.84 (15.19)
80.92 (20.61)
12 (2.9)
NA
NA
NA

WAB = Western Aphasia Battery; NA = Not Available; MSE = Motor Speech Evaluation; aMonolingual English speaker control values from Milman, Faroqi-Shah, and
Corcoran (2014); bValues from Mandelli et al. (2016); cScore is from short-form version, total 24 items; dScore is from long version, total 48 items; e15 items rated,
maximum score of 60; f13 items rated, maximum score of 52.

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J. R. BATEMAN ET AL.

Audacity® freeware (Audacity Team, 2018) for spontaneous
speech and language tasks. The ApBat was delivered and
recorded through PsychoPy2 software (Peirce, 2007). All
wave files were inspected for noise not originating from the
patient, and, if found, noise was manually removed from each
file in Audacity. The wave files were then analyzed using Praat
software v6.0.29 (Boersma & Weenink, 2018) for differences in
frequency and intensity measures. Pitch tracking errors were
minimized by adjusting pitch floor and ceiling to the values of
q5*0.83 and q65*1.92, which have been shown to be better
estimates of extremes of pitch compared to setting floor and
ceiling values at default parameters (De Looze, 2010; De Looze
& Hirst, 2008). Frequency measures included mean and standard deviations of fundamental frequency in Hertz. These data
were used to calculate the coefficient of variation, also known
as relative standard deviation, which has been used in prior
publications to assess pitch variation (Ross et al., 1997; Vogel,
Maruff, Snyder, & Mundt, 2009). Readings of the Grandfather
Passage were also analyzed using a script developed by de
Jong and Wempe (2009) which quantifies specific time-based
measurements useful in the assessment of apraxia of speech
(Ballard et al., 2014).
Results from the acoustic analysis are displayed in Table 3.
Both AP and the nfvPPA patient demonstrated various impairments, but there were substantial differences. On the affective
repetition task of the ApBat, in which pitch variation was
measured using a coefficient of variation percent (standard
deviation/mean of fundamental frequency in Hertz multiplied
by 100), AP performed markedly worse (z-score = −5.6) on the
sentence repetition task, whereas the nfvPPA patient performed normally on the sentence repetition task (z-score =
+0.7). Furthermore, AP’s performance did not change as verbal-articulatory demand was reduced, whereas the nfvPPA
patient actually became hyperprosodic during the asyllabic
condition, a pattern that may be observed in patients with
left brain damage (Ross & Monnot, 2008). Another major
difference involved speech timing. Although both patients
had impaired speech articulation rates, the rate was substantially lower in the patient with nfvPPA compared to AP. On the
affective prosody comprehension assessment, AP showed mild
impairment on the sentential task (z-score = −1.8) and incremental worsening on the monosyllabic (z-score = −3.6) and
asyllabic (z-score = −3.6) tasks, a pattern that is consistent with
right-brain damage, and can be observed in older adults as
a normal (age-related) impairment in affective prosody

comprehension (Orbelo, Grim, Talbott, & Ross, 2005).
Affective prosody comprehension data were unavailable on
our nfvPPA comparison patient.

Assessments of facial expression and oral apraxia
AP’s spontaneous facial expressions were closely noted
throughout the clinical evaluation. Generally, his spontaneous
emotional facial expressivity was flat, although he sometimes
spontaneously produced a Duchenne smile, a smile involving
the orbicularis oculi in addition to the zygomaticus major
(Ekman, Davidson, & Friesen, 1990). Facial expressions were
recorded on a Samsung HMX-F90 camcorder during dedicated
affective imitation and production tasks. AP was first directed
to express a named emotion and was then shown a picture of
that emotion and asked to imitate it. Emotions included fear,
anger, sadness, happiness, disgust, and surprise. The patient’s
expressed emotions were then reviewed using slow playback
of the video and rated using a previously defined method that
correlates well with the Facial Action Coding System (Gola
et al., 2017). This method involved a subjective categorization
of whether the patient expressed the expected emotion perfectly (2 points), with difficulty (1 point), or not at all (0 points).
Following the test protocol, 0 and 1 are combined to 0, and
a perfect presentation becomes a 1.
Using standardized assessments, AP was able to approximate a smile, especially when provided an image to copy. The
expression of other facial emotions, however, was poorly performed. AP scored 1/6 on a test to produce a facial expression
on command, and 1/6 for imitation of facial expression. By
comparison, a group of nfvPPA patients was reported to perform at 3.9 (z-score = +0.5) for command on this task, and 3.8
(z-score = +0.5) for imitation (Gola et al., 2017). We were
unable to directly compare AP to our nfvPPA patient as measures of facial expression were not available. We also asked AP
to perform a non-standardized assessment of oral apraxia. He
was asked to pretend to sniff, blow out a match, cough,
whistle, lick an ice cream cone, lick peanut butter off the
roof of his mouth, and chew bubble gum. Each item was
scored 0–2, which was then scaled as above for comparison.
On these tests, he scored 5/7 on both spontaneous and imitation tasks, and 11/14 on a brief oral mechanism examination
(investigating basic movements like opening and closing the
jaw and moving the tongue). In summary, using a similar
scoring schema on tests of putative oral apraxia versus

Table 3. Acoustic analysis.
Patient ID
Aprosodia Battery: Repetition
Sentential (mean CoV %)
Monosyllabic (mean CoV %)
Asyllabic (mean CoV %)
Aprosodia Battery: Comprehension
Sentential (# correct out of 24)
Monosyllabic (# correct out of 24)
Asyllabic (# correct out of 24)
Spontaneous Speech (CoV %)
Grandfather Passage (CoV %)
Grandfather Passage: articulation rate (syllable number/phonation time)

AP

nfvPPA

8.5 (−5.6)
10.9 (−4.3)
11.5 (−4.5)

25.94 (0.7)
33.63 (0.8)
51.35 (3.9)

18 (−1.8)
13 (−2.8)
10 (−3.6)
6.3 (−4.3)
4.8 (−4.0)
3.40

NA
NA
NA
4.92 (−3.9)
4.53 (−4.1)
1.01

CoV = coefficient of variation, higher score indicates more variation in pitch; NA = not available; z-scores in parentheses calculated from normative data provided in
Ross and Monnot (2008).

NEUROCASE

5

Figure 1. (a–c) 3T MRI T1-weighted coronal images 1 year prior to our evaluation (1 year after motor speech symptom onset) demonstrating right more than left
fronto-insular and anterior temporal atrophy. (d–f) 3T MRI T1-weighted coronal images 1 year after our initial evaluation (2 years after motor speech onset)
demonstrating progression of right more than left fronto-insular and anterior temporal atrophy. (g–i) A 3T MRI T1-weighted coronal image showing left frontoinsular and perisylvian atrophy. All images are in radiographic orientation.

affective prosoplegia, he achieved 71.4% of the possible
points on oral apraxia, and 16.6% of the possible points on
affective facial expression.

Neuroimaging
A 3.0 T brain MRI 7 months prior to our evaluation was read as
showing mild parenchymal atrophy. However, a detailed
review by our group determined that there was striking focal
atrophy of the right frontal operculum with mild atrophy of
the parietal and temporal operculum and less conspicuous left
side involvement in the same areas (Figure 1(a–c). A repeat 3.0
T brain MRI 1 year after our evaluation found progressive
atrophy of the anterior temporal and insular regions with
posterior progression, again more striking on the right than
the left (Figure 1(d–f)). For comparison, the 3.0 T MRI of the
nfvPPA patient (Figure 1(g–i)) showed significant focal atrophy
of the left frontoinsular regions mild perisylvian atrophy.

Discussion
We have presented the case of a man with a severe deficit in
production of affective prosody and prosoplegia typical of
right brain damage, who presented initially with moderate
apraxia of speech, in the setting of predominant right frontoopercular atrophy. As the patient does not meet probable
criteria for any known conventional diagnosis, we present AP
to illustrate the specific neurobehavioral effects of focal right

frontal neurodegeneration. Detailed analysis of this case,
together with contrasts in a case of nfvPPA, leads us to conclude that aprosodia and prosoplegia in AP reflected initial
right-sided degeneration that was then followed by left frontal
involvement that caused the onset of apraxia of speech, which
precipitated his initial clinical assessment.
AP’s performance on the ApBat differed remarkably
from the performance of a patient with nfvPPA. In left
brain-damaged patients with diminished ability to express
affective prosody, reducing the verbal-articulatory
demands (i.e., moving from sentential to asyllabic tasks
on the ApBat) causes a robust improvement in the repetition of affective prosody, as was observed in the nfvPPA
case. In contrast, in right brain-damaged patients with
diminished ability to express affective prosody, reducing
the verbal articulatory demands does not improve their
performance, as observed in AP. In addition, AP had
poorer mimicry of facial expressions than any performance
previously described in nfvPPA (Gola et al., 2017). Our
patient’s relative sparing of grammar could suggest the
presence of primary progressive apraxia of speech (PPAoS;
Duffy et al., 2015; Josephs et al., 2014, 2012) type II, which
has been characterized as having “loss of prosody.” Here it
is again important to discriminate if the “loss of prosody”
is predominantly linguistic or affective. Because acoustic
analyses in PPAoS have focused on timing (Duffy et al.,
2015; Josephs et al., 2012) rather than measures of pitch
variation, the prosodic deficits described are most likely
linguistic rather than affective (Ross et al., 2013).

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J. R. BATEMAN ET AL.

Given his right frontal and temporal atrophy, one might
have expected AP to meet criteria for bvFTD. While his wife
noted that he had become less emotionally expressive than
usual, both she and the patient denied any other substantial
personality changes. He continued to be actively engaged in
what he enjoyed doing and showed no erosion in empathy or
social graces. He had no obsessions or unusual behaviors
beyond a stereotypical contraction of his mouth musculature.
Mild executive dysfunction was present, but he met no other
bvFTD criteria. Some of his deficits with affective-prosodic
comprehension are reminiscent of the right temporal variant
of frontotemporal dementia (Binney et al., 2016), especially
since and the right temporal lobe has been associated with
impaired production and comprehension of affective prosody
(Ross & Monnot, 2008; Wright et al., 2016). However, AP’s most
prominent deficit involved the production of affective prosody
rather than loss of comprehension. In addition, the right temporal variant is not commonly associated with apraxia of
speech.
If aprosodia and prosoplegia can initially present as distinct
syndromes of emotional expression, apart from any altered
internal emotional experience typical of bvFTD, what could
potentially be interpreted as a personality change may in fact
be no more than diminished ability to express emotion, i.e.,
the difference between not appearing to care versus truly not
caring. Atypical nonverbal behaviors due to neurological disease (e.g. hypomimia in Parkinson’s disease) have been shown
to result in negative first impressions of patients (Hemmesch,
2014), which can adversely impact interpersonal relationships
(Pentland, Pitcairn, Gray, & Riddle, 1987). Alterations in emotional displays are critical but may often be missed as more
obvious clinical features appear with disease progression, such
as aphasia with left frontoinsular involvement, alterations in
comportment with spread to ventral regions and the anterior
cingulate region, or a movement disorder if the basal ganglia
are involved.
Notably, AP was reported as not being particularly emotive
at his baseline. This raises the possibility that he may have
a premorbid right-hemispheric developmental syndrome,
characterized by diminished paralinguistic communication
and social deficits in children (Voeller, 1986, 1995; Weintraub
& Mesulam, 1983). Such a syndrome may have left him more
susceptible to a focal right hemisphere neurodegenerative
process, similar to developmental dyslexia’s relationship to
the logopenic variant of primary progressive aphasia (Miller
et al., 2013; Rogalski, Johnson, Weintraub, & Mesulam, 2008).
As described in AP and in similar cases (Confavreux,
Croisile, Garassus, Aimard, & Trillet, 1992; Ghacibeh &
Heilman, 2003; Graff-Radford, Drubach, Strand, & Josephs,
2012), the clinical detection of aprosodia and prosoplegia
may be accomplished by the systematic screening of all
patients in whom a neurodegenerative disease is suspected.
This goal may be efficiently achieved by asking the patient
to imitate a few different emotional phrases and faces. As
with screening for language deficits, lower frequency emotional expressions (e.g., disgust) are likely to be of higher
yield. If a patient is unable to perform these tasks, a more
detailed assessment of the affective communication is
warranted.

In summary, we have described a patient with striking
focal atrophy of the right greater than left perisylvian
regions and temporal lobes, and particularly of the right
frontal operculum, who does not clearly meet probable
diagnostic criteria for any neurodegenerative disorder, but
whose presentation offers unique insights into brain–behavior relationships. Objective acoustic measures indicate relative sparing of common measures of linguistic fluency, but
with disproportionately severe loss of the ability to produce
affective prosody. Similarly, common measures of oral
apraxia were relatively spared, but with a severe inability
to imitate emotional facial expression. In concordance with
the neuroanatomic understanding of affective communication based on the study of stroke patients, AP has disproportionate atrophy of the right anterior insula and frontal
operculum that can plausibly explain his aprosodia and
prosoplegia. The presence of perisylvian atrophy in the temporal neocortex may explain his milder difficulties with affective-prosodic comprehension. Apraxia of speech is also
present, but in our view was a late development most likely
reflecting disease progression involving the left frontal operculum. We have demonstrated techniques to distinguish
between affective and linguistic communication, and the
detection of aprosodia and prosoplegia even in the setting
of other clinical features that may otherwise obscure
a patient’s earliest and most severe deficits. Whether AP
can be diagnosed with primary progressive aprosodia must
await further investigation with other similarly affected
patients, but his case indicates that including an evaluation
of paralinguistic communication as part of a clinical assessment will lead to an enhanced diagnostic understanding of
a patient’s condition and improve patient care. Thus, we
urge clinicians to add an appropriate assessment of paralinguistic communication, including affective prosody and
processing of facial expressions, to the evaluation of patients
with neurodegenerative disorders.

Disclosure statement
No potential conflict of interest was reported by the authors.

Funding
This research is supported by the Department of Veterans Affairs Office of
Academic Affiliations Advanced Fellowship Program in Mental Illness
Research and Treatment, the Medical Research Service of the W.G. (Bill)
Hefner Veterans Affairs Medical Center, and the Department of Veterans
Affairs Mid-Atlantic Mental Illness Research, Education, and Clinical Center
(MIRECC), as well as the Colorado Clinical and Translational Science
Institute (CCTSI).

ORCID
James R. Bateman

http://orcid.org/0000-0002-3646-9148

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