LANGUAGE FUNCTIONS IN PATIENTS WITH EPILEPSY
Ali Rıza SONKAYA* Zeynep Zeliha BAYAZIT** Mustafa Tansel KENDİRLİ*
*GATA Haydarpasa Training Hospital Department of Neurology
**Ankara University Department of Linguistic and Literature
Abstract. Epilepsy, as a chronic disorder, often impacts cognitive skills including language. A correlation between
language impairment and epilepsy is frequently reported. The neuroanatomical underpinnings of processing
lexical semantics and phonology have been investigated in several clinical and imaging studies but it is
unknown whether this language impairment develops gradually as a consequence of epilepsy or precedes
the onset of seizures. In this research, we administered the ‘Ambiguous Word Test’ to 25 epileptic patients
(12 diagnosed with temporal lobe epilepsy, 8 left-sided, 4 right-sided, and 13 diagnosed with idiopathic
generalized epilepsy) and 40 healthy controls. The test assessed their ability to select the appropriate word
to fill out sentences against alternative words that were phonologically or semantically similar to the correct
option. Patients overall produced significantly more mistakes as compared to controls across conditions.
Characteristically, though, patients with temporal lobe epilepsy exhibited significantly more phonological
mistakes than both patients with idiopathic generalized epilepsy and controls. In particular, phonological
processing of verbs was heavily deteriorated in temporal lobe epileptics, while it was preserved in
idiopathic generalized epileptics. These findings are discussed in the light of relevant neurolinguistic
theories and experimental studies, addressing issues on epilepsy and language that require further
investigation.
Keywords: Language functions, phonology, semantics, ambiguity, epilepsy.
INTRODUCTION
The traditional components of language, phonetics, semantics, and syntax, adequately
characterise the structure of language, but are insufficient to explain the richness of meanings that
arise whenever language is used to communicate. The terms speech and language are sometimes
used as synonyms. However, from a linguistic point of view, they are different sides of the same
coin and are inseparably intertwined. Language refers to the cognitive set-up of the sounds of a
language, the rules for their combination into words and sentences and the meaning behind them.
Speech refers to the articulated utterances and the motor act and ability to perform them. Speech
and language are mainly used for communication and this term also incorporates the use and
understanding of social context and meaning. Language is usually described as consisting of
phonology, which means the set-up of sounds and the rules for their combinations into words. It
also consists of lexicon, meaning the vocabulary of a language and the meaning of words, which
is also referred to as semantics. Additionally it consists of grammar, which refers to the
combination of words into sentences, and pragmatics, which means the social use of language, or
communication.
Researchers from different disciplines have previously focused on different aspects of speech and
language disorders. Linguists have studied specific language functions,neurologists have
interested constructive language functions and psychologists have dealt with explanations
regarding the underlying nature, with particular emphasis on different aspects of cognitive
processing capacity. The etiology of alterations in language, phonological, lexical and semantic
disorders varies and may involve factors such as: organic, intellectual / cognitive, environmental
and emotional which most of the time happens to have an interrelationship among all these
factors (Lemos, Barros & Amorim, 2006). From all of them, it is highlighted the role of epilepsy
which recent studies (Svoboda, 2004) has also emphasized the presence of additional disabilities,
but it is unclear how they are related to speech and language disorders. Interrupted cerebral
activity in epileptic conditions results in disturbances in a variety of cognitive functions and may
also affect speech and language development, but it is not known how epileptiform discharges
contribute to speech and language disorders. Research in the area of speech and language
dysfunctions in patients with epilepsy is scarce and the need for speech and language intervention
has not received much attention (Svoboda, 2004).
Epilepsy, as a chronic disorder, frequently impacts cognitive skills including language (Tuchman,
1994; Besag, 2004). Different types of epilepsy may include impairments in distinct language-
related cortical areas, such as the temporal cortex in temporal lobe epilepsy (Pisano et al., 2005)
and the frontal lobes in idiopathic generalized epilepsy (Meencke, 1985;Hommet et al., 2006).
Previous studies have documented atypical language representation in patients with epilepsy
usually by showing atypical language lateralization (Rasmussen & Milner, 1977; Sabsevitz at
al.,2003;Gaillard et al., 2004; Yuan et al., 2006). However, neurolinguistic research on epilepsy
still lacks insight into particular types of language representation and processing. For example
while the involvement of temporal lobe structures in both semantics and phonology has been
amply studied in the relevant literature (Hagoort, 2005; Indefrey & Cutler, 2005), the effects of
temporal lobe epilepsy on such processes remains poorly investigated.In the few studies
conducted so far, effects of temporal lobe epilepsy have been found on semantic interpretation of
visual input ( Schwarz & Pauli, 2009), as well as on phonological and/or reading processes
(Vanass at al., 2003; Vanass at al., 2005). However, the literature still lacks any systematic
attempts to clarify whether epileptic pathology may selectively affect semantic and/or
phonological processing of particular types of linguistic categories. While the neuroanatomical
foundations of the representation of different grammatical classes (noun/verb) and/or semantic
properties (concreteness/abstractness, entityobject/action) predominantly involve frontal and
temporal cortical areas (Damasio & Tranel, 1993; Cappa & Perani, 2003), neurolinguistic studies
on epilepsy have yet to shed light on such topics. Another characteristic case is that of research on
lexical ambiguity resolution. A complex and dynamic process, it has attracted a significant
amount of considerations (Hogaboam & Perfetti, 1975; Onifer & Swinney, 1981; Glucksberg,
Kreuz, & Rho, 1986; Friederici at al., 1998), as well as several clinical and neuroimaging studies,
overall establishing the involvement of a widespread neural network (Price, 2000). Among others,
this network has been shown to involve the perirhinal, entorhinal, and parahippocampal cortices
within the medial temporal lobe (Schmolck, Stefanacci, & Squire, 2000), as well as left dorsal-
lateral frontal areas, the anterior cingulate and the right inferior parietal lobe (Chan et al., 2004).
The present study was thus designed to address these issues by investigating whether aspects of
semantic and phonological processing forwords of different grammatical classes are impaired in
patients with epilepsies that are not surgically treated. From based on this data, we hypothesized
that patients with epilepsy would exhibit difficulties in processing ambiguous words. On the basis
of the significance of the temporal lobe in the storage of linguistic representations, we also
predicted that patients with temporal lobe epilepsy would demonstrate more profound
impairments in both semantic and phonological aspects of language processing.
MATERIALS AND METHODS
The population included 25 patients with an idiopathic or probably symptomatic form of epilepsy
(11 males, 14 females) attending the Department of Neurology at Ankara University and 40
healthy normal controls (18 males, 22 females). After providing informed consent for the
procedures, which were approved by an institutional review board. All participants were
monolingual native speakers of Turkish.
All patients underwent detailed clinico-electrographic investigations (including 24 h – video
EEG)
as well as a 1.5 T brain MRI scan as part of the diagnostic procedure.With respect to their
intellectual level, intelligence status remains relatively intact in epilepsy. However, mild cognitive
decline, including language and memory impairment, is frequently observed (Motamedi
&Meador, 2003) and is ascribed to biological factors (Meador at al., 2001), psychosocial
parameters (Banos et al., 2004) and anti-epileptic drug treatment (Meador at al., 2003). Patient
entry criteria thus included absence of any other neurological or psychiatric disease, as well as a
Mini-Mental State Examination score exceeding 24 points. The two epileptic groups did not differ
significantly in their scores (Wilcoxon W= 240.5, z = 1.58, p =.07, two-tailed). Patients with
hippocampal sclerosis, but no evidence of dual pathology, were also allowed to participate in the
study.
13 patients suffered from idiopathic generalized epilepsy (IGE). Using the International League
Against Epilepsy diagnostic scheme (Engel & ILAE, 2001), 9 patients were diagnosed with
Juvenile Myoclonic Epilepsy, 4 with IGE with generalized tonic–clonic seizures only, while the
rest suffered from other IGE syndromes not better defined. The remaining 12 patients suffered
from temporal lobe epilepsy. These patients were further subdivided into left (8) and right (4)
temporal lobe epilepsy groups, based on seizure semiology, EEG and MRI criteria. With regard to
etiology, 8 patients suffered from probably symptomatic focal epilepsy and 4 patients had medial
temporal lobe sclerosis. All patients were examined at least 72 h from the occurrence of an
absence, myoclonic, simple or complex partial epileptic seizure (CPS) and at least 7 days from a
primarily (p CTC) or secondarily generalized tonic–clonic seizure (s CTC).
Patients and controls were administered the ‘Ambiguous Word Test’ (Roikou et al., 2003). This
tool
has been previously administered in order to test linguistic functions in healthy subjects and
patients with psychiatric diseases (Kouvatsou et al., 2005; Pita at al., 2003). Subjects were
presented with a set of 45 sentences each missing an ambiguous word (henceforth, the ‘target
word’); the context provided by the sentences from which it was excised sufficed to disambiguate
it: 15 sentences were missing the noun (ambiguous nouns subtest), 15 were missing the verb
(ambiguous verbs subtest) and 15 were missing the adjective (ambiguous adjectives subtest), and
were asked to select the appropriate word among three options, in order to form a meaningful
sentence (Roikou et al., 2003). One of the words had the correct meaning according to context
information, as it was synonymous with the omitted target word with respect to its contextually
appropriate sense (correct choice); another corresponded to an alternative meaning of the target
word, which was, however, incompatible with the context (semantic error); a third onewas
phonologically similar to, but semantically unrelated with the target word (phonological error).
All sentences were presented in a written form. For example, the following sentence was
presented (adapted translation from Turkish):
He has ______ manners.
a) Final (phonological error; contextually inappropriate, but phonologically similar to ‘fine’)
b) Delicate (correct choice; contextually appropriate, semantically similar to ‘fine’)
c) Thin (semantic error; contextually inappropriate synonym of ‘fine’)
According to on our assumption that systematic semantic errors would demonstrate failure in
accessing-retrieving the full range of different senses conveyed by the target word, and/or failure
in inferentially processing contextual information to disambiguate the target word, and/or failure
in sufficiently inhibiting the contextually inappropriate sense of the target word, and/or failure in
sufficiently disinhibiting the contextually appropriate one. Apart from this, systematic
phonological errors would likely exhibit failure in accessing–retrieving the phonological
representation of the lexical morphology of the target word, and/or disruptions in more generic
reading-related processes.
The study employed a 3x 3 x 2 between-subjects design, involving the following independent
variables: Group (3; NC, IGE, TLE), Grammatical Class, based on the three subtests–subsets used
(3;Noun, Adjective, Verb), and Error Type (2; Phonological, Semantic). The dependent measure
was accuracy rates, representing the rate of successful avoidance of phonological and semantic
errors, and thus directly reflecting the extent to which phonological and semantic processing was
shown intact in the particular task. For each condition generated by the factorial crossing of the
above variables, accuracy rates were calculated as follows:
Type A Accuracy = Trialsanswered – Type A Errors
Trialsanswered
RESULTS
Semantic and phonological impairments across grammatical classes
TLEs made more errors overall than NCs (three-way ANCOVA: MSe = .021, p < .005; post-hoc:
NC–TLE: p < .0025, one-tailed; rest of ps, p > .1). In particular, they made more phonological
errors than both NCs and IGEs (MSe=.004, p < .00025; post-hoc: TLE–NC: p < .00025; TLE–
IGE: p < .035, one-tailed; IGE–NC: p > .78), as well as more semantic mistakes than NCs ( MSe
=.035, p < .05; post-hoc: NC–TLE: p < .025, one tailed; rest of ps, p > .5; Fig. 1 below).
Fig. 1. Adjusted mean accuracy rates controlling for the effect of education in semantic and phonological conditions among the three
groups, collapsing over grammatical class. TLEs performed poorer than NCs in semantic conditions. In phonological conditions, TLEs
made more mistakes than both IGEs and NCs. NC: Normal controls; IGE: Idiopathic generalized epileptics; TLE: Temporal lobe
epileptics; NS: Non-significant; *: p < .05; ***: p < .0005; error bars represent ±1 S.E.M.
While TLEs made more errors on verbs than NCs and IGEs across error types (MSe = .002, p < .
005; post-hoc: TLE–IGE: p < .025; TLE–NC: p < .0025, one-tailed; NC–IGE: p > .6), they made
even more phonological mistakes for verbs than the other two groups. Indeed, they made more
phonological mistakes than IGEs across grammatical classes, but significantly even more for
verbs. Similarly, they made more phonological mistakes than NCs across classes (p < .00005), but
even more for verbs ( p < .017). This was verified by one-way ANCOVAs, with TLEs making
significantly more phonological errors for verbs (p < .00000025) than both NCs (p < .000025)
and IGEs (p < .0000025, one-tailed; IGE–NC: p > .35).
Furthermore, IGEs, as compared to NCs, showed spared phonological processing for verbs ( p < .
04). Indeed, while the three grammatical classes did not differ with respect to the phonological
mistakes made by NCs (one-way ANCOVA; p < .005; post-hoc: all ps, p > .4) or TLEs
(Grammatical Class: p > .25), they differed for IGEs, who made significantly less phonological
mistakes for verbs than for adjectives and nouns (one-way ANCOVA; p < .005; post-hoc: verbs–
nouns: p < .035; verbs–adjectives: p< .035, two-tailed; nouns–adjectives: p > .65).
Phonological processing of verbs in IGE and TLE
TLEs showed significantly stronger impairments in processing the phonology of verbs, while
IGEs also showed selectively spared performance in this condition (Fig. 2). The selective nature
of these patterns was revealed with a significant Grammatical Class x Error Type x Group
interaction in a three-way ANCOVA (p < .04). Genuinely, no interaction was observed for
semantic errors, but only for phonological ones (p < .00025).
Fig. 2. Adjusted mean accuracy rates controlling for the effect of Education of the three groups for semantic and phonological types of
errors made for the nouns, adjectives, and verbs subsets of the Ambiguous Word Test. Patients showed lower accuracy rates for the
semantic condition than NCs across grammatical classes. TLEs demonstrated lower accuracy rates for the phonological condition
across grammatical classes than both NCs and IGEs, and even more so for verbs. However, IGEs showed spared performance for
phonological processing of verbs. NS: Non-significant; *: p < .05; ****: p < .00005. Error bars represent ±1 S.E.M.
Inorder to examine laterality effects of TLE, the Group variable was redefined so as to involve
right-, left-TLEs, IGEs, and NCs. Both left- and right-TLEs made more phonological mistakes
than NCs ( MSe = .004, p < .001; post-hoc: left TLE–NC: p < .005; right TLE–NC: p < .03, one-
tailed; rest of ps, p >.25), while only left-TLEs made more semantic mistakes than NCs
(MSe=.018, p<.04; post-hoc: left TLE–NC:p<.03, one-tailed; rest of ps, p>.35).With respect to
the strong phonological disruptions for verbs TLEs showed above, both left- and right-TLEs were
less accurate than NCs and IGEs (MSe=.001, p<.000005; post-hoc: left TLE–NC: p<.0005; left
TLE– IGE: p<.00005; right TLE–NC:p<.017; right TLE–IGE: p<.0025,one-tailed; rest of ps,
p>.9; Fig.3 below).
Fig. 3. Adjusted mean accuracy rates (controlling for the effect of Education) for NCs, IGEs, left-, and right-TLEs for semantic and
phonological conditions, collapsing across grammatical classes. While both left- and right-TLEs show impairments in phonological
conditions, only left-TLEs show significantly more semantic mistakes than NCs. NC: Normal controls; IGE: Idiopathic generalized
epileptics; TLE: Temporal lobe epileptics; NS: Non-significant; *: p < .05; error bars represent ±1 S.E.M.
DISCUSSION
Our results extend findings of previous studies with regard to the impact of epilepsy on semantic
and phonological processing, suggesting that both are disrupted in non-operated patients with
epilepsy. These deficits are shown to pertain to language dysfunction caused by the epileptic
process per se, rather than by surgical excision of brain tissue. In particular, the results
demonstrated more errors for the group of temporal lobe epileptic patients in phonological
aspects of linguistic performance than those produced by idiopathic generalized epileptic patients
and normal controls, across grammatical classes. In addition, epileptic patients demonstrated
significantly poorer performance than the control group in semantic ambiguity resolution, with
stronger disruptions for the temporal lobe epileptic group. Separately, while phonological
processing for verbs was spared for idiopathic generalized patients with epilepsy, it was most
impaired for temporal lobe epileptic patients. Finally, while both left- and right-temporal lobe
patients with epilepsy made more phonological errors than normal healthy controls, only left-
temporal lobe ones made more semantic errors.
Let we begin by saying that lexical ambiguity resolution was deficient in epileptic patients. While
only temporal lobe epileptics exhibited semantic deterioration as compared with normal healthy
controls, idiopathic generalized epileptics did not differ significantly from temporal lobe
epileptics. The findings here are compatible with models incorporating broader fronto-temporal
circuits for lexical semantic processing (Hickok, 2009). Different parts of the left middle and
inferior temporal gyri have been considered crucial for lexical-semantic processing (Hagoort,
2005; Indefrey & Cutler, 2005), and conceptual access mechanisms have been proposed to
primarily involve the lateral posterior temporal lobe (Hickok, 2009).
Furthermore, a replication of the study here with larger sample sizes may also yield significantly
poorer performance for idiopathic generalized epileptics as compared to normal healthy controls.
Semantic information is discussed in the relevant literature as being more distributed in the brain
than phonological information. For idiopathic generalized epileptics, cognitive dysfunction, and
deficits in semantic processing in particular are considered to be quite subtle (Motamedi &
Meador, 2003), with a number of studies indicating that these patients’ performance on several
cognitive tasks lies slightly under normal values (Farwell, Dodrill, & Batzel,1985; Mirsky,
Duncan, & Levav, 2001). Even so, neuropsychological and neuroimaging studies provide
evidence for frontal lobe dysfunction in idiopathic generalized epilepsy (Hommet et al., 2006;
Meencke, 1985). Additionally cognitive functions are well established to involve the mediation of
the frontal, especially prefrontal, cortex (Lezak, 1995). Thereby, as long as the processing and
integration of a lexical meaning into a sentence context heavily involves cognitive functions, a
deficit of the prefrontal cortex may compromise semantic processing (Demb et al., 1995; Faust &
Chiarello, 1998; Fiez, 1997; McDonald et al., 2005).
Patients with temporal lobe epilepsy here showed significant phonological impairments as
compared with both idiopathic generalized epileptics and normal healthy controls. This
corroborates the significance of temporal lobes in phonological processing. Besides, the fact that
both left- and right-temporal lobe epileptics showed these impairments corroborates the idea of
the participation and/or the cooperation of both temporal lobes in phonological processes.
Actually, acoustic and phonological processing has been supported to primarily involve the
superior temporal lobe (and sulcus) bilaterally (Okada & Hickok, 2006;Hickok, 2009).
Activations related to phonological properties are primarily reported for the central to posterior
superior temporal gyrus extending into the superior temporal sulcus (Hagoort, 2005; Indefrey &
Cutler, 2005). A fortiori, the left posterior superior temporal gyrus has been found to participate in
accessing lexical phonology independently of semantic access (Graves at al., 2008). It should be
noted, though, that the findings here cannot dissociate between a more general phonological
(Vanasse et al., 2003) and a more modality-specific reading deficit associated with temporal lobe
epilepsy (Vanasse et al., 2005). Moreover, these findings run contrary to imaging studies on
healthy individuals showing relatively greater activation in frontal regions for phonological as
compared with semantic processing (Billingsley at al.,2001 ).
Interestingly, though, the results here are complementary to and compatible with findings on
types of paraphasias in different epileptic groups. In a study comparing the confrontation naming
ability of dominant, non-dominant temporal lobe epileptic patients, and patients with psychogenic
nonepileptic seizures, it was found that while verbal-semantic paraphasias were similar across
patient groups, phonemic-literal paraphasias were significantly more frequent in dominant
temporal lobe epilepsies (Fargo at al., 2005). Most probably, then, our results here obtain the
equivalent pattern in language comprehension, with phonological deficits occurring selectively
for temporal lobe and not idiopathic generalized epileptic patients, and semantic impairments
occurring for the epileptic patient group as compared to normal healthy controls. Another
interesting case has been obtained by Knott and Marslen-Wilson (2001), who examined an
amnesic patient with medial temporal lobe damage: theirword span performancewas normal, yet
their supraspan recall was characterized by a distinctive pattern of phonological errors, where
they recombined phonemes fromthe original list to form newresponsewords, similar-sounding to
the original ones (e.g. ‘life tramp’). These errors closely resemble the phonological ones made by
both right- and lefttemporal lobe epileptics here, as compared to both idiopathic generalized
epileptics and normal healthy controls. Consciously our findings support that phonological
processing of verbs was selectively spared for idiopathic generalized epileptics, while it was most
strongly deteriorated in temporal lobe epileptics, both right- and left-sided. This pattern would
consistent with the idea that phonological processing of verbs basically relies on temporal lobe
structures, in contrast to semantic properties of verbs, which are held to rely on frontal cortical
areas (Damasio & Tranel, 1993;Cappa & Perani, 2003). Presumably, this may be ascribed to the
high complexity of morphology-to-phonology mappings involved in processing verbs. In Turkish,
morphological features of person, number, mood, tense, voice, and aspect are phonologically
instantiated in verbs, whereas nouns and adjectives involve mappings for case. Such heavy load
in processing the phonology of verbs may thus require intact temporal cortical areas for the
efficient application of such mappings – otherwise, the computational burden of retrieving the
correct morphological information for processing verbs would compromise the retrieval of the
correct lexical form.
With respect to the laterality of the observed failures, patients with left temporal lobe epilepsy
made more semantic mistakes than normal healthy controls, while both temporal lobe epileptic
groups made more phonological errors. This is inherently the reverse pattern of that demonstrated
in other researches, where more phonological mistakes are stated in left temporal lobe epilepsy,
while semantic mistakes are encountered both in left and right temporal lobe epilepsy (N’Kaoua
at al., 2001). While several neuropsychological studies have genuinely attributed separate roles to
each cerebral hemisphere in semantic ambiguity processing (Zaidel et al., 1995; Federmeier &
Kutas, 1999; Coney & Evans, 2000; Grindrod & Baum, 2005), it has been also suggested that
both hemispheres play similar roles (Zempleni at al., 2007). In view of the small number of
participants, especially for the right-temporal lobe epileptic patient group, the non-selective
nature of the findings here does not allow us to further discuss the significance of laterality effects
of temporal lobe epilepsy in language processing (Schwarz & Pauli, 2009; Yucus & Tranel,
2007). However, it is worth noting that there have been previous, unexpected findings of
linguistic impairments for right-, and not left-temporal lobe epileptic patients (Billingsley et al.,
2001). Finally, another limitation of the present study to consider in the context of further
experimentation would be the absence of overt matching of normal healthy controls with patients
in measures of intellectual level. For the present study, the level of education was factored in as a
between-subjects variable to minimize any confounds with the group variable, while both patient
groups here scored above average in a mini-mental state examination.
CONCLUSION
Our study evidence was provided for the involvement of temporal lobe epilepsy in phonological
processing, with particular reference to verbs, as well as for the impact of epilepsy on semantic
processing, examined here in the process of lexical ambiguity resolution. The results support a
very significant role of bilateral temporal lobe structures in phonological processes, with more
complex morpho-phonological mappings, such as those of verbs, relying more on those
structures. These findings should optimally be replicated with more diligently matched subject
groups in intellectual and education level, and any marginal effects found here remain to be
further explored.
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