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ORIGINAL ARTICLE
Year : 2022  |  Volume : 25  |  Issue : 6  |  Page : 1080-1086
 

Exploring novel word learning via fast mapping and explicit encoding in persons with temporal lobe epilepsy


1 R Madhavan Nayar Centre for Comprehensive Epilepsy Care, Department of Neurology, Sree Chitra Institute for Medical Sciences and Technology, Thiruvananthapuram, Kerala, India
2 Department of Speech Language Pathology, All India Institute of Speech and Hearing, Department of Neurology, Mysore, Karnataka, India
3 Institute for Communicative and Cognitive Neurosciences, Thiruvananthapuram, Kerala, India

Date of Submission03-Mar-2022
Date of Decision19-May-2022
Date of Acceptance23-May-2022
Date of Web Publication21-Nov-2022

Correspondence Address:
P Manju Mohan
Speech Language Pathologist, Sree Chitra Tirunal Institute for Medical Sciences and Technology, Medical College Campus, Trivandrum - 695 011, Kerala
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/aian.aian_222_22

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   Abstract 


Objective: To explore novel word learning via fast mapping (FM) and explicit encoding (EE) in temporal lobe epilepsy (TLE). Methods: 16 right and 16 left temporal lobe epilepsy (RTLE and LTLE) patients along with 32 normal controls (NC) underwent learning of 24 novel object name pairs through standard FM and EE techniques. Their learning was assessed via a three-choice alternate delayed recognition task on the day of learning and on the following day. Recognition scores were compared using nonparametric statistics across the groups with P value set at <.05. Results: RTLE and NC performed similarly, while LTLE and NC differed significantly in novel word learning irrespective of the method of encoding. LTLE and RTLE differed in EE-based novel word learning alone. Further, with respect to encoding techniques, all groups performed better on EE compared to FM. The novel word associations learned via FM showed a lesser decline compared to EE following overnight integration in RTLE and NC. Conclusion: Novel word learning via FM did not facilitate learning above EE in TLE patients or NC. But FM-based words could better overcome forgetting following overnight integration in RTLE and NC. Hence, it is possible that FM has the potential to improve retention of novel information following overnight integration in RTLE as in NC. However, its efficacy in improving retention in LTLE needs further evidence.


Keywords: Epilepsy, explicit encoding, fast mapping, forgetting, novel word learning, overnight integration


How to cite this article:
Mohan P M, Menon RN, Goswami SP, Thomas SV, Cherian A, Radhakrishnan A. Exploring novel word learning via fast mapping and explicit encoding in persons with temporal lobe epilepsy. Ann Indian Acad Neurol 2022;25:1080-6

How to cite this URL:
Mohan P M, Menon RN, Goswami SP, Thomas SV, Cherian A, Radhakrishnan A. Exploring novel word learning via fast mapping and explicit encoding in persons with temporal lobe epilepsy. Ann Indian Acad Neurol [serial online] 2022 [cited 2023 Feb 6];25:1080-6. Available from: https://www.annalsofian.org/text.asp?2022/25/6/1080/361553





   Introduction Top


Temporal lobe epilepsy (TLE) has been known to cause significant memory and language difficulties, especially when it affects the language dominant hemisphere.[1–5] According to the material specificity theory, left TLE (LTLE) patients are more at risk to develop verbal memory deficits, while right TLE (RTLE) patients have significant difficulty with nonverbal memory deficits.[6–9] Mesial temporal abnormalities are the primary structural correlates for the memory deficits in TLE patients and there are reports of sleep-based consolidation deficits leading to memory dysfunction in epilepsy patients.[10],[11]

Interventions to improve memory skills are of paramount significance in epilepsy patients as memory and quality of life are positively correlated.[12–14] Recently fast mapping (FM) based novel word learning was noted to improve memory functions in patients with hippocampal amnesia who failed to learn novel words which were explicitly encoded (EE).[15] Moreover, the amnesic patients were able to retain these novel word associations when tested after one week. FM is an incidental and inferential learning method wherein no direct and intentional learning is established between a novel word and its referent. The new learning happens in the background of preexisting knowledge.[16] FM method is purported to encode information directly to anterior temporal lobe (ATL) through an alternate neural pathway bypassing hippocampal-based slow consolidation phase.[15],[16]

Given the above background, the aim of this study was to explore novel word learning via FM and EE in patients with right and left temporal lobe epilepsy (RTLE and LTLE respectively) alongside normal controls (NC). It was speculated that the novel word learning skills of LTLE would be poorer than RTLE and NC due to the lateralization of verbal memory functions in left temporal lobe. Further, it was also hypothesized that since LTLE has impaired explicit memory, FM may improve learning via establishing alternate declarative learning pathway and EE, which utilize hippocampus-based intentional learning, would be beneficial in RTLE and NC.


   Methods Top


Participants

A total of 16 right and 16 left TLE patients along with 32 cognitively normal healthy controls (NC) participated in this study. The participants were matched for age, education, and handedness. TLE was diagnosed based on clinical history, semiology as documented during video electroencephalography (VEEG), magnetic resonance imaging (MRI), and electrophysiological data acquired from VEEG. The MRI and VEEG protocols are well described in previous studies from our center.[17],[18] The diagnoses for all participants were arrived at patient management conferences based on clinical, imaging, and electrophysiological data. All TLE patients had drug-resistant epilepsies and were undergoing comprehensive evaluation with VEEG for surgical treatment of epilepsy. TLE were included on meeting the following criteria: (1) all subjects had to be native speakers of Malayalam (vernacular language used in the state of Kerala, a south Indian state) with a minimum of 12 years of education, (2) all subjects had to be right-handed as evidenced from the Edinburgh Handedness Inventory,[19] (3) all patients should perform adequately on the delayed recall and recognition measures of Rey Auditory Verbal Learning Test (RAVLT) and Wechsler Memory Scale (WMS) paired associate learning that assess explicit memory as detailed previously by Jeyaraj et al.[20] Accordingly, RAVLT delayed recall for right and left side scores were to be within 9.3 +/- 2.7 and 7+/-3, while RAVLT recognition to be within range of 13.7 +/- 1.9 and 13.2 +/- 1.5 for right and left side, respectively. For the WMS paired associate learning test, total scores were to be within 12.81 +/- 4.47 and 11.32+/- 5.48 for right and left side, respectively. In the said study, the authors had carefully recruited mesial TLE patients after controlling for age of onset of seizures, age at evaluation, duration of epilepsy, average seizure score, and average number of antiepileptic drugs. Any patient who scored below the lower range in the said memory tests were excluded as they were expected to have significant learning issues at baseline itself. The neuropsychological tests used in inclusion were peripheral to the intent of investigation and were only used to bring some uniformity with regard to the disease and treatment related variables. TLE were also excluded if they had features of any active psychosis noted in medical records. All patients had clinically normal speech and language skills. After meeting the inclusion and exclusion criteria, 12 male and 20 female TLE subjects were recruited. A similar gender distribution of NC was recruited after confirming normal cognitive performance in ACE- Malayalam. The mean ACE-Malayalam score for NC was 95.21 (with a standard deviation of 2.21). All participants were given written informed consent and were included in the study procedures after getting their consent. The study was approved by the Institute Ethics Committee.

Stimuli

A total of 30 novel words and their exact images were selected from world wide web under the fair use policy. These 30 words were rated to be unfamiliar from a total list of 100 words by 10 cognitively normal healthy Malayalam-English bilingual adults with minimum 18 years of education. Moreover, to ensure that the participants were unlikely to have encountered these words before, all the participants were asked to prerate the words for familiarity on a 5-point rating scale, wherein 5 represented extremely familiar and 0 represented not at all familiar, on the 5-point rating scale. All the participants rated the words “as not at all familiar” prior to the study procedure.

Of these 30 words, 12 words each were randomly assigned under FM and EE conditions. The limited number of stimuli were set because larger stimuli sets are purported to contaminate FM learning.[21] Of the rest of the 6 words, 3 words each were selected for practice sessions for FM and EE conditions.

Encoding phase

In the FM encoding session, participants were informed in advance that they are going to be tested for an assessment regarding the perceptual clarity of a few images. They were informed that they will be shown two images, of which one is familiar and other being unfamiliar and there will be a Yes/no question based on the perceptual characteristics of the images, which they have to answer verbally. Questions were framed such that an equal proportion of yes/no answers were elicited. Thus, a total of 12 words and corresponding images were presented along with a Yes/no question in FM condition. The questions were simultaneously presented in written mode and were also audible. Each presentation lasted for 15 seconds within which participants had to respond, after which the next stimulus followed. Each novel target stimulus was presented twice along with the familiar image of the same category.

In the EE study paradigm, the novel word and the corresponding image were presented simultaneously in both written and auditory modes. Each target was presented for 15 seconds and each target was given two exposures for encoding. Three stimuli each were presented in study trials to familiarize the participants on FM and EE study conditions before the actual FM and EE study paradigms were implemented. All participants were exposed to the FM paradigm first followed by EE paradigm and randomization was not followed. This was done in order to avoid any potential cues that participants derive about learning novel words from EE paradigms and applying them to FM-based learning later on. There is prior evidence that counterbalancing the task order did not influence the encoding procedures or the time-based delays.[22] Again, it was recommended that true learning could be masked by cognitive interferences when the number of stimuli is increased while accommodating for experimental design pressures.[21] Henceforth, counterbalancing was not considered as it could have affected the unintentional learning of FM words. [Figure 1] illustrates the FM and EE encoding conditions.
Figure 1: A representative trial of the fast mapping (a) and explicit encoding (b) paradigms. In FM (a), The Malayalam written and audio format for the yes/no question provided is, “Is there white spots on paca? and in EE (b) the written and audio Malayalam input was the word “babaco”

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Delayed recognition phase on day 1

After a 30-minute interval following each study encoding condition, the participants were invited to undertake a three alternative forced choice recognition task. Like in the encoding phase, FM test phase was conducted before EE test phase. In the test phase, there were 12 runs each in FM and EE condition. In the test phase, each target word stimuli were presented in the center of the computer screen along with the target image and two other foil images. All the images were presented with three response alternatives in three locations along with the numbers, i.e., (1) top-left, (2) top-right, and (3) and bottom center of the screen with the target word written in the center of the screen. The position of the target was counterbalanced across the three response locations of the display. The participants had to tell the number indicating the position of target in the screen. The items were displayed for up to 15 seconds. The patient responses were noted down in the recognition form by the investigator. Of the two foils, one foil would be an image the presenter was exposed to as a novel target during the encoding phase and the other foil would be a familiar image from the same superordinate category of the target. This familiar image was different from the familiar images selected in the FM encoding phase.

Delayed recognition phase on day 2

Delayed recognition phase was conducted on two days, i.e., on the day of encoding (day 1) and on the following day (i.e., day 2).

Testing was carried out between 9 AM and 3 PM on both days, and for every participant, the procedure was completed within 24-26 hours across day 1 and day 2. Participants were not informed about the testing that would take place on the second day, so as to prevent recall expectation affecting memory.[23] The recognition task of FM was followed with EE in all participants. All the patients were tested during long-term video EEG telemetry admission during variable phases of ongoing anti-seizure medication taper. Seizure freedom of 24 hours was mandatory for testing and none of the patients had any seizures recorded between testing (encoding and delayed recognition on day 2). [Figure 2] illustrates the 3 AFC recognition test.
Figure 2: The three alternative forced choice (3AFC) recognition task in fast mapping (a) and explicit encoding (b) with “Paca” and “Babaco” in Malayalam written and audio formats

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[Figure 3] illustrates the experimental tasks and order for FM and EE conditions.
Figure 3: Experimental tasks and order for FM and EE conditions

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Statistical analysis

Statistical tests were appropriately selected on case-by-case basis based on the Shapiro Wilk's test for normality. Whenever the Shapiro Wilk's test for normality noted non-normal distribution (P <.05), nonparametric tests were used. Demographic variables such as age, education, and handedness of the participants of RTLE, LTLE, and NC were analyzed using the Kruskal–Wallis H test and neuropsychological test results of RTLE and LTLE were analyzed using independent t-test. The outcome measures of recognition for both study conditions (FM vs EE) and for both days were compared using nonparametric statistics like Kruskal–Wallis H test and Wilcoxon signed rank tests considering nonnormality and limited sample size. Recognition scores for FM and EE encoded novel words for both days served as the dependent variable, while RTLE, LTLE, and NC served as the independent variables. Effect sizes (r') were calculated using the formula Z/√ n.[24],[25] Further relationship between phenotypes and word learning measures were studied using Pearson's correlation. A P value of <0.05 was considered significant.


   Results Top


Demographic and clinical characteristics

The demographic details of age, years of education, gender, and MRI findings of the TLE patients are provided in the [Supplementary File]. [Table 1] provides the results of Kruskal–Wallis H test with regard to demographic variables, suggesting no significant difference for the groups studied. Further, [Table 2] provides the descriptive measures and comparisons on the neuropsychological tests used in inclusion criteria for RTLE and LTLE along with patient characteristics. [Figure 4] provides the median values of percentage scores for various declarative memory measures of RTLE, LTLE, and NC groups.

Table 1: Comparisons across RTLE, LTLE, and NC for demographic variables

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Table 2: Comparisons of neuropsychological test measures and patient characteristics

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Figure 4: Median percentage scores of RTLE, LTLE, and NC in declarative memory measures

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FM and EE performance among RTLE, LTLE, and NC

Kruskal–Wallis H tests with post hoc comparisons [Table 3] were used to analyze the performance on FM and EE recognition measures across both days for participant groups. These results revealed that at least one pair of groups showed significant differences between each other on all measures considered. Post hoc comparisons revealed RTLE and LTLE showing significant differences on EE measures. LTLE and NC differed significantly in all memory measures irrespective of the type of encoding. RTLE and NC performed similarly across all measures of FM and EE.
Table 3: Kruskal-Wallis test comparing performance on novel word learning across groups

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FM and EE performance within RTLE, LTLE, and NC

To understand the effect of study conditions on declarative memory measures of recognition in RTLE, LTLE, and NC, Wilcoxon signed rank tests were used. It revealed superior memory performance for day 1 recognition (/Z/= 3.44, P =0.001) and day 2 recognition (/Z/= 3.43, P =0.001) for words learned via EE compared to FM in RTLE and NC (day 1 recognition (/Z/= 4.40, P = <.001) and day 2 recognition (/Z/= 4.38, P = <.001). However, EE was leading to superior memory performance when compared to FM in LTLE patients only in the recognition scores of day 1 (/Z/= 3.19, P =.001). On day 2, there were no significant differences between FM and EE recognition scores in LTLE. (/Z/= 0.69, P = 0.49).

FM and EE performance following overnight sleep in RTLE, LTLE, and NC

Wilcoxon signed rank tests were used to compare the overnight performance on recognition scores of words learned via FM and EE in RTLE, LTLE, and NC [Table 4]. In all the three groups, there was a significant decline in the number of words learned via EE between day 1 and day 2. However, words learned via FM showed significant decline only in LTLE.
Table 4: Wilcoxon signed rank tests comparing performance on overnight consolidation across days

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Further, the age of onset/duration of epilepsy, seizure score, and number of AEDs did not reveal any correlation (Pearson's) with the novel word learning measures of FM and EE on either day in any of the patient groups.


   Discussion Top


Our results showed that the novel word learning via FM and EE were poorer in LTLE compared to RTLE and NC as speculated. EE offered superior learning rates over FM among all participant groups contrary to our speculation of FM being beneficial for LTLE. Surprisingly the results also noted that FM led to better overnight retention of novel words in RTLE and NC.

The better word learning of RTLE and NC over LTLE is well explained by the role of dominant and nondominant ATL in semantic processing. Though bilateral ATL support semantic representation and processing, the specific pattern of contribution of ATL scales across both hemispheres with regard to its differential connectivity to lateralized speech and face perception regions. Hence, left and right temporal lobe's greater lateralization to verbal and visual information explains the poorer word learning exhibited by LTLE[26] and comparable performance between RTLE and NC. There are prior reports of similar performance between few patient groups and NC.[15],[27] Hence, it may be concluded that RTLE can learn novel words similar to NC.

Among the methods of novel word learning, EE resulted in better word learning scores than FM, which was consistent with prior studies[22],[27],[28],[29],[30] and reaffirms the more conscious allocation of attentional resources during EE.

On accounting FM, no major difference was noted in FM learning rates of RTLE and LTLE. This could be because of the employment of a wider network involving neocortical association areas, occipital, and prefrontal areas during FM mediated novel word acquisition.[16],[31] These widespread networks involved in FM could have led LTLE to not to deviate widely from RTLE. However, compared to NC, FM learning in LTLE was poorer. This may be because of the prominent role of left hemisphere in mediating verbal memory functions.[32],[33]

Current results did not favor FM to enhance learning in LTLE. Involvement of anterior temporal lobar and temporopolar networks recognized for FM mediation[15],[16] was noted to be affected in some of the patients, which would have contributed to poor FM learning in LTLE. Further as revealed from imaging and histopathological studies in TLE, The structural pathology correlates to epileptogenic foci may not be restricted to circumscribed areas of mesial temporal region but could extend to involve more distal temporal limbic regions such as temporopolar[34],[35] and lateral temporal neocortices.[36],[37] Alternately, the extent of pathology, effect of refractory seizures, and anti-epileptic drugs would have also rendered FM inefficient to promote novel word acquisition in LTLE. On similar lines, neocortical damage in schizophrenia was proposed as a possible reason for the absence of FM advantage over EE.[27] The poor learning via EE in LTLE is consistent with the hippocampal damage common to the LTLE subjects.[15],[16] With regard to RTLE and NC, the deficient learning via FM may be attributed to the much easier learning employed by EE via the hippocampal-mediated intended learning pathway of intact left temporal lobe. FM was reported to be effective only when severe hippocampal damages affect the usual declarative learning routes.[27],[30]

Though time-based delay and sleep brought in an expected decline in recognition scores of words learned via EE and FM in both patient and NC groups, the decline noted for words encoded via FM did not reach statistical significance for RTLE and NC. Similarly, in LTLE also, there was a decline of learned concepts encoded via FM and EE with more pronounced loss for EE. The lesser forgetting of FM-based words was previously noted in schizophrenics also.[27] The differential performance of novel words following overnight integration suggests the possibility for processing differences in FM and EE methods. This finding corroborates the idea of FM leading to rapid encoding to neocortical structures bypassing hippocampus and overcoming the consolidation phase that EE words would need to undergo. Thus, FM and EE may be conceived as two different ways of learning with at least partial modularity on the underlying neural correlates sub serving these functions as well as the processing complexities involved. The slow consolidation phase required for EE words would have resulted in its vulnerability towards forgetting following overnight integration while the ability to bypass this route has rendered FM to be better preserved from forgetting. The reduced overnight forgetting rates noted for FM learning in participant groups can also be discussed on the basis of a recent report that suggested forgetting rates to be reduced when information was encoded via FM leading to better storage of declarative information with reduced learning levels in behavioral tests.[38]

When FM had led to insignificant overnight forgetting in NC and RTLE, not finding the same advantage for LTLE was disappointing. It was reported that the FM memory traces established via an alternate neurocognitive pathway are weak and hypothetical in nature with high susceptibility to cognitive interferences especially if the semantic base is debilitated.[21],[39] LTLE has an exclusive association with impaired verbal semantic memory[1],[2] that would have destabilized FM maintenance in memory for long.

Though FM had not resulted in better learning scores compared to EE, FM learning had been resistant to forgetting at the expense of encoding lesser items. As a premature inference, FM encoding may then be considered adjunct to EE whenever deemed necessary to establish better retention in TLE patients. Additionally, FM paradigm was sensitive to elicit differences in performance with respect to laterality among TLE patients despite a higher cognitive reserve provided by education, and this may armor the clinicians to possibly understand its utility as a presurgical neurolinguistic tool for lateralizing epilepsy. Future studies on FM paradigms may conclusively ascertain this notion in the light of current findings.

The study is however not devoid of limitations. Since the results are novel and preliminary, future research with larger sample size is warranted. Also, since we have only looked at recognition scores and delay across 24-hour period, more stringent forms of memory assessment and retention delays may be looked into.


   Conclusion Top


Our study noted that LTLE had poor novel word learning skills compared to RTLE and NC. We did not find FM to better facilitate novel word learning than EE in RTLE/LTLE or NC but we could demonstrate that FM leads to lesser forgetting compared to EE in RTLE and NC and, hence, has the potential to form more stabilized memory traces at least across a 24-hour interval in TLE patients as in NC. This study also extended evidence to the possible differential neurocognitive mediation and processing involved in the FM and EE methods of novel word learning. It also proved that overnight forgetting of novel words was influenced by the method of encoding.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4]



 

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