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Semantic inhibition and dementia severity in Alzheimer's disease.

It is well known that Alzheimer's' disease (AD) is primarily diagnosed by episodic memory failures, often associated with emotional deficits (Melendez et al., 2019). In recent decades research in the neuropsychological field indicates that the second most important symptom of the early manifestation of AD is a decrease in executive functioning (EF) (Perry, Watson, & Hodges, 2000). EF could be defined as a set of "cognitive skills that are responsible for planning, initiation sequencing, and monitoring of complex goal-directed behaviours" (Royal et al., 2002). EF is a multicomponent construct that can be measured by a variety of neuropsychological tests.

Control of inhibition seems to be more impaired than other executive functions in people with AD (e.g. Amineva, Philips, Delia Sala, & Henry, 2004). Some studies have shown that inhibition impairment is present early in AD and increases gradually (Belanger & Belleville, 2009). The results of a recent meta-analysis using a variety of tasks have indicated inhibitory control impairment in AD, with dementia severity being an important contributing factor in these deficits (Kaiser, Kuhlman, & Bosnjak, 2018). Control of inhibition plays an important role in tasks that require the suppression of automated well-learned responses, and it is necessary when the individual undertakes a novel task or a task that has to be done in a different way. This ability has traditionally been evaluated using the verbal fluency and Stroop tests. However, the use of these tests has received some criticism. For instance, some authors have warned about a possible lack of ecological validity (Burgess et al., 2006; Martyr, Boycheva, & Kudlicka, 2017) because the performance on these tests shows only a modest association with everyday functioning in people with AD. Instead, these authors proposed the use of the Hayling sentence completion test (Burgess & Shallice, 1996), which has a closer resemblance to the inhibition demands of real life (for instance, in conversations or other social interactions). Another advantage of this test is that it is easy to administer, it takes no more than 10 minutes to complete, and individuals with motor or visual difficulties can perform the task.

In the Hayling task the individual is asked to complete 30 sentences with the last word missing. In part 1 (automatic), the word is strongly constrained by the preceding context, (eg, in the sentence "This man has travelled everywhere around the..." the correct response would be "world"). In part 2 (inhibition) the individual must give a word that makes no sense in the sentence context or is unrelated to the target word. For instance, for the sentence "Most sharks attack very close to the...", the participant could give the word "table". Thus, in order to accomplish this task, the individual has to inhibit the most obvious word that fits in the sentence context ("coast") and generate a new unrelated word. In both sections, the number of errors and the response time (RT) are registered. In this task, the error scores are calculated by combining type 1 (when the participant completes the sentence with a word somewhat related to the target word) and type 3 errors (when the individual produces a word that fits the sentence when instructed to produce a word irrelevant to the sentence context) following the classical procedure of giving 1 point to type 1 errors and 3 points to type 3 errors (Burgess & Shallice, 1996). If a subject cannot respond within 60 seconds, this response is considered as type 3 error and 60 seconds is recorded as the latency response. If a subject cannot respond on more than one item the test is considered not appropriated for this individual (as per test manual) and was excluded from the study.

In spite of the interest in the use of the Hayling test in people with AD, the number of related studies is still quite low. Moreover, most of the existing studies used participants with a wide range of dementia severity (mild-to-moderate, Collette, Van der Linden, & Salmon, 1999; Belanger & Belleville, 2009; Belleville, Rouleau, & Van del Linden, 2006, 2007). Another study by Martyr et al., (2017) used early-stages AD participants with the aim to find possible differences between people with AD and people with Parkinson's disease.

The present study investigates semantic inhibition impairment in people with AD, but our aim was to compare mild and moderate stages of AD and to find possible different patterns of deterioration depending on the disease severity. Although the clinical course of AD is gradual, it is useful to distinguish different AD severity levels in order to better understand its progression and develop intervention strategies adapted to each individual. We hypothesized that participants with mild AD would perform quite well on the automatic section but have more difficulties on the inhibition section of the test (compared to healthy controls), whereas the performance of people with moderate AD would be deficient on both parts of the test. We also expected that mild and moderate participants would differ more on type 3 errors (reflecting total failure to inhibit the target word) than on type 1 errors (reflecting partial inhibition deficits). Finally, the associations between the Hayling test measures and other neuropsychological tests routinely used to evaluate dementia in these patients were also examined in this study with the aim to determine which measures of the Hayling task were related to other tests of executive functioning and working memory. We hypothesize that the inhibition part of the test is more related to other cognitive measures than the automatic part. To our knowledge, very few studies have explored this issue.

Method

Participants

The final sample consisted of 31 individuals with AD (15 individuals with mild AD, and 16 individuals with moderate AD). In addition, a sample of 15 healthy elderly individuals made up a control group. They were diagnosed according to the NINCDS-ADRDA criteria (McKhann et al., 1984) and the Diagnostic and Statistical Manual for Mental Disorders-Fourth Edition (DSM-IV) criteria for dementia of the Alzheimer type (American Psychiatric Association, 1994). The two groups were differentiated according to the severity of the illness, mild and moderate, on the basis of the Clinical Dementia Rating scale (CDR, Hughes, Berg, Danziger, Coben, & Martin, 1982). None of them presented clinical symptoms of depression (based on the short version of the Geriatric Depression scale by Yesavage et al., 1984) or other psychiatric disorders. The two groups of AD patients did not differ from the control group in age or years of education. Participants or their relatives gave their written informed consent, which was approved by the institutional review boards of the University.

Instruments

The material consisted of 30 sentences randomly distributed in two parts, automatic and inhibition, with 15 sentences in each part, and 4 sentences used as practice sentences (Table 1). The sentences of the present study had a cloze probability of between 97 and 100% (previously determined on a sentence completion task performed by a group of 189 university students), and the final words (key words) had frequency of occurrence per million values ranging from 24 to 334 and subjective ratings of familiarity ranging from 4.4 to 6.7 according to the EsPal database (Duchon, Perea, Sebastian-Galles, Marti, & Carreiras, 2013). It should be noted that although Perez-Perez et al., (2016) developed a Spanish version of the Hayling task for evaluating healthy individuals, when the present study was conducted this study had not been published yet.

Procedure

All the participants were tested individually in a quiet room. In the first session, they completed the neuropsychological tests. They included a general screening cognitive test (Mini-Mental State examination, MMSE by Folsein, Folstein, & McHug, 1975), a vocabulary test (Boston Naming Test, BNT by Kaplan, Goodglass, & Weintraub, 2001, 12-item version by Serrano, Allegri, Butman, Nagle, & Ranalli, 2001), and classical measures of verbal inhibition (phonological and semantic fluency) and working memory capacity (WM) (word span, alphabetical span, digit span forward, digit span backward and direct and reverse Corsi blocks tasks). In the second session, the participants were presented with the Hayling task. The instructions, procedure, and scoring were the same as in the original test by Burgess and Shallice (1996).

Data analysis

To compare the performance of the three groups on the Hayling test, we conducted two ANOVAs: (a) a mixed 3 x 2 ANOVA, with the RTs as dependent variable, and two independent variables (Group as a between factor: control, mild AD, and moderate AD, and Condition: automatic and inhibition as a within factor); and (b) the same design was used with the error scores as dependent variable. In case of interaction, post hoc simple effects tests and t tests pairwise comparisons with Bonferroni correction were performed when needed. The level of significance was set at p < 0.05. The effects sizes were calculated by means of Eta square ([[eta].sup.2]). Finally, a matrix of product-moment Pearson correlations was computed to determine the relationship between the measures on the Hayling task and the performance on the neuropsychological tests. The IBM SPSS 24.0 version was used for all the statistical analyses.

Results

Mild and moderate AD groups showed significant deficits on all the neuropsychological tests, except for the Corsi cubes test (inverse), where only the participants with moderate AD were deficient (Table 2). Regarding the performance on the Hayling test, response times on the Hayling task are presented in Table 3, which shows that RTs were slower for the two groups of individuals with AD than for controls; in turn, people with moderate AD were slower than those with mild AD. The statistical analysis revealed significant effects for Group (F(2,43) = 10.28, p < 0.01, [[eta].sup.2] = 0.32), Condition (F(1,43) = 68.23, p < 0.01, [[eta].sup.2] = 0.61), and the interaction (F(2,43) = 9.28, p< 0.01, [[eta].sup.2]= 0.30). In order to study this interaction, simple effect tests for each condition between groups, and post-hoc comparisons with Bonferroni correction were performed. The simple effects test showed significant differences between groups for the automatic condition (F(2,43) = 6.98, p < 0.05, [[eta].sup.2] = 0.24), with longer latency responses in the moderate AD group than in the control group (p < 0.05). However, there were no significant differences between controls and mild AD and between mild and moderate AD. The simple effects tests also showed significant differences between groups for the inhibition condition F(2,43) = 9.84, p < 0.01, [[eta].sup.2]= 0.31) with longer latency responses for mild AD than for the control (p < 0.01), moderate AD than control (p < 0.01), and moderate than mild AD groups (p < 0.01). Thus, both AD groups differed from the controls in the inhibition condition but, in the automatic condition, only moderate AD differed from the controls. Mild and moderate AD groups did not differ in the automatic or the inhibition conditions.

Regarding the study of each group, the t test with Bonferroni correction showed significant effect of the condition in the control group (t(1,14) = -5.83, p < 0.01) in the mild AD group (t(1,15) = -5.90, p < 0.01) and in the moderate AD group (t(1,14) = -5.01, p < 0.01) with longer latency responses in the inhibition condition than in the automatic condition in the three cases.

Regarding the error scores, Table 3 shows higher error scores on the inhibition part of the test than on the automatic part, and the difference was greater in the participants with AD than in the control group. The statistical analysis showed significant effects for Group (F(2,43) = 28.27, ,p< 0.01, [[eta].sup.2]= 0.57), Condition (F(1,43) = 37.32, p < 0.01, [[eta].sup.2] = 0.46), and the interaction (F(2,43) = 11.80, p < 0.01, [[eta].sup.2]= 0.35). In order to examine the interaction, the simple effects test of each condition between groups showed significant differences between groups for automatic condition (F(2, 43) = 3.27, p < 0.05, [[eta].sup.2]= 0.13), with a greater number of errors in the moderate AD than in the control group (p < 0.05), but there were no significant differences between controls and mild AD and between mild and moderate AD. The simple effects tests also showed significant differences between groups for the inhibition condition F(2,43) = 23.02, p< 0.01, [[eta].sup.2] = 0.52) with a greater number of errors in the moderate AD group than in the controls (p < 0.01), in the mild AD group than in the controls (p < 0.01), and in the moderate AD than in the mild AD participants (p < 0.01).

Thus, The error scores of the two groups of participants with AD (mild and moderate) differed from the control group in the inhibition condition, but in the automatic condition, only moderate AD differed from controls. Mild and moderate AD groups did not differ in the automatic condition, but they did in the inhibition condition. Considering the number of type 1 errors in the inhibition condition, the one-way ANOVA with Group as a between factor showed significant differences for Group (F(2,43) = 13.42, p < 0.01, [[eta].sup.2]= 0.38). Post-hoc analysis showed significant differences between controls and mild AD (p < 0.01) and between controls and moderate AD (p < 0.01), but not between mild and moderate AD groups. Considering the type 3 errors, there were significant effects of Group (F(2,43 ) = 11.35, p < 0.01, [[eta].sup.2] = 0.35), and the post-hoc test revealed significant differences between controls and moderate AD (p < 0.01) and between mild and moderate AD groups (p < 0.01), but not between controls and mild AD groups. Thus, the moderate AD group differed from controls on both types of errors but the mild AD group differed from controls only on type 3 errors Thus, mild and moderate AD groups differed on type 3 errors but not on type 1 errors.

Regarding the relationship between the performance on the Hayling test and the other neuropsychological tests in people with AD, significant negative relationships were found between the RTs in the automatic condition and the semantic and phonemic fluency tests (p < .05), between the RTs in the inhibition condition and the semantic fluency (p < .05), digit span (p < .01), digit ordering (p < .01), Corsi direct (p < .01) and Corsi inverse tests (p < .01), and between the error scores on the inhibition section and the semantic fluency (p < .05) and alpha span (p < .05). The error scores in the automatic condition only showed significant relationships with digit ordering (p < .05). The full correlation matrix is shown in Table 4

Discussion

This study examines the use of the Hayling test to differentiate dementia severity in people with AD. People with AD presented worse performance in the inhibition condition than in the automatic condition of the Hayling test, as expected based on previous studies using participants with mild-to moderate AD (Belleville et al., 2006; Belanger & Belleville, 2009; Collette et al., 1999). However, the present study aimed to discover whether some of the measures on the Hayling test could differentiate people with mild AD from people with moderate AD. The results revealed that the mild and moderate AD participants did not show the same pattern of performance on the Hayling task. Mild AD participants only showed impairment on the inhibition part of the test, whereas moderate AD participants showed impairment on both the automatic and inhibition parts.

Thus, the present study shows that initiation and suppression abilities are impaired differently in people with AD depending on the AD severity. Well-learned and automated responses might still be preserved in the initial phase of AD, but not in posterior phases. The Hayling test would be an appropriate measure to differentiate between these two cognitive capacities (compared to more traditional inhibitory control tests such as Stroop or verbal fluency tests, which do not make this distinction), and it could be used by clinicians and researchers to better understand the neuropsychological profile of AD in each stage.

Regarding the error responses (type 1 and type 3), in the present study, people with moderate AD differed from healthy controls on both types of errors, which can be interpreted as a complete failure to inhibit the word that fits the sentence. This result agrees with the results by Collette et al. (1999, 2002) and Belanger and Belleville (2009), who found more type 3 errors in people with AD than in healthy older people. The mild AD group differed from the control group on type 1 errors, but not on type 3 errors, which can be interpreted as partial inhibition difficulties rather than complete failure. This result did not completely agree with the findings by Martyr et al., (2017) showing more type 3 errors in AD participants in the early stages than controls. Some differences in the scoring procedure (that study used did not use the standard test scoring protocol) might explain in part these differences.

In the present study, performance on the Hayling test (especially on the inhibition part) correlated with other measures of executive functioning such as semantic fluency and working memory. The relationship with semantic fluency is consistent with results from studies showing more impairment in semantic fluency than in phonemic fluency in people with AD (e.g. Henry, Crawford, & Phillips, 2004, for a meta-analysis). In addition, a decline in WM in people with AD is also frequently observed (Baddeley, Logie, Bressi, Delia Sala, & Spinnler, 1986), although its relationship with inhibitory control, measured by the Hayling task, has only been explored in healthy older individuals (Borella, Ludwig, Fagot, & de Ribaupierre, 2011). The authors obtained results supporting the hypotheses that older individuals with higher WM capacity can maintain a large amount of information active, and that they are more efficient in resisting interference (Sebastian & Mediavilla, 2017). The results of the present study with participants with AD would agree with these hypotheses.

The findings from the present study suggest that the Hayling sentence completion test may be a valuable tool to help clinicians and researchers to assess inhibitory control in people with different degrees of AD severity, offering a different approach from more widely used tests. The results of the present study also suggest that mild and moderate levels of dementia in people suffering from AD can be explored by analysing the errors on the inhibition part of the test. The present study can be considered a first step, and more data are needed to better understand the characteristics and progression of the inhibitory difficulties in people with AD, for instance, with larger sample sizes and through longitudinal studies.

Acknowledgments

This study was supported by the Spanish Ministry of Economy and Competitiveness (Research Grant FFI2017-84951-P).

References

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Teresa Cervera-Crespo (1), Julio Gonzalez-Alvarez (1), and Vicente Rosell-Clari (2)

(1) Universitat de Valencia and (2) Universitat Jaume I Castellon

Received: February 11, 2019 * Accepted: May 17, 2019

Corresponding author: Teresa Cervera-Crespo

Facultad de Psicologia Universitat de Valencia 46010 Valencia (Spain)

e-mail: Teresa.Cervera@uv.es

doi: 10.7334/psicothema2019.40
Table 1 List of sentences of the Hayling task

Automatic section                 Inhibition section

Practice sentences:               Practice sentence:
Hay que tostar el pan por
ambos LADOS (You have to
toast the bread on both SIDES)    Ella lleva el anillo puesto en el DEDO
                                  (She's wearing the ring on her FINGER)
Cada dia desayuno un cafe con
LECHE (I have coffee with
MILK for breakfast every day)     Las plantas se secaran si no tienen
                                  AGUA. The plants will dry out if they
                                  don't have WATER
Test:                             Test:
1. Se saludaron dandose la MANO
(They greeted each other
by shaking HANDS)                 1.E1 abuelo cuida de su NIETO
                                  (The grandfather takes care of his
                                  GRANDSON)
2. El tiene solo 9 anos,
todavia es un NInO (He's only
9 years old. He's just a CHILD)   2. Para leer necesito ponerme las
                                  GAFAS
                                  (I have to put my GLASSES on to read)
3. Se pincharon las cuatro
ruedas del COCHE (All four
tires on the CAR were flat)       3. Los catolicos van los domingos a
                                  MISA
                                  (Catholics go to MASS on Sunday)
4. La gallina pone HUEVOS
(The hen lays EGGS)               4. Con la camara hago una FOTO
                                  (I use the camera to take a PHOTO)
5. El pajaro estaba dentro
de la JAULA (The bird was
inside the CAGE)                  5. A la hora de comer nos sentamos
                                  todos a la MESA
                                  (When it's time to eat, we sit at the
                                  TABLE)
6. Entro cuidadosamente en la
habitacion sin hacer RUIDO
(He entered the room carefully    6. La comida se sirve en un PLATO
without making NOISE)             (Food is served on a PLATE)
7. En otono, de los arboles
caen las HOJAS (In autumn,
trees lose their LEAVES)          7. Se bebio una copa de VINO
                                  (He drank a glass of WINE)
8. Me pongo el anillo en el
DEDO (I am putting the ring
on my FINGER)                     8. Con la llave abro la PUERTA
                                  (I use the key to open the DOOR)
9. No puedo entrar en casa si
no tengo la LLAVE (I can't get
in the house if I don't have the  9. Para coser necesitas aguja e HILO
KEY)                              (You need a needle and THREAD to sew)
10. Cojo el paraguas porque
han anunciado LLUVIA (I'm taking
the umbrella because they         10. Me acuesto en la CAMA (I lie down
                                  on the BED)
said it was going to RAIN)
11. Nadie ha limpiado y esta
todo muy SUCIO (Nobody has
cleaned up, and everything is     11. Me siento en una SILLA (I sit down
                                  on a CHAIR)
very DIRTY)
12. En el mar nadan los PECES
(FISH swim in the sea)            12. El capitan es el ultimo en
                                  abandonar el BARCO (The captain is the
                                  last one to leave the
                                  SHIP)
13. Cuando hace buen dia el
cielo es de color AZUL (When
it's a nice day, the sky is the   13. Fui al dentista porque me dolia un
                                  DIENTE (I went to the dentist because
                                  my TOOTH
color BLUE)                       hurt)
14. El come demasiado y esta
muy GORDO (He eats too much
and is quite FAT)                 14. Un perro tiene cuatro PATAS (A dog
                                  has four PAWS)
15. No puedo andar porque me
he roto una PIERNA (I can't
walk because I broke my LEG)      15. No sale agua aunque he abierto el
                                  GRIFO (I turned on the FAUCET, but no
                                  water comes
                                  out)

Table 2 Demographic and neuropsychological data of the participants

Test                 Control       Mild AD            Moderate AD
                     M (SD)        M (SD)             M (SD)

Age                  77.9 (5.14)   79.1 (6.26)         79.3 (3.16)
Gender (M/F)        8/8           7/8                 8/8
Education (years)    10.57 (4.12)  11.2  (3.85)         8.66 (3.89)
MMSE                 28.66 (2.49)  23.81 (0.91) (**)   22.46 (1.06) (**)
BNT                  10.86 (0.35)   9.68 (0.79) (**)    9.13 (0.74) (**)
Semantic fluency     16.46 (2.47)  13.28 (3.64) (**)    8.80 (3.55) (**)
Phonemic fluency     16.00 (1.41)   9.78 (2.66) (**)    7.10 (1.44) (**)
Word span             4.33 (0.48)   4.11 (1.16) (**)    3.70 (8.84) (**)
Alpha span            3.46 (0.51)   3.35 (0.49) (*)     2.80 (0.78) (**)
Digit span            5.69 (0.63)   4.21 (1.18) (**)    4.40 (0.51) (**)
Digit ordering        3.46 (0.51)   3.07 (0.47) (**)    2.40 (1.42) (**)
Corsi cubes direct    6.84 (0.55)   3.85 (0.66) (**)    3.20 (1.68) (**)
Corsi cubes inverse   4.07 (0.49)   3.28 (1.12)         3.10 (1.66) (*)

Notes: AD = Alzeimer's disease. Mild AD and moderate AD groups were
compared with the older control group (Tuckey test after ANOVA). The
differences between mild and moderate AD were only significant (p
<.001) for the alpha span test. MMSE = Mini-Mental State examination
BNT = Boston Naming Test (**) p<.01, (*) p<.05

Table 3 Descriptive data of participants in the performance on the
Hayling test

                   Controls     Mild AD      Moderate AD
                                M(SD)        M(SD)

RT Automatic       0.88 (0.45)  1.11 (0.18)   1.45 (0.55)
RT Inhibition      2.38 (0.66)  1.11 (0.18)   1.45 (0.55)
Errors Automatic   0.07 (0.26)  1.19 (1.51)   2.53 (4.36)
Errors Inhibition  0.67 (0.48)  6.06 (2.05)  14.00 (9.54)
Type 1             0.07 (0.26)  0.37 (0.50)   1.28 (2.62)
Type 3             0.20 (0.41)  3.87 (2.78)   4.00 (2.77)

Note: AD = Alzheimer's disease, RT = response time

Table 4 Matrix of correlations between Hayling measures (H) and
neuropsychological tests

Measures                     1  2        3         4         5

1. RT Automatic H            -  46 (**)   .41 (*)   .35 (*)   .39 (*)
2. RT Inhibition H              -        -.07      -.04      -.47 (*)
3. Error score Automatic H               -          .03       .34
4. Error score Inhibition H                        -         -.43 (*)
5. Semantic fluency                                          -
6. Phonemic fluency
7. Word span
8.Alpha span
9. Digit span
10. Digit ordering
11. Corsi cubes (direct)
12. Corsi cubes (inverse)

Measures                     6         7         8         9

1. RT Automatic H             .41 (*)  -.08       .11       .03
2. RT Inhibition H           -.26      -.12       .17      -.59 (**)
3. Error score Automatic H    .01       .17       .26       .33
4. Error score Inhibition H  -.29      -.28      -.39 (*)  -.01
5. Semantic fluency           .44 (*)   .56 (*)   .08       .47 (*)
6. Phonemic fluency          -          .44 (*)   .10       .05
7. Word span                           -          .21       .59 (**)
8.Alpha span                                     -          .04
9. Digit span                                              -
10. Digit ordering
11. Corsi cubes (direct)
12. Corsi cubes (inverse)

Measures                     10         11         12

1. RT Automatic H            -.32       -.05 (**)  -.69
2. RT Inhibition H           -.71 (**)   .70 (**)  -.75 (**)
3. Error score Automatic H   -.37 (*)    .18        .24
4. Error score Inhibition H  -.41       -.48       -.21
5. Semantic fluency           .57 (**)   .40 (*)    .21
6. Phonemic fluency           .41 (*)    .40 (*)    .21
7. Word span                  .02        .10        .03
8.Alpha span                  .07        .10        .11
9. Digit span                 .23        .29        .36
10. Digit ordering           -           .85 (**)   .68 (**)
11. Corsi cubes (direct)                -           .86 (**)
12. Corsi cubes (inverse)                          -

(*) p<.05, (**) p<.01
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Author:Cervera-Crespo, Teresa; Gonzalez-Alvarez, Julio; Rosell-Clari, Vicente
Publication:Psicothema
Date:Jul 1, 2019
Words:5188
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