Executive Function in Autism Spectrum Disorder

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Neuropsychology
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JoVE Educación científica Neuropsychology
Executive Function in Autism Spectrum Disorder

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10:02 min

April 30, 2023

Descripción

Source: Laboratories of Jonas T. Kaplan and Sarah I. Gimbel—University of Southern California

Attention, working-memory, planning, impulse control, inhibition, and mental flexibility are important components of human cognition that are often referred to as executive functions. Autism spectrum disorder is a developmental disorder that is characterized by impairments in social interaction, communication, and repetitive behaviors. It is a disorder that lasts a lifetime, and is thought to affect 0.6% of the population. The symptoms of autism suggest a deficit in executive function, which may be assessed by specialized neuropsychological tests. By employing several tests that each emphasize different aspects of executive function, we can gain a more complete picture of the cognitive profile of the disorder.

One such task, known as the Wisconsin Card Sorting Test (WCST), is a cognitively complex task used widely in research and clinical studies as a highly sensitive measure of deficits in executive function. It tests a person’s ability to shift attention and tests their flexibility with changing rules and reinforcement.1 In the WCST, a participant is presented with four stimulus cards, incorporating three stimulus parameters: color, shape, and number. The participant is asked to sort response cards according to different principles, changing their sorting criteria based on feedback from the experimenter. Participants try out different rules until they find the correct method for sorting the cards. Patients with executive dysfunction tend to get stuck in the card sorting task, unable to change their sorting strategy. This persistence with an incorrect strategy is called perseveration.

A second task, The Tower of London (ToL) is a test dependent on complex planning, re-evaluation, and updating of planned moves. Individuals with autism have been reported to be impaired on tasks involving planning.2 In the ToL task, individuals must move disks from a prearranged sequence on three pegs to match a goal state in as few moves as possible, following specific rules.

A third task, known as the Stroop test, targets cognitive inhibition. In this task participants are shown a name of a color, written in a different color, and are asked to identify the color the word is written in. For example, in an incongruent condition, the word blue would be written in green. Individuals with inhibition difficulty should not perform as well as typically developing individuals on this task involving inhibition of the written word.

In this video, we show how to administer the WCST, ToL, and Stroop task to compare flexibility, planning, and inhibition in children with autism spectrum disorder and typically developing counterparts, and explore how each of these groups performs on these different aspects of executive function.

Procedimiento

1. Participant recruitment

  1. Autistic population recruitment
    1. Recruit 40 participants, aged 6-18 years, with autism spectrum disorder. Diagnosis of autism can be verified using the Autism Diagnostic Interview-Revised3 and the Autism Diagnostic Observation Schedule.4
  2. Control population recruitment
    1. Recruit 40 participants aged 6-18 years, who are matched in age and intellect with the autistic participant population.
  3. Make sure that the participants have been fully informed of the research procedures and have signed all the appropriate consent forms.

2. Data collection

Figure 1
Figure 1. Four stimulus cards presented on the computer screen. These cards are used as the categories to match each of the 64 cards from the deck. Cards can match based on three rules: number, color, and/or shape.

  1. Wisconsin Card Sorting Test (WCST)
    1. Have the participant sit at a table in front of a computer.
    2. Tell the participant that the game requires the matching of a single card to one of four cards displayed at the top of the screen (Figure 1).
      1. After matching each card, the participant is informed if the correct or incorrect decision was made, based on if they guessed the rule correctly or not (the rules are predetermined for each card match).
      2. The rule is applied for a run of trials (10 correct card placements) and then changed without warning.
    3. Tell the participant:
      1. You have four cards placed face up and a pack of 64 cards to match to them.
      2. There is a rule for matching the cards and you will need to guess what it is.
      3. Your task is to choose which card matches your card, based on the rule in place.
      4. You will be told "correct" or "incorrect."
      5. You can take as long as you like for each decision, but may not change your mind.
      6. You should attempt to get as many right as possible.
      7. From time to time, the rule will change without you being told. You will then need to discover the new rule.
    4. End the task when rules have been followed for 10-card turns six times, or when all 64 cards have been placed.
  2. Tower of London (ToL)
    1. The participant sits at a table in front of a computer.
    2. The computer screen shows a starting configuration of three colored balls that are arranged in a pattern on three different pegs. The screen also shows a goal configuration in which the balls have been re-arranged into a new configuration on the pegs.
    3. Tell the participant:
      1. Preplan a series of moves to reconfigure the start set of balls to the goal set (Figure 2).
      2. Execute the moves one by one, using the computer mouse, using as few moves as possible.
      3. There is no time limit, but once a ball is moved, the move cannot be undone.
    4. End the task when the participant has completed 20 trials.

Figure 2
Figure 2. Tower of London: Starting and final position of the colored balls on the three pegs. Participants are instructed to move balls from a prearranged sequence on three different pegs to match a goal state in as few moves as possible.

  1. Stroop task
    1. The participant sits at a table in front of a computer.
    2. Tell the participant:
      1. A word will appear on the screen. Please say the color that the word is written in (Figure 3).
    3. Present 120 trials, consisting of equal numbers of congruent and incongruent trials.
    4. On each trial, present one of four color words (red, blue, green, or yellow) on the screen for 4.0 s or until a response is made. On half of the trials the ink color matches the word (congruent trials), while on the other half of the trials the ink color does not match the word (incongruent trials).
    5. Wait 1.5 s between each stimulus, and do not repeat the color name or presentation color from one trial to the next.
    6. The experimenter records if each response is correct or incorrect. Incorrect responses will be excluded from the reaction time analysis.

Figure 3
Figure 3. Stroop Test: Examples of a congruent and incongruent stimulus, with correct responses. Participants are instructed to verbally say the color of the word presented.

3. Data analysis

  1. The WCST is scored by the computer according to the WCST manual.5
    1. For this study, the primary index of executive dysfunction used is the number of perseverative responses in which the participant continued to sort based on the previously correct rule despite feedback that it was incorrect.
  2. The computerized version of the ToL is scored automatically based on: time spent preplanning, mean move times, number of moves made, and number of trials solved in the minimum number of moves possible.
    1. For this study, the primary index of executive dysfunction used is number of excess moves, which counts the number of moves made beyond the minimum required to solve the puzzle.
  3. The computerized version of the Stroop test is scored automatically by recording the time of onset of the spoken color name.
    1. The average reaction time for congruent trials is subtracted from the average reaction time for incongruent trials for each participant, excluding incorrect responses.
  4. A t-test can be used to test differences in these scores between autistic and control participants.

Autism Spectrum Disorder is characterized by impairments in communication and executive function, with an onset that is often noted during early childhood.

Across normal development, children improve their executive processes, which include: flexibility—adapting thoughts in response to a changing environment; planning—the actions needed to attain a specific goal, and inhibition—being able to stop what they’re doing

However, in this social situation, the child who showed difficulty executing those functions—the one who didn’t go inside to get a coat because he kept waving a stick around—is an example of someone with components indicative of Autism Spectrum Disorder.

This video demonstrates how to perform a series of behavioral tests that tap into the processes of executive function in the laboratory, as well as how to analyze the data and interpret results in children diagnosed with Autism Spectrum Disorder compared to those without any known developmental disorders.

In this experiment, children with Autism Spectrum Disorder along with typically developing counterparts ages 6 to 18 are asked to complete three tasks—the Wisconsin Card Sorting Test, the Tower of London, and the Stroop Task—that measure different components of executive function.

In the first task, the Wisconsin Card Sorting Test, children are presented with four stimulus cards that incorporate three stimulus patterns: color, shape, and number.

They are asked to sort response cards according to one of these parameters, but the trick here is that they must figure out the sorting rule based on the feedback provided after matching each one.

Participants try sorting by color, shape, or number until they find the acceptable rule, which is applied for a run of 10 correct placements and then changed without warning.

The dependent variable then is the number of responses in which the participant continues to sort based on the previously correct rule, despite feedback that it was incorrect. This is known as perseveration: focusing on the same response even though it may not lead to an advantageous outcome.

The second task is the Tower of London, where participants must move disks from a prearranged sequence on three pegs to match a goal state in as few steps as possible. In this case, the dependent variable is number of moves made that surpass the minimum number necessary.

The third and final task is the Stroop test, where participants are asked to say out loud the colors of presented words. The colored terms are equally divided into either congruent trials—where the name and font color match, or incongruent ones—the two features are mismatched, for example, the word green is colored blue.

Here, the dependent variable is the time it takes for participants to say the correct color. Responses in the incongruent condition tend to be slower than congruent trials because participants must inhibit reading the word, which is fast and automatic, in favor of saying the actual color of the letters.

The symptoms of Autism Spectrum Disorder suggest deficiencies in the executive functions required to complete the three tasks. It is predicted that participants already diagnosed with the disorder will not have the same flexibility as controls with changing rules in the Wisconsin Card Sorting Test.

Likewise, they are also expected to demonstrate poor planning when solving the Tower of London, and reduced cognitive inhibition to correctly complete the Stroop test, compared to aged-matched and typically developing participants.

To begin, greet the recruited participant and have them sit comfortably in front of a computer. Note that all participants should be age- and intellect-matched. After gaining parental approval, guide them through the consent forms.

Now, explain to each participant that they will complete three tasks: first is the Wisconsin Card Sorting Test, where they have to match a single card to one of the four displayed on the screen. Elaborate that the cards can match in either color, shape, or number and that they will be told if their guess was correct or not.

Further inform them that, from time to time, the rule will change without notice and that they will have to discover the switch on their own to get as many as possible correct. Answer any questions they might have.

Then, start the task, and allow the participant time to complete the trials, which depends on either six runs of 10 correct placements or until all 64 cards have been sorted. When the task ends, provide them with a 2-min break.

Once the break is over, have the participant sit down again. Explain that the second task—the Tower of London—involves rearranging the configuration of three colored balls located on three pegs, and that their objective is to match the goal configuration in the shortest number of moves.

Also inform them that they should preplan the series of moves and to remember that a transfer cannot be undone. Following the instructions, allow them to complete 20 trials, using the mouse to execute their intended movements.

After another 2-min break, start the third and final test—the Stroop Task. Explain that in this case, a word will be displayed on the screen for up to 4 s, with 1.5 s in between each, and they are to say out loud, the color that the word is written in.

Note that the computer program logs reaction times based on the onset of the spoken color, over the course of 120 trials. You’ll still need to quickly record the participant’s verbalized responses and whether they are correct or not, between word presentations.

To analyze the data, evaluate each task individually: for the Wisconsin Card Sorting Test, determine the average number of perseveration responses; for the Tower of London, calculate the average number of excessive moves beyond the minimum required to solve each puzzle; and for the Stroop Task, average the difference in reaction times for naming the words in the incongruent compared to the congruent condition.

Plot the results for both control and autistic spectrum individuals across all tasks. First, in the Wisconsin Card Sorting Test, notice that participants with autism were less able to set-shift, or adjust to a new sorting rule mid-task.

In other words, they tended to get stuck in the card-sorting task and were unable to change their sorting strategy, which resulted in more perseverative errors.

In the Tower of London test, the autistic spectrum participants showed a deficit in the ability to solve the puzzle using the minimum number of moves, suggesting impairments in planning.

As for the Stroop test, both groups had the same reaction times, indicating that cognitive inhibition was not affected.

Now that you are familiar with several tests of executive function, let’s look at how such batteries could be used to diagnose and differentiate disorders with cognitive dysfunctions and possibly even lead to rehabilitation in these individuals.

While there are many neurodevelopmental disorders with impairments of executive function, including Autism, ADHD, and Tourette’s Syndrome, they may have differing executive profiles. For instance, as we’ve shown here, those with Autism Spectrum Disorders show deficits in the Wisconsin Card Sorting Test and Tower of London.

In contrast, children with ADHD demonstrate impairments in the Tower of London and Stroop Task, whereas those with Tourette’s Syndrome primarily display deficits in the Stroop Task.

Thus, if specific, yet differential, patterns of cognitive dysfunction can be identified across disorders, series of behavioral measures could be used as indicators during diagnosis.

In addition, understanding the cognitive differences amongst different disorders can lead to the development of more targeted rehabilitation programs, like using transcranial direct current stimulation.

Brain regions can be targeted, like the dorsolateral prefrontal cortex, before and after behavioral tasks. That way, researchers can measure whether stimulation enhances executive function, providing a promising approach for rehabilitating a number of disorders with distinct neural underpinnings.

You’ve just watched JoVE’s introduction to executive function in Autism Spectrum Disorder. Now you should have a good understanding of how to design and run a Wisconsin Card Sorting Test, the Tower of London test and the Stroop test, as well as how to analyze and assess the results.

Thanks for watching!

Resultados

Individuals with autism perform significantly worse on tests of mental flexibility and planning, but do not show a difference from typically developing individuals in tests of inhibition (Figure 4). 6 In the WCST, a test measuring mental flexibility, individuals with autism are less able to set-shift, adjusting to a new sorting rule mid-task (i.e., they make more perseverative errors). Consistent deficits have been found in the total number of categories correctly identified and the total number of errors made (Figure 4, left). The ToL test can be used to examine specific aspects of difficulty in planning. Even though the autistic group was impaired in relation to the control group (Figure 4, middle), this deficit was evident only on puzzles that required longer sequences of moves. On the classic Stroop test of inhibition, autistic participants were not impaired in comparison to typically developing participants (Figure 4, right). In summary, autistic and normally developing children show a difference in performance on tasks of planning and mental flexibility, but not on this task of inhibition.

Figure 4
Figure 4. Performance on the Wisconsin Card Sorting Test (WCST), Tower of London test (ToL) and Stroop task. Participants in the autism group (blue) were more impaired on the WCST and ToL tests, but there was no difference between the autism group and control group (red) in the Stroop task.

Applications and Summary

This cognitive battery of tasks to examine executive function could possibly be used as a diagnostic marker for autism. While there are many disorders of executive function, it is possible that the pattern of performance on different tests examining different components of executive function may lead to a dissociation between different disorders. Executive function disorders such as autism, ADHD, Tourette’s syndrome, and conduct disorder may have differing executive profiles in regard to these, and related, tasks. If a specific, yet differential, profile of executive dysfunction can be identified in these disorders, then it could be possible to use measures of executive function as a marker for the diagnosis of autism. Furthermore, understanding the specific profile of cognitive disabilities in this disorder can help develop more targeted rehabilitation and training programs.

Referencias

  1. Grant, D. A. and Berg, E. A. (1948). A behavioural analysis of degree of reinforcement and ease of shifting to new responses in a Weigl-type card sorting problem. Journal of Experimental Psychology, 38, 404-411.
  2. Ozonoff, S. et al. (1991) Executive function deficits in high-functioning autistic individuals: relationship to theory of mind. J. Child Psychol. Psychiatry 32, 1081-1105
  3. Lord, C., Rutter, M., & Le Couteur, A. (1994). Autism Diagnostic Interview-Revised: A revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. Journal of Autism and Developmental Dis- orders, 24, 659-685.
  4. Lord, C., Rutter, M. L., Goode, S., Heemsbergen, J., Jordan, H., Mawhood, L., & Schopler, E. (1989). Autism Diagnostic Observation Schedule: A standardized observation of communicative and social behavior. Journal of Autism and Developmental Disorders, 19, 185-212.
  5. Heaton, R. K. (1981). Wisconsin Card Sorting Test Manual. Odessa, FL: Psychological Assessment Resources, Inc.
  6. Hill, E. L. (2004). Executive Dysfunction in Autism. Trends in Cognitive Sciences, 8(1), 26-32.

Transcripción

Autism Spectrum Disorder is characterized by impairments in communication and executive function, with an onset that is often noted during early childhood.

Across normal development, children improve their executive processes, which include: flexibility—adapting thoughts in response to a changing environment; planning—the actions needed to attain a specific goal, and inhibition—being able to stop what they’re doing

However, in this social situation, the child who showed difficulty executing those functions—the one who didn’t go inside to get a coat because he kept waving a stick around—is an example of someone with components indicative of Autism Spectrum Disorder.

This video demonstrates how to perform a series of behavioral tests that tap into the processes of executive function in the laboratory, as well as how to analyze the data and interpret results in children diagnosed with Autism Spectrum Disorder compared to those without any known developmental disorders.

In this experiment, children with Autism Spectrum Disorder along with typically developing counterparts ages 6 to 18 are asked to complete three tasks—the Wisconsin Card Sorting Test, the Tower of London, and the Stroop Task—that measure different components of executive function.

In the first task, the Wisconsin Card Sorting Test, children are presented with four stimulus cards that incorporate three stimulus patterns: color, shape, and number.

They are asked to sort response cards according to one of these parameters, but the trick here is that they must figure out the sorting rule based on the feedback provided after matching each one.

Participants try sorting by color, shape, or number until they find the acceptable rule, which is applied for a run of 10 correct placements and then changed without warning.

The dependent variable then is the number of responses in which the participant continues to sort based on the previously correct rule, despite feedback that it was incorrect. This is known as perseveration: focusing on the same response even though it may not lead to an advantageous outcome.

The second task is the Tower of London, where participants must move disks from a prearranged sequence on three pegs to match a goal state in as few steps as possible. In this case, the dependent variable is number of moves made that surpass the minimum number necessary.

The third and final task is the Stroop test, where participants are asked to say out loud the colors of presented words. The colored terms are equally divided into either congruent trials—where the name and font color match, or incongruent ones—the two features are mismatched, for example, the word green is colored blue.

Here, the dependent variable is the time it takes for participants to say the correct color. Responses in the incongruent condition tend to be slower than congruent trials because participants must inhibit reading the word, which is fast and automatic, in favor of saying the actual color of the letters.

The symptoms of Autism Spectrum Disorder suggest deficiencies in the executive functions required to complete the three tasks. It is predicted that participants already diagnosed with the disorder will not have the same flexibility as controls with changing rules in the Wisconsin Card Sorting Test.

Likewise, they are also expected to demonstrate poor planning when solving the Tower of London, and reduced cognitive inhibition to correctly complete the Stroop test, compared to aged-matched and typically developing participants.

To begin, greet the recruited participant and have them sit comfortably in front of a computer. Note that all participants should be age- and intellect-matched. After gaining parental approval, guide them through the consent forms.

Now, explain to each participant that they will complete three tasks: first is the Wisconsin Card Sorting Test, where they have to match a single card to one of the four displayed on the screen. Elaborate that the cards can match in either color, shape, or number and that they will be told if their guess was correct or not.

Further inform them that, from time to time, the rule will change without notice and that they will have to discover the switch on their own to get as many as possible correct. Answer any questions they might have.

Then, start the task, and allow the participant time to complete the trials, which depends on either six runs of 10 correct placements or until all 64 cards have been sorted. When the task ends, provide them with a 2-min break.

Once the break is over, have the participant sit down again. Explain that the second task—the Tower of London—involves rearranging the configuration of three colored balls located on three pegs, and that their objective is to match the goal configuration in the shortest number of moves.

Also inform them that they should preplan the series of moves and to remember that a transfer cannot be undone. Following the instructions, allow them to complete 20 trials, using the mouse to execute their intended movements.

After another 2-min break, start the third and final test—the Stroop Task. Explain that in this case, a word will be displayed on the screen for up to 4 s, with 1.5 s in between each, and they are to say out loud, the color that the word is written in.

Note that the computer program logs reaction times based on the onset of the spoken color, over the course of 120 trials. You’ll still need to quickly record the participant’s verbalized responses and whether they are correct or not, between word presentations.

To analyze the data, evaluate each task individually: for the Wisconsin Card Sorting Test, determine the average number of perseveration responses; for the Tower of London, calculate the average number of excessive moves beyond the minimum required to solve each puzzle; and for the Stroop Task, average the difference in reaction times for naming the words in the incongruent compared to the congruent condition.

Plot the results for both control and autistic spectrum individuals across all tasks. First, in the Wisconsin Card Sorting Test, notice that participants with autism were less able to set-shift, or adjust to a new sorting rule mid-task.

In other words, they tended to get stuck in the card-sorting task and were unable to change their sorting strategy, which resulted in more perseverative errors.

In the Tower of London test, the autistic spectrum participants showed a deficit in the ability to solve the puzzle using the minimum number of moves, suggesting impairments in planning.

As for the Stroop test, both groups had the same reaction times, indicating that cognitive inhibition was not affected.

Now that you are familiar with several tests of executive function, let’s look at how such batteries could be used to diagnose and differentiate disorders with cognitive dysfunctions and possibly even lead to rehabilitation in these individuals.

While there are many neurodevelopmental disorders with impairments of executive function, including Autism, ADHD, and Tourette’s Syndrome, they may have differing executive profiles. For instance, as we’ve shown here, those with Autism Spectrum Disorders show deficits in the Wisconsin Card Sorting Test and Tower of London.

In contrast, children with ADHD demonstrate impairments in the Tower of London and Stroop Task, whereas those with Tourette’s Syndrome primarily display deficits in the Stroop Task.

Thus, if specific, yet differential, patterns of cognitive dysfunction can be identified across disorders, series of behavioral measures could be used as indicators during diagnosis.

In addition, understanding the cognitive differences amongst different disorders can lead to the development of more targeted rehabilitation programs, like using transcranial direct current stimulation.

Brain regions can be targeted, like the dorsolateral prefrontal cortex, before and after behavioral tasks. That way, researchers can measure whether stimulation enhances executive function, providing a promising approach for rehabilitating a number of disorders with distinct neural underpinnings.

You’ve just watched JoVE’s introduction to executive function in Autism Spectrum Disorder. Now you should have a good understanding of how to design and run a Wisconsin Card Sorting Test, the Tower of London test and the Stroop test, as well as how to analyze and assess the results.

Thanks for watching!