The FAB

Methods.

Description of the Frontal Assessment Battery (FAB). According to current theories, the frontal lobes control conceptualization and abstract reasoning, mental flexibility, motor programming and executive control of action, resistance to interference, self-regulation, inhibitory control, and environmental autonomy.6,10-14⇓⇓⇓⇓⇓ Each of these processes is needed for elaborating appropriate goal-directed behaviors and for adapting the subject’s response to new or challenging situations—functions that are mediated by the prefrontal cortex. For that reason, the designed battery consists of six subtests, each exploring one of the aforementioned functions related to the frontal lobes. Moreover, these subtests were chosen because the score of each of them significantly correlated with frontal metabolism, as measured in terms of the regional distribution of 18-fluorodeoxyglucose in a PET study of patients with frontal lobe damage of various etiologies.9 The processes studied and the corresponding subtests of the FAB are presented below. The content, instructions and scoring of each subtest are provided in the Appendix. The total scores are calculated by adding the notes of the six subtests. The overall duration of the battery is approximately 10 minutes.

• Conceptualization: Abstract reasoning is impaired in frontal lobe lesions.11 This function is currently investigated by card-sorting tasks, proverb interpretation, or similarities.15 The last task is easier for bedside assessment and scoring. Subjects have to conceptualize the links between two objects from the same category (e.g., an apple and a banana). Patients with frontal lobe dysfunction may be unable to establish an abstract link between the items (i.e., fruit), adhering to the concrete aspects of objects (i.e., both are yellow), or may be unable to establish a link of similarity (i.e., one is round but the other is elongated).

• Mental flexibility: Patients with frontal lobe lesions are specifically disturbed in nonroutine situations in which self-organized cognitive strategies have to be built up.16,17⇓ Literal fluency tasks are unusual, require self-organized retrieval from semantic memory, and are easy to score. Frontal lesions, regardless of side, tend to decrease verbal fluency, with left frontal lesions resulting in lower word production than right frontal lesions.18 In this task, subjects need to recall as many words as they can beginning with a given letter in a 1-minute trial.

• Motor programming: Patients with frontal lobe lesions are also impaired in tasks requiring temporal organization, maintenance, and execution of successive actions.12,13,19⇓⇓ In Luria’s motor series, such as “fist–palm–edge,” less severely impaired patients are unable to execute the series in correct order, whereas the most severely affected are unable to learn the series. Simplification of the task (two gestures instead of three) and perseveration (inappropriate repetition of the same gestures) may be observed.

Sensitivity to interference: Deficits in behavioral self-regulation may be observed in tasks in which verbal commands conflict with sensory information. This occurs in the Stroop test, in which the subject must name the colors of words while inhibiting the natural tendency to read the words. This also occurs in the case of conflicting instructions, in which subjects must provide an opposite response to the examiner’s alternating signal, e.g., tapping once when the examiner taps twice. Thus, subjects should obey verbal commands and refrain following what they see.20 Patients with a frontal lobe lesion usually fail to obey the verbal command and tend to execute echopractic movements, imitating the examiner.14

Inhibitory control: Withholding a response may be difficult for patients with damage to the ventral part of the frontal lobes.21 In tasks anticipated to elicit a false-alarm motor response, these patients are often unable to inhibit inappropriate responses.22 This difficulty in controlling impulsiveness can be assessed with the go–no go paradigm,23 in which the subjects must inhibit a response that was previously given to the same stimulus, e.g., not tapping when the examiner taps twice.

Environmental autonomy: Patients with frontal lobe lesions are excessively dependent on environmental cues.24 Sensory stimuli can activate patterns of responses that are normally inhibited in normal controls. For example, the patient conceives the sight of a movement as an order to imitate (imitation behavior); the sight of an object implies the order to use it (utilization behavior); and the sight or sensory perception of the examiner’s hands compels the patient to take them (prehension behavior). In some cases, the patients can elicit these behaviors even if they have been explicitly told not to do so. These abnormal behaviors (the spontaneous tendency to adhere to the environment) express the lack of inhibition normally exerted by the prefrontal cortex on the activation of patterns of behavior triggered by sensory stimulations.

Results.

Technical properties of the battery. Validation. Concurrent validity. A correlation was found between the FAB scores and the Mattis DRS performance in 121 patients (r = 0.82, p < 0.001). Similarly, the FAB scores correlated with the number of criteria (r = 0.77, p < 0.001) and perseverative errors (rho = 0.68, p < 0.001) achieved in the Wisconsin CST. A stepwise multiple regression was used to evaluate the influence on the FAB performance of the following independent variables: age of patient, MMSE and Mattis DRS scores, and the number of criteria and perseverative errors in the Wisconsin CST. The Mattis DRS score and number of criteria achieved in the Wisconsin CST accounted for 79% of variance in the FAB (F [2,82] = 152.9; p < 0.001; r² = 0.79). Interestingly, age and MMSE scores had no significant influence.

Discussion.

In order to provide a simple tool for assessing frontal lobe function that could be applied by any practitioner, we designed a short assessment battery, the FAB, based on our experience with focal frontal lobe lesions24 and movement disorders associated with striatofrontal dysfunction.4 Other tools have already been designed to evaluate frontal lobe function at the bedside.38-41⇓⇓⇓ A brief assessment of frontal and subcortical functions was proposed for patients with suspected subcortical pathology, but patients with AD scored significantly lower on this scale than those with Huntington’s disease or PD.38 The EXIT 25, an executive interview, correlates not only with tests sensitive to frontal lobe dysfunction but also with the MMSE (r = −0.85). This suggests that the EXIT 25 is also sensitive to functions that are not executive.39 Another brief tool sensitive to executive control, the CLOX (a clock drawing test),40 has been proposed, but only investigates one domain of cognitive function: drawing. Lastly, Ettlin and Kischka41 proposed the “frontal lobe score,” which is, however, not convenient for bedside assessment because it includes tasks such as the Trail-Making Test and takes up to 40 minutes to complete. The FAB is an easy test to administer, requires less than 10 minutes to complete, and is well accepted by patients. The six FAB subtests explore both cognitive and behavioral domains under the control of the frontal lobes, each of them having been shown to be significantly correlated with frontal lobe metabolic activity measured by 18-fluorodeoxyglucose using PET scan.9 Moreover, each subtest is associated with specific areas of the frontal lobes on the basis of neuropsychological, electrophysiologic, and functional arguments: conceptualization with dorsolateral areas,42,43⇓ word generation with medial areas,44,45⇓ and inhibitory control with orbital or medial frontal areas.46,47⇓ Therefore, performance on the six subtests of the FAB can give a composite global score, which evaluates the severity of the dysexecutive syndrome and may suggest a descriptive pattern of executive dysfunction in a given patient.

The FAB presents good metric properties. The study demonstrated good internal consistency (Cronbach’s alpha was 0.78),37 optimal interrater reliability (κ = 0.87), and concurrent validity. Indeed, the FAB score was strongly associated with the performance of patients on the Mattis DRS (rho = 0.82) and Wisconsin CST (rho = 0.77 for the number of criteria), both of which evaluate different cognitive functions under frontal lobe control. These functions include initiation, conceptualization, and attention for the Mattis DRS scale25 and conceptualization and cognitive flexibility for the Wisconsin CST. Several recent studies have demonstrated that performance in the Wisconsin CST is related to functional activity in the prefrontal cortex.42,48-50⇓⇓⇓ In contrast, the FAB score is correlated neither with the MMSE score, a measure of more general cognitive function, nor with age (see the results of the stepwise multiple regression). The battery also presents good discriminant validity, allowing differentiation to be made between control subjects and patients with frontal or subcorticofrontal cognitive impairment. However, the FAB global score does not allow discrimination between patients with predominantly subcortical (PSP) or cortical (FTD) dysfunction. Only two subtests discriminated between these patients to some extent—prehension behavior (more severely impaired in patients with PSP) and similarities (more severely impaired in patients with FTD). This result is not unexpected because patients with frontal and subcorticofrontal lesions usually present similar cognitive deficits and share only subtle neuropsychological differences.51-53⇓⇓

Some points should be stressed, however. Test–retest reliability was not assessed. The anatomic correlation of the different subtests of the battery was derived from data obtained with similar tests, but not from the subtests themselves. Finally, although highly significant correlations were shown between the FAB and tests sensitive to frontal lobe functions, but not between the FAB and MMSE, it would be necessary to demonstrate that patients with non–frontal lobe injuries perform at a higher level than that observed for patients with frontal lobe injuries, to definitively consider the FAB as a measure of frontal lobe dysfunction.

Appendix

Content, instructions, and scoring of the FAB

1. Similarities (conceptualization)

“In what way are they alike?”

A banana and an orange (In the event of total failure: “they are not alike” or partial failure: “both have peel,” help the patient by saying: “both a banana and an orange are...”; but credit 0 for the item; do not help the patient for the two following items)

A table and a chair

A tulip, a rose and a daisy

Score (only category responses [fruits, furniture, flowers] are considered correct)

Three correct: 3

Two correct: 2

One correct: 1

None correct: 0

2. Lexical fluency (mental flexibility)

“Say as many words as you can beginning with the letter ‘S,’ any words except surnames or proper nouns.”

If the patient gives no response during the first 5 seconds, say: “for instance, snake.” If the patient pauses 10 seconds, stimulate him by saying: “any word beginning with the letter ‘S.’ The time allowed is 60 seconds.

Score (word repetitions or variations [shoe, shoemaker], surnames, or proper nouns are not counted as correct responses)

More than nine words: 3

Six to nine words: 2

Three to five words: 1

Less than three words: 0

3. Motor series (programming)

“Look carefully at what I’m doing.”

The examiner, seated in front of the patient, performs alone three times with his left hand the series of Luria “fist–edge–palm.” “Now, with your right hand do the same series, first with me, then alone.” The examiner performs the series three times with the patient, then says to him/her: “Now, do it on your own.”

Score

Patient performs six correct consecutive series alone: 3

Patient performs at least three correct consecutive series alone: 2

Patient fails alone, but performs three correct consecutive series with the examiner: 1

Patient cannot perform three correct consecutive series even with the examiner: 0

4. Conflicting instructions (sensitivity to interference)

“Tap twice when I tap once.”

To be sure that the patient has understood the instruction, a series of three trials is run: 1-1-1. “Tap once when I tap twice.” To be sure that the patient has understood the instruction, a series of three trials is run: 2-2-2. The examiner performs the following series: 1-1-2-1-2-2-2-1-1-2.

Score

No error: 3

One or two errors: 2

More than two errors: 1

Patient taps like the examiner at least four consecutive times: 0

5. Go–No Go (inhibitory control)

“Tap once when I tap once.”

To be sure that the patient has understood the instruction, a series of three trials is run: 1-1-1. “Do not tap when I tap twice.” To be sure that the patient has understood the instruction, a series of three trials is run: 2-2-2. The examiner performs the following series: 1-1-2-1-2-2-2-1-1-2.

Score

No error: 3

One or two errors: 2

More than two errors: 1

Patient taps like the examiner at least four consecutive times: 0

6. Prehension behavior (environmental autonomy)

“Do not take my hands.”

The examiner is seated in front of the patient. Place the patient’s hands palm up on his/her knees. Without saying anything or looking at the patient, the examiner brings his/her hands close to the patient’s hands and touches the palms of both the patient’s hands, to see if he/she will spontaneously take them. If the patient takes the hands, the examiner will try again after asking him/her: “Now, do not take my hands.”

Score

Patient does not take the examiner’s hands: 3

Patient hesitates and asks what he/she has to do: 2

Patient takes the hands without hesitation: 1

Patient takes the examiner’s hand even after he/she has been told not to do so: 0