Need to void and attentional process interrelationships

Authors

  • Marylène Jousse,

    Corresponding author
    1. Faculté de Médecine, GRC UPMC 01, Université Pierre et Marie Curie, France
    • AP-HP Groupe Hospitalier Universitaire Est Service de Neuro-Urologie et d'Explorations Périnéales, Hôpital Tenon, France
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  • Delphine Verollet,

    1. AP-HP Groupe Hospitalier Universitaire Est Service de Neuro-Urologie et d'Explorations Périnéales, Hôpital Tenon, France
    2. Faculté de Médecine, GRC UPMC 01, Université Pierre et Marie Curie, France
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  • Amandine Guinet-Lacoste,

    1. AP-HP Groupe Hospitalier Universitaire Est Service de Neuro-Urologie et d'Explorations Périnéales, Hôpital Tenon, France
    2. Faculté de Médecine, GRC UPMC 01, Université Pierre et Marie Curie, France
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  • Frédérique Le Breton,

    1. AP-HP Groupe Hospitalier Universitaire Est Service de Neuro-Urologie et d'Explorations Périnéales, Hôpital Tenon, France
    2. Faculté de Médecine, GRC UPMC 01, Université Pierre et Marie Curie, France
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  • Laurent Auclair,

    1. Inserm, U663
    2. Sorbonne Paris Cité, Faculty of Medicine, Université Paris Descartes, Paris, France
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  • Samer Sheikh Ismael,

    1. AP-HP Groupe Hospitalier Universitaire Est Service de Neuro-Urologie et d'Explorations Périnéales, Hôpital Tenon, France
    2. Faculté de Médecine, GRC UPMC 01, Université Pierre et Marie Curie, France
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  • Gérard Amarenco

    1. AP-HP Groupe Hospitalier Universitaire Est Service de Neuro-Urologie et d'Explorations Périnéales, Hôpital Tenon, France
    2. Faculté de Médecine, GRC UPMC 01, Université Pierre et Marie Curie, France
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  • Registration number CPP Ile de France X: PC/AP 09-2012 N° IDRCB 2011-A00923-38.

Correspondence: Marylène Jousse, Service de Neuro-Urologie et d'Explorations Périnéales, Hôpital Tenon, 4 rue de la chine, 75020 Paris cedex 20, France.

e-mail: marylene.jousse@tnn.aphp.fr

Abstract

Objectives

  • To determine whether a strong urge to void could affect a person's attentional performance.
  • To determine whether an attentional task could decrease a strong urge to void a prospective study was performed.

Subjects and Methods

  • Healthy adults were asked to perform two neuropsychological tests, the modified Paced Auditory Serial Addition Test (mPASAT) and the Psychology Experiment Building Language Continuous Performance Test (pCPT), under two different conditions: no need to void, and a strong urge to void defined by a score of >70/100 mm on a visual analogue scale.

Results

  • In all, 21 healthy volunteers were included.
  • There was no statistical difference between the mPASAT scores from the two sessions (P = 0.57).
  • The mean total error score of the pCPT increased with the individual's urge to void (P = 0.043).
  • The mean omission score decreased, but was not statistically different (P = 0.129), the commission error score increased with the urge to void (P = 0.017), with a shorter reaction time for the inter-stimuli intervals of 1 (P < 0.001) and 2 s (P = 0.036), suggesting a tendency to hurry.

Conclusions

  • A strong urge to void can alter attentional performance, with a tendency to hurry, in healthy volunteers taking part in a sustained attention test pCPT involving the use of the anterior cingulate cortex.

Introduction

The need to void is a bladder sensation that occurs many times a day in healthy people. This sensation is a key component in the continence micturition cycle. It can be altered in many bladder dysfunctions, such as an overactive or neurogenic bladder.

Usually, healthy people can postpone their desire to void, depending on the social situation in which the need occurs. Many individuals have the ability to defer voiding, despite a strong urge, if the circumstances dictate the need to wait. Conversely, a strong desire to void can also prevent people from concentrating or paying attention during activities, e.g. holding a conversation or sitting for an examination.

Over the last 10 years, many imaging studies have taken an interest in the cerebral integration of the sensation of the urge to void. In 2001, using a positron-emission tomography (PET) study, Athwal et al. [1] showed that an increase in cerebral activity of the periaqueductal grey, midbrain stem, and cingulate cortex frontal lobe were associated with an increase in bladder volume, and that increased brain activity relating to decreased urge to void was seen in a different portion of the cingulate cortex, in the premotor cortex and in the hypothalamus. Some of these results were confirmed by Kuhtz-Buschbeck et al. [2].

Some of these areas are not only related to bladder control, but also involved in the attention process. The prefrontal cortex appears to have a particular importance in selective attention (i.e. the ability to focus on certain objects, or stimuli, at the exclusion of others for brief periods) and decision-making processes, whereas the medial and anterior cingulate gyri appear to be involved in activities requiring sustained attention (i.e. also referred to as concentration or vigilance, the maintenance of attention toward a stimulus for a more extended time) [3, 4].

Very few authors have studied the relationships between the need to void and cognitive functions. Harvey et al. [5] recently interviewed focus groups of 25 women on their perceptions of bladder sensation, and the rationale for going to the bathroom. The results showed that in the case of most voids, the decision to void was not based on the sensation itself, but was determined by multiple factors: personal knowledge of the time of the last void, fluid intake, anticipated time until the next void, proximity of a bathroom, and risk assessment or habituated behaviour, all of which involve cognitive functions.

Recently, Lewis et al. [6] found that the sensation of an extreme urge to void was associated with a deterioration in speed performance in attention measurements (Identification task) and working memory (One back task), but not in psychomotor functions (Detection task).

The aim of the present study was to confirm the interrelationship between attention and the need to void in healthy volunteers. We studied variations in the need to void and attentional performance in healthy volunteers, who performed two attentional tests before and after experiencing a strong desire to void, after drinking 500 mL water.

The first hypothesis was that a strong desire to void could be decreased in healthy people following an attentional task. The second hypothesis was that the volunteers’ performance in an attentional test could be significantly altered by a strong need to void, as compared to a situation in which the volunteers felt no need to void.

Subjects and Methods

Healthy volunteers were recruited among the medical students and medical staff working in the authors’ unit at a university hospital, where the experiment was performed.

The volunteers agreed to participate in the study, after reading and signing an informed written consent. Inclusion criteria were: age > 18 years, no urological and neurological history, and no medication except for oral contraception.

All of the volunteers had completed between 2 and 10 years of graduate studies.

Attentional Tests

Two different tests were each performed twice, under two different sets of conditions: the Modified Paced Auditory Serial Addition Test (mPASAT) for 4 s, and a continuous performance test (CPT).

The mPASAT (Test d'attention soutenue: PASAT modifié. Adaptation française. Marseille: Solal; (2003) [7]) comprises an auditory series of 61 numbers from one to nine, which are played back at a constant rate of one number every 4 s. The task consists in adding the last number heard to the second-to-last number. The numbers are presented in sequence, so that the sum of any given pair never exceeded 15. The number of correct responses was recorded (mPASAT maximum score 60). This test assesses information processing speed and/or working memory [8], and activates the left frontal and parietal areas [9]. The total duration of the test is 4 min.

The Psychology Experiment Building Language (PEBL) Continuous Performance Test (pCPT) is part of the PEBL: Psychology Experiment Building Language, which is freely available over the internet and is based on the Conner's CPT (Conners C.K., Conner's Continuous Performance Test, Multi-Health Systems, Toronto, Canada [10]). In this test, letters of the alphabet appear on a screen and the subject must push on the space-bar as quickly as possible when a letter appears (Go-event), except for the letter ‘X’ (No-Go event). Letters were presented with an inter-stimulus interval (ISI) of 1, 2 or 4 s. The mean reaction time was calculated for each rate of appearance. The omission errors (i.e. when the subject failed to push the space bar when a target letter was presented), as well as the commission errors (i.e. when the subject pushed the space bar, but a letter X (No-Go event) was presented) were calculated for each rate of appearance. The total duration of this test was 14 min.

The CPT is one of the most widely used psychological tests for the study of sustained attention. This defines the individual's ability to maintain a high-level of vigilance for a long period, allowing the subject to react to unpredictable events.

Tana et al. [11] studied the brain areas associated with CPT and found blood-oxygen-level dependent (BOLD) activation in the cingulate, temporal, and occipital cortical regions, and in the cerebellum. The strongest brain activation was located in the right anterior cingulate cortex (ACC).

Need to Void Measurement

Each volunteer's need to void was monitored by the volunteer using an electronic visual analogue scale (VAS), ranging from zero (no need to void) to 100 mm (maximum need to void), connected to a Biopac labpro MP35, from Biopac® Systems Inc.

The VAS was chosen to measure bladder sensation because of its ease of use. Patients are accustomed to using this scale to measure pain, and it has already been used in a few studies [12-14]. Dompeyre et al. [12] used a VAS during cystometry in women, and reported a good correlation with the initial sensation of the need to void, and with the subjects’ maximum cystometric capacity. Lowenstein et al. [13] used the Urgeometer, a very similar device to the VAS described here, for bladder sensation monitoring during filling cystometry in patients and controls. The mean urgeometer level for all patients rose significantly during bladder filling, with an initial desire to void occurring at 21/100 ± 18, a strong need to void occurring at 68/100 ± 27, and maximum cystometric capacity (MCC) occurring at 85/100 ± 21 on the urgeometer (P < 0.001). The urge sensation at 50% of MCC was correlated with the Urogenital Distress Inventory score and the Medical Epidemiological and Social Aspects of Aging urge subscales (ρ 0.34, P < 0.03 and ρ 0.39, P < 0.02).

Based on these data, it was decided to make a threshold at 70/100 mm on the VAS. A strong need to void, but not maximal bladder capacity, was required.

Procedure

All of the tests were performed in a quiet room before midday. The volunteers were asked to urinate to begin the test with an empty bladder and no desire to void.

They were seated comfortably and the two attentional tests were performed for the first time. The volunteers were then asked to drink 500 mL water and to quantify their need to void on the VAS until they reached 70/100 mm, as a strong need to void but not maximal bladder capacity, was required for the second session. The attentional tests were then performed for the second time. The volunteers were asked to quantify their need to void, and then underwent uroflowmetry. During the interval between the two attentional tests, the volunteers were asked to work on a computer.

Ethical Considerations

The local ethics committee approved the present study.

Statistical Analysis

Descriptive statistics were used to describe the population, and a paired Student's t-test was used to compare the results of the first and second attentional tests.

Results

In all, 21 healthy volunteers including 14 women and seven men participated in the study. Their mean (sd; range) age was 23.57 (4.19; 20–32) years.

Three volunteers notified a significant decrease in their need to void after the final attentional test, with a need to void score reaching 50/100 mm. Eight volunteers described no change, or a small change (VAS variation < 10 mm), in their need to void. Ten volunteers notified a significant increase in their need to void after the final attentional test, with a mean (sd; range) need to void score equal to 85.2/100 (3.33; 80–90) mm (Fig. 1). The mean (sd; range) voided volume was 531.2 (134.2; 291–847) mL (Fig. 1).

Figure 1.

The need to void evolution of the 21 volunteers.

For the mPASAT results, the mean correct response score was 56.52/60 (range 48–60; sd 3.23; median 58) for the first session, and 57.04/60 (range 51–60; sd 2.67; median 57) for the second session and were not statistically different (P = 0.57).

For the CPT, during the first session the mean (sd; range) total error score was 7.38/324 (4.96; 0–18), the mean omission error score was 0.90/324 (1.14; 0–3), and the mean commission error score was 6.48/324 (4.40; 0–15).

During the second session, the mean (sd; range) total error score was 9.81/324 (6.32; 0–23), the mean omission error score was 0.57/324 (0.68; 0–2), and the mean commission error score was 9.24 (6.0; 0–23). The mean total error score on the pCPT was higher during the second session and statistically different from that of the first session (P = 0.043). The mean omission score tended to decrease with an increasing need to void, but was not statistically different (P = 0.129). The commission error scores were statistically different (P = 0.017), with a higher score associated with a stronger need to void, and shorter reaction times for an ISI of 1 s (P < 0.001) and 2 s (P = 0.036). The mean reaction times for an ISI of 4 s also decreased, but were not statistically different (P = 0.051). The results are summarised in Table 1.

Table 1. mPASAT and pCPT results
 Score (95% CI)Student's paired t-test
No need to voidStrong need to voidP
mPASAT   
Mean mPASAT score/6056.52 (55.1–57.9)57.04 (55.9– 57.9)0.57
pCPT   
Mean total error/247.38 (4.2–10.5)9.81 (5.6–14)0.043*
Mean omission error0.90 (0.5–1.3)0.57 (0.3–0.8)0.129
Mean commission error6.48 (3.7–9.2)9.24 (5.2–13.2)0.017*
Mean reaction time at an ISI of:   
1s391.8 (367.8–415.8)358.2 (205–511.5)<0.001*
2s421.3 (385.6–457.1)396.9 (227.2–566.7)0.036*
4s459.9 (414.9–504.9)438.9 (251.2–626.6)0.051

The higher total commission score, associated with shorter reaction times and a stronger need to void, indicates the volunteers’ tendency to be in a hurry under such conditions.

Discussion

This is the first study describing an alteration in healthy volunteers in attentional performance with an increase in total pCPT error score associated with an increase in the need to void. The higher commission error score and shorter reaction times with the pCPT provide evidence of a tendency to hurry, associated with a strong urge to void.

Very few authors have studied the relationships between the need to void and cognitive functions. Morris [15] compared bladder diary, Bladder Sensation Intensity Score, Attentional Demands Survey (measures attentional demands in four domains: physical environment, informational, behavioural, and affective demands) and performance on several neuropsychological tests (Operation and Reading Span, Wisconsin Card-Sorting, Stroop Colour Reading, Map Planning, and Maze Speed tests) in 100 women with urge incontinence and 100 continent women at baseline. No differences were found in the neuropsychological tests. These tests were performed with an empty bladder. Only bladder diary data, Bladder Sensation Intensity Score and total score of Attentional Demands Survey differed between the two groups. Changes in the neuropsycological test with the intensity of bladder sensation were not assessed. Conversely, Lewis et al. [6] observed in eight healthy volunteers, with an increase of urge intensity, a deterioration in the speed of performance in attention measurements (Identification task) and working memory (One back task), but not for psychomotor function (Detection task), whereas the performance itself remained unchanged.

Surprisingly, Tuk et al. [16] found in a Stroop Test-based study that response times in the colour-naming blocks (task requiring inhibition of the dominant response, i.e. reading) decreased with increasing urinary urgency, whereas urination urgency had no effect on response times in the word-meaning blocks (dominant response which does not require response inhibition). In second and third studies based on intertemporal decision making (participants had to choose between a smaller and immediate reward or a larger but differed reward) Tuk et al. [16] observed an increased impulse control (choosing the larger and deferred reward) with increasing urinary urgency. They suggested that inhibition of a visceral signal (urinary urgency) could facilitate impulse control in unrelated domains.

In the present study, the attentional tests were chosen because of their weak learning effect and their short test duration, which are advantageous when they need to be repeated. The PASAT is widely used to study the working memory, the speed of information processing, sustained attention in multiple sclerosis [17, 18] and other neuropsychological pathologies [19-21] . It involved the left frontal and parietal lobes. It was expected that the same PASAT results would be found for strong and no desire to void, firstly because, despite its excellent inter- and intra-rater reliability [22], this test can be influenced by practice, and secondly because the brain areas involved in the PASAT are less specifically involved in bladder sensation and micturition control.

The CPT is one of the most widely used psychological tests for the study of sustained attention. Tana et al. [11] studied the brain areas associated with CPT and found BOLD activation in the cingulate, temporal, and occipital cortical regions, and in the cerebellum. The strongest brain activation was located in the right ACC.

The ACC is known to play an important role in attentional processing by modulating target selection (i.e. focusing attention) [23], motor response selection, error detection, and performance monitoring [24]. It is also involved, together with the premotor cortex, in selective attention control in the presence of conflicting tasks [25].

Recently, several functional MRI (fMRI) and PET studies [1, 2, 26] have revealed ACC and premotor cortex involvement in bladder sensation integration, such as an increase in bladder volume and the need to void, with different activation patterns in healthy volunteers and patients with overactive bladder [27].

The present results suggest that in the presence of a strong urge to void, healthy volunteers no longer paid any attention to the ‘X’ or ‘not-X’ stimulus, and pushed on the space bar as quickly as possible, to complete the test and be free to go to urinate. Their ability to inhibit their response was weaker. These results suggest that the ACC is involved both in sustained attention and in the perception of the need to void, resulting in poorer CPT performance.

As a strong need to void can disrupt attentional processes in healthy volunteers, it would be interesting to study the attentional performance of patients with overactive bladder when they are experiencing an urgent need to void.

If the ACC seems to have a major role in attentional control in the presence of conflicting tasks, e.g. bladder control, other brain areas could be involved. In animal models, the Barrington nucleus, orbitofrontal cortex and ACC had several projections toward the locus coeruleus (LC) and recently Rickenbacher et al. [28] studied LC and cortex activation in rats with partial bladder obstruction. They found an elevation of tonic activity of the LC associated with cortical electroencephalographic activation. The LC is part of the noradrenergic system, and has several projections all over the brain [29]. The LC is involved in arousal, alertness, sleep–wake cycle and in facilitating decisions related to task-directed behaviour [30]. Phasic LC activation is supposed to be associated with good performance in tasks that require selective attention, whereas tonic LC activation is thought to favour disengagement from ongoing tasks involving focused attention and to promote scanning of the environment for alternate strategies [31].

Rickenbacher et al. [28] suggested that LC tonic activation elicited by bladder pressure serves to increase arousal and facilitate disengagement from ongoing behaviour and a shift to elimination-related behaviour in rats. The role of the LC in bladder control has been studied less in humans.

One limitation of the present study is the absence of bladder volume measurement. The volunteers’ bladder volumes before the tests were not measured because bladder scans tend to have a low accuracy. Forced diuresis with the intake of 200 mL water every 10 min, as was used in the study of Heeringa et al. [32], could have been used to standardise diuresis measurements between volunteers. As, according to Harvey et al. [5], urination is influenced by the individual's knowledge of fluid intake, a more typical daily lifestyle was chosen.

Some volunteers notified a decrease or no modification in their need to void, whereas their bladder volumes had probably increased (time spent on the attentional test: 18 min), whereas others described an increased desire to void. If these results are suggestive of inter-individual variations in the ability to postpone or reduce the need to void, caution should be taken when interpreting them, given the probably different diuresis between the volunteers, which was not assessed. The results could also have been different if a lower threshold, e.g. 50 or 60/100 mm had been selected. An individual's ability to postpone the need to void probably depends on his/her perceived intensity of bladder sensation.

Another limitation is the absence of follow-up in the three patients who had a decrease in their bladder sensation. If they had been asked to postpone voiding until their need again reached 70/100 mm, this could have provided greater insight into the delay permitted by the attentional task. It would have been also interesting to verify in all volunteers the normalisation of attentional scores after voiding.

The results of the present study suggest that there are two-way interactions between attentional processes and the need to void, such that in a situation, e.g. driving, when it is necessary to inhibit a strong need to void, attentional performance can be altered with an increased risk of error or accident. In some subjects, performing an attentional task can lead to a variation in their need to void.

Further studies are needed to confirm these results in healthy volunteers and to compare them with patients with overactive bladder, in whom an increased AAC activation associated with the urge to void have already been observed [33].

In conclusion, a strong urge to void can alter attentional performance, with a tendency to hurry in healthy volunteers, in particular in the case of a sustained attention test involving the ACC, a brain area also involved in bladder sensation.

Acknowledgements

Thanks to Dr G. Lund, Jetzen Consulting for English language support.

Financing Disclosure

None of the contributing authors has received any direct or indirect commercial financial incentive associated with the publishing of this article.

Conflict of Interest

None declared.

Abbreviations
ACC

anterior cingulate cortex

BOLD

blood-oxygen-level dependent

(p)CPT

(The Psychology Experiment Building Language, PEBL) Continuous Performance Test

fMRI

functional MRI

ISI

inter-stimuli interval

LC

locus coeruleus

mPASAT

modified Paced Auditory Serial Addition Test PET, positron-emission tomography

VAS

visual analogue scale

Ancillary