Elsevier

Clinical Neurophysiology

Volume 117, Issue 9, September 2006, Pages 1885-1901
Clinical Neurophysiology

Invited review
Vigilance, alertness, or sustained attention: physiological basis and measurement

https://doi.org/10.1016/j.clinph.2006.01.017Get rights and content

Abstract

Vigilance is a term with varied definitions but the most common usage is sustained attention or tonic alertness. This usage of vigilance implies both the degree of arousal on the sleep–wake axis and the level of cognitive performance. There are many interacting neural and neurotransmitter systems that affect vigilance. Most studies of vigilance have relied on states where the sleep–wake state is altered, e.g. drowsiness, sleep-deprivation, and CNS-active drugs, but there are factors ranging from psychophysics to motivation that may impact vigilance. While EEG is the most commonly studied physiologic measure of vigilance, various measures of eye movement and of autonomic nervous system activity have also been used. This review paper discusses the underlying neural basis of vigilance and its assessment using physiologic tools. Since, assessment of vigilance requires assessment of cognitive function this aspect is also discussed.

Introduction

There are activation states of cerebral cortex that impact the ability to process information where the activation itself contains no specific information. These activation states can be tonic or phasic and may be relatively global or more localized. Terms that have been used to describe these states include arousal, alertness, vigilance, and attention. Unfortunately, no terms are ideal to describe these states of cortical activation since most terms are in broad use with varied associations and there are not perfect physiological markers. The term vigilance, in particular, has unfortunately been used in different ways by different groups of scientists. Psychologists and cognitive neuroscientists use the term to describe an ability to sustain attention to a task for a period of time (Davies and Parasuraman, 1982, Parasuraman, 1998a). They often specifically refer to a vigilance decrement, the decline in attention-requiring performance over an extended period of time (Mackworth, 1964). Animal behavior scientists and psychiatric clinicians use the term vigilance similarly but more specifically referring to attention to potential threats or dangers, with hypervigilance being one of the symptoms of post-traumatic stress disorder (American Psychiatric Association, 1994). This usage of vigilance is probably closest to the common lay usage and to the English dictionary primary definitions of vigilance, e.g. ‘state of being alertly watchful, especially to avoid danger’ (Merriam-Webster [online], 2005). A third group of scientists are clinical neurophysiologists who sometimes use the term vigilance level to refer more narrowly to arousal level on the sleep–wake spectrum without any mention of cognition or behavioral responsiveness. This is partly related to the EEG's exquisite sensitivity to the activity of the corticothalamic networks underlying the sleep–wake dimension (Steriade, 1999). It also may relate to the lack of lay usage of the term vigilance in languages other than English, the translation of the English word arousal into a more medically used term vigilance in French and Vigilanz in German, and to a less common English definition of the term vigilance. Most would consider arousal or wakefulness an aspect of vigilance (Parasuraman et al., 1998) and in many cases the two are very closely related, e.g. with sleep-deprivation. For this discussion, vigilance will mean sustained attention, the most common scientific usage.

Arousal is another term that is used differently by different groups of scientists but more consistently refers to non-specific activation of cerebral cortex in relation to sleep–wake states. While vigilance as we have defined it is conceptually distinct from arousal, most research on vigilance has, in fact, studied alterations in arousal through the use of subjects who are sleep-deprived, have sleep disorders, or are taking sedative medications. This problem is compounded by the fact that relative sleep-deprivation is common in the overtly healthy population (Bonnet and Arand, 1995b, Levine et al., 1988) contributing to healthy subjects becoming drowsy during performance of a prolonged, often tedious task. Thus, the aspect of vigilance distinct from arousal that requires a normally awake person to attend to a task for a prolonged period has not been as well-studied physiologicially. Attention usually refers to a more focused activation of cerebral cortex that enhances information processing (Mesulam, 1990, Mountcastle, 1978, Parasuraman, 1998a, Posner and Petersen, 1990) but one aspect, sustained attention, is used synonymously with the most common usage of vigilance (Parasuraman, 1998b). While focused attention, divided attention, and shifting of attention, as well as executive control of attention, are all important, sustained attention is the aspect closely related to the alertness systems and the only attentional aspect that will be discussed in detail. Alertness is another term that overlaps with arousal but more specifically includes some cognitive processing. Some researchers use the terms phasic and tonic alertness (Nebes and Brady, 1993, Posner and Petersen, 1990). Phasic alertness relates to the orienting response (Sokolov, 1963) and tonic alertness will be used synonymously to vigilance and sustained attention.

This review paper of the biologic bases and physiologic correlates of vigilance, perhaps better referred to as tonic alertness or sustained attention, encompasses an extremely large field. The paper focuses on the basic underlying mechanisms including animal studies and on physiologic measurements that have been related to these states, including EEG, event-related potentials, eye movements, and measures of autonomic nervous system activity. The human electrophysiology section focuses on just several conditions associated with altered alertness: the normal wake–sleep transition, sleep-deprivation and sleep fragmentation, as well as declines on sustained continuous performance tasks. Some relevant topics such as drug effects were omitted in the interest of space. Additionally, only a subset of excellent papers could be cited.

Section snippets

Underlying mechanisms and physiology

Alertness and sustained attention to the environment have multiple underlying brain processes and related psychological constructs. A very important aspect already referred to is the sleep–wake state, dependent on multiple brain-stem–thalamo–cortical pathways. There are also many modulatory systems that impact the sleep–wake state and alertness. These neural-based systems include the suprachiasmatic nucleus–circadian rhythm (Dijk and Czeisler, 1995), the hypothalamo–pituitary–adrenal axis, and

Conditions associated with changes in alertness and sustained attention

To further understand the alertness and sustained attention systems, the physiology associated with altered attentional conditions will next be discussed: the usual awake–sleep transition and sleep deprivation. Due to space limitations of this review, declines in vigilance associated with other conditions will not be discussed further, including attention-deficit hyperactivity disorder (Barkley et al., 1992), sleep apnea (Engleman and Martin, 1994, Verstraeten and Cluydts, 2004) and narcolepsy (

Conclusions

There are a number of neural and functional systems relatively directly affecting phasic and tonic alertness. In addition, there are a number of systems that directly modulate these alertness systems, such as the neural systems related to motivation and stress. The multiple constructs and neural systems underlying the relatively non-specific phasic and tonic alertness activation states imply that they are not unidimensional. Thus, one should rarely, if ever, simplify and speak about vigilance

Acknowledgements

Supported in part by NIH AT002656 and AT01993.

References (254)

  • H. Engleman et al.

    Effect of continuous positive airway pressure treatment on daytime function in sleep apnoea/hypopnoea syndrome

    Lancet

    (1994)
  • R. Gallassi et al.

    Fatal familial insomnia: neuropsychological study of a disease with thalamic degeneration

    Cortex

    (1992)
  • A.S. Gevins et al.

    Computer rejection of EEG artifact. Ii. Contamination by drowsiness

    Electroencephalogr Clin Neurophysiol

    (1977)
  • C. Guilleminault et al.

    A cause of excessive daytime sleepiness: the upper airway resistance syndrome

    Chest

    (1993)
  • Y. Harrison et al.

    High sleepability without sleepiness. The ability to fall asleep rapidly without other signs of sleepiness

    Neurophysiol Clin

    (1996)
  • P. Achermann et al.

    Mathematical models of sleep regulation

    Front Biosci

    (2003)
  • T. Akerstedt

    Sleepiness as a consequence of shift work

    Sleep

    (1988)
  • T. Akerstedt et al.

    Subjective and objective sleepiness in the active individual

    Int J Neurosci

    (1990)
  • T. Akerstedt et al.

    Shift work and napping

  • American Psychiatric Association. Diagnostic and statistical manual of mental disorders. 4th ed. Washington, D.C.:...
  • D. Arand et al.

    The clinical use of the MSLT and MWT

    Sleep

    (2005)
  • G. Aston-Jones et al.

    Activity of norepinephrine-containing locus coeruleus neurons in behaving rats anticipates fluctuations in the sleep-waking cycle

    J Neurosci

    (1981)
  • G. Aston-Jones et al.

    Nonrepinephrine-containing locus coeruleus neurons in behaving rats exhibit pronounced responses to non-noxious environmental stimuli

    J Neurosci

    (1981)
  • G. Aston-Jones et al.

    Locus coeruleus neurons in monkey are selectively activated by attended cues in a vigilance task

    J Neurosci

    (1994)
  • H. Babkoff et al.

    Monotonic and rhythmic influences: a challenge for sleep deprivation research

    Psychological Bulletin

    (1991)
  • L.K. Barger et al.

    Extended work shifts and risk of motor vehicle crashes among interns

    N Engl J Med

    (2005)
  • R.A. Barkley et al.

    Frontal lobe functions in attention deficit disorder with and without hyperactivity: a review and research report

    J Abnorm Child Psychol

    (1992)
  • M. Beaumont et al.

    Slow release caffeine and prolonged (64-h) continuous wakefulness: effects on vigilance and cognitive performance

    J Sleep Res

    (2001)
  • H. Begleiter et al.

    P3 and stimulus incentive values

    Psychophysiology

    (1983)
  • L.S. Bennett et al.

    A behavioural test to assess daytime sleepiness in obstructive sleep apnoea

    J Sleep Res

    (1997)
  • B.O. Bergum et al.

    End-spurt in vigilance

    J Exp Psychol

    (1963)
  • G.G. Bernston et al.

    Autonomic determinism. The modes of autonomic control, the doctrine of autonomic space, and the laws of autonomic constraint

    Psychol Rev

    (1991)
  • P. Binks et al.

    Short term total sleep deprivation does not slelctively impair higher cortical functioning

    Sleep

    (1999)
  • J. Black et al.

    Upper airway resistance syndrome: central electroencephalographic power and changes in breathing effort

    Am J Respir Crit Care Med

    (2000)
  • M. Bonnet et al.

    The consequences of a week of insomnia

    Sleep Research

    (1995)
  • M. Bonnet et al.

    We are chronically sleep deprived

    Sleep

    (1995)
  • M.H. Bonnett et al.

    Sleepiness as measured by MSLT varies as a function of preceding activity

    Sleep

    (1998)
  • M. Bonnet et al.

    Performance and cardiovascular measures in normal adults with extreme MSLT scores and subjective sleepiness levels

    Sleep

    (2005)
  • M. Bonnet et al.

    The threshold of sleep: perception of sleep as a function of time asleep and auditory threshold

    Sleep

    (1982)
  • D.M. Caggiano et al.

    The role of memory representation in the vigilance decrement

    Psychon Bull Rev

    (2004)
  • C. Cajochen et al.

    Power density in the theta/alpha frequencies of the waking EEG progressively increases during sustained wakefulness

    Sleep

    (1995)
  • C. Cajochen et al.

    EEG and ocular correlates of circadian melatonin phase and human performance decrements during sleep loss

    Am J Physiol

    (1999)
  • J.A. Caldwell et al.

    Effects of task duration on sensitivity to sleep deprivation using the multi-attribute task battery

    Behav Res Methods Instrum Comput

    (1998)
  • J. Caldwell et al.

    Body posture affects electroencephalographic activity and psychomotor vigilance task performance in sleep-deprived subjects

    Clin Neurophysiol

    (2002)
  • M. Carskadon

    Cumulative effects of sleep restriction on daytime sleepiness

    Psychophysiology

    (1981)
  • M. Carskadon et al.

    Nocturnal determinants of daytime sleepiness

    Sleep

    (1982)
  • M.A. Carskadon et al.

    Effects of total sleep loss on sleep tendency

    Percept Mot Skills

    (1979)
  • M.A. Carskadon et al.

    Guidelines for the multiple sleep latency test (MSLT): a standard measure of sleepiness

    Sleep

    (1986)
  • A. Cavallo et al.

    Impact of night-float rotation on sleep, mood, and alertness: the resident's perception

    Chronobiology International

    (2002)
  • G.G. Celesia et al.

    Acetylcholine release from cerebral cortex in relation to state of activation

    Neurology

    (1966)
  • Cited by (583)

    • Using caffeine as a chemical means to induce flow states

      2024, Neuroscience and Biobehavioral Reviews
    View all citing articles on Scopus
    View full text