Invited reviewVigilance, alertness, or sustained attention: physiological basis and measurement
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.
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