Consciousness: A Neurological Perspective

107 Behavioural Neurology 24 (2011) 107–116 DOI 10.3233/BEN-2011-0322 IOS Press Consciousness: A neurological perspective Andrea E. Cavannaa,b,∗, Sachin Shaha,c, Clare M. Eddya, Adrian Williamsd and Hugh Rickardsa a Department of Neuropsychiatry, University of Birmingham and BSMHFT, Birmingham, UK Department of Neuropsychiatry, Institute of Neurology, UCL, London, UK c University of Birmingham Medical School, Birmingham, UK d Division of Neurosciences, University of Birmingham and UHB, Birmingham, UK b Abstract. Consciousness is a state so essentially entwined with human experience, yet so difficult to conceptually define and measure. In this article, we explore how a bidimensional model of consciousness involving both level of arousal and subjective awareness of the contents of consciousness can be used to differentiate a range of healthy and altered conscious states. These include the different sleep stages of healthy individuals and the altered states of consciousness associated with neurological conditions such as epilepsy, vegetative state and coma. In particular, we discuss how arousal and awareness are positively correlated in normal physiological states with the exception of REM sleep, while a disturbance in this relationship is characteristic of vegetative state, minimally conscious state, complex partial seizures and sleepwalking. Keywords: Arousal, awareness, coma, consciousness, epilepsy, neurology, sleep 1. Two components of consciousness: arousal and awareness For something experienced so intimately by humans, consciousness has nonetheless proven a difficult concept to explain [26]. Consciousness is an ambiguous term, with multiple definitions. Zeman et al. identified several different senses in which the term is used [80], two of which have been of particular interest in the investigation of consciousness: consciousness as arousal and consciousness as awareness [79]. 1.1. Arousal In clinical practice consciousness is typically equated with arousal (i.e. wakefulness, alertness, or vigilance), referring to the ability of an individual to respond to stimuli in the integrated manner expected in the waking state [79]. In healthy individuals, varying degrees of arousal correspond to a range of conscious ∗ Corresponding author: Andrea Eugenio Cavanna, MD, Depart- ment of Neuropsychiatry, University of Birmingham and BSMHFT, Barberry Building, 25 Vincent Drive, Birmingham B15 2FG, United Kingdom. E-mail: . states that extend from deep dreamless sleep, through drowsiness to alert wakefulness [64]. Consciousness in this sense can be evaluated objectively using behavioural criteria such as those specified in the Glasgow Coma Scale (GCS) [74]. Electroencephalogram (EEG) recordings from the cerebral cortex reveal different wave patterns of electrical activity in the brain corresponding to different levels of arousal [8]. Activity is typically divided into four basic types, according to frequency of waveforms per second (hertz). Beta activity is low amplitude fast activity occurring at frequencies of 13–30 Hz, characterising an “active EEG” associated with mental exertion. Alpha activity, at frequencies of 8–13 Hz, characterises the “passive EEG”, and is the predominant background activity during the relaxed waking state when the individual’s eyes are closed. Theta activity is a slower rhythm of 4–7 Hz, present in states of drowsiness. Even slower frequencies of less than 4 Hz are seen in delta activity, associated with sleep. Thus it is evident that increasing levels of arousal are normally associated with increasing frequency of electrical activity in the cerebral cortex. This is caused by a reduction in the extent and degree of cortical synchronisation. Arousal is a function of the ascending reticular activating system (ARAS), a functional component of the ISSN 0953-4180/11/$27.50  2011 – IOS Press and the authors. All rights reserved 108 A.E. Cavanna et al. / Consciousness: A neurological perspective complex neuronal network within the reticular formation of the upper brainstem. The ARAS contains two major axes: the reticulothalamocortical pathway and extrathalamic pathways. Activation of the reticulothalamocortical pathway promotes cortical arousal by facilitating the transthalamic passage of sensory information towards the cerebral cortex [59]. The cholinergic system of the ARAS provides the main input to the thalamic nuclei from the upper brainstem [65]. The intralaminar and reticular nuclei are the thalamic components most associated with this pathway of the ARAS [8]. Meanwhile extrathalamic pathways activate the cortex via a series of direct inputs originating in the brainstem and basal forebrain and collectively exert a large influence on arousal [59]. 1.2. Awareness Consciousness as awareness refers to the content of experience: awareness of the environment and the self. An individual who is conscious will be conscious of something, and it is in this sense that they have awareness. The content of an individual’s subjective experience is comprised of their sensations, thoughts, emotions, memory, imagination and other major psychological processes [79]. The contents of consciousness are associated with activity in specific cortical areas. For example, awareness of visual movement is associated with activity in visual area V5, while awareness of colour is associated with activity in visual area V4 [76]. Focal cortical lesions in these areas have led to akinetopsia and achromatopsia, respectively, in affected individuals [77,78]. How the level of arousal and the contents of consciousness interact is a complex matter and yet to be fully explained. It has been demonstrated that the contents of consciousness can vary independently of the level of consciousness [64]. However, in most conditions the level of consciousness can greatly influence the contents of consciousness. As might be expected, an increase in the level of arousal leads to an increase in the extent and quality of conscious experience. In normal physiological states, arousal and content are positively correlated (Fig. 1). An exception is the dream-state seen in “rapid eye movement” (REM) sleep, where a low level of arousal is associated with vivid sensory imagery [30]. The positive correlation between arousal and content is also disrupted in certain pathological conditions. High levels of arousal, for example, may be associated with poor content of experience, as seen in limbic status epilepticus [60]. Fig. 1. Simplified representation of consciousness as a bidimensional model, along the two axes of Level (Y) and Contents (X). Normal physiological states (green) show positive correlation between level and content of consciousness, with the exception of the dream state in REM sleep. Abnormal states (red) such as coma, anaesthesia and generalised seizures represent a loss of consciousness where both arousal and awareness is low or absent. Dissociated states of consciousness (blue) incl (...truncated)