Epilepsy & Behavior 23 (2012) 98–102
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The assessment of consciousness during partial seizures Fizzah Ali a, Hugh Rickards a, Andrea E. Cavanna a, b,⁎ a b
The Michael Trimble Neuropsychiatry Research Group, Department of Neuropsychiatry, University of Birmingham and BSMHFT, Birmingham, UK National Hospital for Neurology and Neurosurgery, Institute of Neurology and UCL, London, UK
a r t i c l e
i n f o
Article history: Received 26 September 2011 Revised 12 November 2011 Accepted 25 November 2011 Available online 10 January 2012 Keywords: Epilepsy Complex partial seizures Simple partial seizures Consciousness Responsiveness Assessment
a b s t r a c t A wide range of controversial deﬁnitions and dynamic components surround the multi-dimensional concept of consciousness, with important reﬂections on the phenomenological description of ictal states relevant to epileptic seizures. The inadequacies of terminology, the insufﬁcient emphasis on the subjective nature of consciousness, as well as the intrinsic limitations of the simple versus complex dichotomy for partial seizures, are to be considered in view of a modern deﬁnition of consciousness. In this paper, we review the difﬁculties encountered by clinicians in assessing the ictal conscious state in patients with epilepsy, and illustrate how a more sophisticated bi-dimensional model of consciousness can prove a valuable conceptual tool for the clinical assessment of ictal consciousness and the categorization of seizures. © 2011 Elsevier Inc. All rights reserved.
1. Introduction 1.1. The neuroscience of consciousness Recent decades have witnessed a vigorous renewal of neuroscientiﬁc interest into the concept of consciousness. Nevertheless, the connection between conscious thought and electrical activity in the brain continues to pose as a modern scientiﬁc enigma . Deﬁnitions of consciousness have varied over time and across different academic domains, such as philosophy, psychology and clinical neurosciences, including epileptology [2–6]. The distinction between consciousness and self-consciousness has received particular emphasis. The former has been noted to encompass ‘wakefulness’, ‘experience’ or ‘mind’, while the latter conveys at least ﬁve alternative meanings, including ‘self-detection’, ‘self-recognition’ and ‘self-knowledge’ as well as ‘awareness of awareness’ and ‘proneness to embarrassment’ . A broader deﬁnition sums consciousness as the ‘the state of awareness of the self and the environment’ . Likewise, a practical deﬁnition proposed by the Paris school of epileptology regards ictal impairment of consciousness as a ‘transient loss of contact’ between an individual and the internal and external environment . From a clinical
Abbreviations: GCS, Glasgow Coma Scale; ICI-L, Ictal Consciousness InventoryLevel; ICI-C, Ictal Consciousness Inventory-Contents; CSS, Consciousness Seizure Scale; PCI, Phenomenology of Consciousness Inventory. ⁎ Corresponding author at: Department of Neuropsychiatry, University of Birmingham and BSMHFT, The Barberry National Centre for Mental Health, 25 Vincent Drive, Birmingham B152FG, UK. E-mail address: [email protected]
(A.E. Cavanna). 1525-5050/$ – see front matter © 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.yebeh.2011.11.021
perspective, consciousness has been considered akin to the waking state, and the ability to perceive, interact and communicate with the environment and with other individuals [4,7,10]. Throughout this paper we will refer to consciousness as the concept outlined in the epileptologist's terminology. 2. Consciousness and seizure activity Despite conceptual ambiguities, the assessment of consciousness is undeniably fundamental to epileptology, to the point that impairment of consciousness is considered a hallmark of seizure activity. The use of conceptual tools supplied by philosophers of mind (e.g. the concepts of mental representations and phenomenal states) may inform scientiﬁc understanding by alleviating certain inconsistencies of deﬁnition [11–13]. 2.1. Consciousness as a criterion in the classiﬁcation of epileptic seizures In 1970 the Classiﬁcation of Epileptic Seizures already posed consciousness as a central criterion to determine the nature of seizures. ‘Complex’ seizures were deﬁned as paroxysmal episodes accompanied by organized, high-level cerebral activity. However, the exact notion of ‘high-level cerebral activity’ tended to vary between different epileptological schools. The importance of consciousness in epilepsy was further formalized in the 1981 Classiﬁcation of Epileptic Seizures, using consciousness as the cornerstone criterion for the differentiation between simple partial seizures (SPS) and complex partial seizures (CPS). This brought to the fore a number of criticisms.
F. Ali et al. / Epilepsy & Behavior 23 (2012) 98–102
One school of thought condemned the re-deﬁnition of the term ‘complex’, preferring retention of the previous meaning. Other authors accepted the dichotomy, but rejected the terms ‘simple’ and ‘partial’ [14,15]. Epileptic seizures form a diverse continuum of clinical events accompanied by reversible brain dysfunction generating variable alterations in consciousness, thereby posing as an ideal model by which to explore the underlying neuroanatomical and neurophysiological correlates of consciousness. Currently, the neural correlates of consciousness may be deﬁned as the minimal assortment of neuronal events producing a particular aspect of a conscious percept [16,17]. At the heart of the consciousness problem, however, is the inability to connect physical processes to subjective experience . This reconciliation between the subjective and objective aspects of consciousness centers around the problem of ‘qualia’, a philosophical term referring to the subjective experience of percepts . The variety of epileptic semiology allows detailed exploration of the neural correlates of altered consciousness during the ictal state, if epileptologists are appropriately guided through semantic uncertainties about the assessment of consciousness . In both the 1970 and 1981 classiﬁcations, consciousness has been operationally deﬁned as the degree of awareness or responsiveness to external stimuli during the ictal state. Such interpretation is apt at conveying the patient's ability to respond, a clinically measurable parameter, whereby decrement in response equates to impairment or loss of consciousness. Albeit practical, this approach often fails to consider alternative causes of impaired responsiveness such as ictal aphasia and forced attention . The presence of apraxia and impaired comprehension related to other disturbances in sensory processes and memory can also complicate the ictal assessment of impaired level of consciousness [2,6,22,23]. The ictal assessment of consciousness is therefore rarely complete and may be erroneously decided upon, especially in the case of CPS [15,24]. Consideration must also be given to the issue of anterograde amnesia during the seizure, which may masquerade as loss of consciousness due to a patient's inability to recall events despite retention of some degree of both consciousness and cognitive functions . Speciﬁcally, bilateral ictal inactivation of the hippocampal formation has been noted as the possible mechanism for anterograde amnesia for experiential phenomena taking place during a seizure. Unilateral hippocampal discharge in an individual with a nonfunctional hippocampus has additionally been postulated as a contributor . The need for deﬁnitions focusing on an objective perspective on the behavioral constituents of consciousness could be fuelled by the uncertainty spawned by an army of philosophical and neurological debates centered on achieving satisfactory third person assessment of subjective seizure phenomenology . When considering deﬁnitional issues, in particular when making reference to a ‘subjective’ nature, due attention must be given to the patient's perspective. The deﬁnitional issues encircling the concept of consciousness jeopardize clear communication between patients and their physicians. For instance, in a patient suffering from a variety of seizure types the emblematic generalized tonic–clonic seizure may represent ‘loss of consciousness’, despite more subtle alterations in the consciousness state occurring in other types of seizures. Further criticism has suggested rejection of the term ‘loss/ impairment of consciousness’, alternatively encouraging re-deﬁnition in ‘objective behavioral terms’ through consideration of the resultant functional loss, including aspects such as observed behavior, speech function, memory and perceptual skills . Therefore, the use of the ‘loss of consciousness’ criterion as a basis for the classiﬁcation of partial seizures is riddled with difﬁculty. Recent clinical and neuroimaging studies point towards the division of the neural correlates of consciousness into the level and contents of consciousness. This dichotomy may form a more accurate and sophisticated method for assessing the nature of epilepsy-related impairment of consciousness.
2.2. A modern bi-dimensional model of consciousness The recent proposal of a bi-dimensional model allows simpliﬁcation of consciousness alterations into two inter-linked elements, namely the level of consciousness and contents of consciousness, representative of the general level of arousal and speciﬁc subjective aspects of consciousness, respectively. Assessment of both the level and the contents of conscious states contribute to in-depth understanding of the clinical alterations of consciousness that occur during the various epileptic seizures. Conversely, the assortment of ictal semiology (especially during CPS) provides an opportunity to examine the reliability of the bi-dimensional model, which encompasses physiological and pathological states and is derived from a combination of electroencephalographic  and recent neuroimaging work . The level of consciousness corresponds to arousal or vigilance and represents consciousness in the more traditional sense, i.e. what clinical neurologists have referred to when reporting ‘loss’ of consciousness in association with the ictal experience. It may be measured along a continuum ranging from alert wakefulness to sleep and coma [26,27]. Shifts along this ‘consciousness continuum’ may be exogenously induced, for instance with the administration of pharmacological agents acting on the central nervous system (CNS). This component of consciousness may be clinically quantiﬁed through breakdown into the elementary behavioral responses of consciousness as awareness, as in the Glasgow Coma Scale (GCS) . The content of consciousness forms the second major component and encompasses subjective experiences such as sensations, emotions and memories. It is determined by a combination of exogenous factors drawn from the environment and endogenous factors, including attention . The intensity and emotional salience (vividness) of such experiences is therefore highly variable. Written reports and semi-structured interviews  have proven helpful in the assessment of the contents of consciousness. Recent years have unveiled the beneﬁts of neuro-imaging techniques, which in turn have further disclosed the relationship between the contents of conscious states and the activation of speciﬁc cortical areas . The relationship between the level of awareness and contents of consciousness remains to be completely elucidated. Speciﬁc cortical lesions have demonstrated the ability of the contents of consciousness to vary independently of the level of consciousness . However, the level of awareness has a clear inﬂuence over the contents of consciousness. With the exception of particular pathological conditions, namely limbic status epilepticus, a heightening level of arousal comes in hand with enhanced vividness of conscious experience. This relationship is well exempliﬁed by the normal waking state, where the level of consciousness is largely elevated whilst the subjective contents demonstrate considerable variability due to environmental inﬂuence and the individual's internal focus . Although the outlined bi-dimensional model provides an opportunity to systematically assess pathophysiological alterations in the conscious state, this integrated approach inevitably carries limitations which merit mention in the context of assessment of ictal phenomenology. Due to the subjective nature of the contents of consciousness, only the individual experiencing can truly identify the characteristics of the occurrence. It is therefore necessary to take into account the individual's interpretation of ictal subjective experiences, which can in turn reﬂect the highly variable linguistic range and level of insight. Moreover, patients with epilepsy can under-estimate both frequency and duration of episodes of altered consciousness, further complicating the assessment . Overall, the conceptual framework of the bidimensional model highlights that associating seizures with uniform loss of consciousness is a potentially misleading over-simpliﬁcation, as both the level and contents of consciousness show extensive variations during ictal activity.
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2.3. A historical interpretation of the bi-dimensional model of consciousness The modern interpretation of consciousness as a multiplication of both ‘subjective’ and ‘objective’ elements is reminiscent of HughlingsJackson's original categorization of positive and negative ictal symptoms. Hughlings-Jackson advocated a hierarchical system of nervous system function, progressively increasing in complexity . Speciﬁc functions are represented at various levels; initially in their most basic form at the lowest level through to increasingly more complex forms at the highest level . According to this model, CNS insults can generate both negative and positive neurological symptoms: for example, a lesion localized at the highest level (i.e. cerebral cortex) generates negative symptoms as a result of loss of higher function, as well as positive symptoms attributed to loss of inhibitory control over the lower levels [34,35]. This division into positive and negative elements is particularly relevant to the assessment of the multifaceted spectrum of consciousness alterations. Both positive and negative symptoms were represented as a matter of degree: for example, the ﬁrst degree of the positive symptoms was equivalent to the ‘dreamy state’, while the ﬁrst degree of the negative symptoms corresponded to an initial degree of loss of consciousness (unresponsiveness). The second degree of the positive state was identiﬁed with the ‘crude sensations’, while total loss of post-event recollection of on-going ictal events posed as the second degree of negative symptoms. In the ﬁnal degree, the positive symptoms equated to mania and the negative symptoms to complete loss of consciousness, or coma [32,36]. Finally, these ideas on the degrees of consciousness were linked to the notions of the subject and object of consciousness. Within Hughlings-Jackson's concept of sensorimotor function, the sensory function represented the ‘subjective’ component, whereas the motor function corresponded to the ‘objective’ division. In other words, the former relates to the mental representation of an item conjured up from the bunker of stored sensory information of initial perceptions, while the object of consciousness refers to the ability to summon mental images into consciousness . Similarly to the modern bi-dimensional model of consciousness, both subjective and objective elements formed a constant and complex interaction; in the case of Hughlings-Jackson's interpretation of consciousness, the subjective dimension supplied a catalog of mental representations, exploited by the objective aspect for environmental interaction . Of note, in linking consciousness to the ‘dreamy state’, HughlingsJackson was considering the ictal and post-ictal states only, whereby the ‘dreamy state’ is characterized by a variable decrease in object consciousness (negative component) and a variable increase in subject consciousness (positive component) .
The modern notion of a bi-dimensional consciousness is reﬂected in other historical representations. Penﬁeld described patients seemingly caught between ‘two separate streams of consciousness’: ﬁrmly aware of their environment and yet simultaneously preoccupied with vivid emotional experiences generated by temporal lobe stimulation . Likewise, Hughlings-Jackson referred to the symptoms of the ‘dreamy state’ as a ‘double consciousness’, whereby patients demonstrated awareness of ongoing external events and sensed an additional feeling — in this instance, a feeling of familiarity [32,34,38]. It is interesting to re-consider Hughlings-Jackson's dichotomy of positive and negative ictal psychic symptoms in light of the modern conceptualization of consciousness dimensions. In Hughlings-Jackson's view, ictal negative symptoms ranged from reduced wakefulness through to confusion and coma and were related to the dissolution of neural function. Conversely, irritation or hyperactivity of the lower centers generated positive symptoms. In the modern sense, alterations in the contents of consciousness may be considered as products of either excitatory or inhibitory focal cortical discharges . 3. The problem of consciousness in simple partial seizures SPS have been classiﬁed according to motor/sensory signs, autonomic and psychic symptoms (Table 1). Psychic symptoms encompass affective and cognitive disturbances, as well as ictal hallucinations and illusions, and can present in association with ictal dysphasia and dysmnesia. The inclusion of these symptoms as a component of seizures in which consciousness is retained, i.e. SPS, poses as a further controversial fraction of the 1981 classiﬁcation. Historically, a variety of terms have been employed to describe these manifestations of epilepsy which are not convulsive and which are not petit mal. The expressions range from Hoffman's (1862) ‘psychical equivalent’  through to Jackson's ‘uncinate group of seizures’ . In later years, Wilson (1935)  offered ‘psychic variant’ as an alternative, while Penﬁeld  made reference to ‘automatisms’, as well as ‘psychical seizures’, to refer to hallucinatory and illusional episodes. The term ‘psychomotor’ was later adopted by Turner (1907)  as well as Gibbs, Gibbs and Lennox (1938) . Psychic auras, otherwise termed ‘fragmentary psychic seizures’, are usually dominated by unpleasant or frightening sensations, including unexplained feelings of fear and apprehension, as well as a range of ‘ﬂash-back’ experiences such as déjà vu. Despite the variable terminology, a spectrum of ‘changes in consciousness’ is embedded within the symptom catalog of psychomotor seizures . More speciﬁcally, Lennox and Lennox (1960)  documented psychic auras to predominantly consist of unpleasant sensations with the infrequent patient describing the occurrence of a pleasant experience; all the
Table 1 Psychic symptoms reﬂecting altered contents of consciousness during partial seizures. Perceptual phenomena Dysmnesic phenomena Affective phenomena Cognitive phenomena
Factors clouding assessment of psychic ictal phenomena
Illusions including derealization, depersonalization and distortion of body image Structured hallucinations Illusions of memory: déjà vu, déjà vécu, jamais vu, jamais vécu experiences, paramnesias (false recollections) Memory ﬂashbacks Unpleasant emotions (fear, terror, anxiety, guilt, sadness, depression, anger, embarrassment) Pleasant emotions (exhilaration, mirth, blissful happiness, ecstasy, sexual excitement) Dissociative symptoms: Derealization (alteration in one's sense of external reality) Depersonalization (and other forms of alteration) in an individual's sense of personal reality and experience of self, such as autoscopy including out-of-body experiences and seeing one's double Forced thinking and altered speed of thoughts Dysphasic phenomena (language functions): Speech arrest/(Nonﬂuent speech) Comprehension deﬁcit (semantic) paraphasias, anomia Ictal vocalizations/repetitive utterances Aphemia Forced attention Dysmnesic phenomena: Selective memory impairment
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Table 2 Clinical features associated with the general level of awareness and subjective contents of consciousness during partial seizures and correlations with the International Classiﬁcation of Epileptic Seizures (ILAE, 1981).
Preservation Alteration Loss Masking phenomena Assessment tools
Normal interaction (with the examiner)⁎ Selective impaired responsiveness§ [Complete/total] unresponsiveness§ Amnesia, aphasia, “forced attention” GCS, ICI-L, CSS
Motor/somatosensory/autonomic symptoms⁎ Psychic symptoms⁎ “Zombie-like” states⁎ Amnesia, poor insight, lack of introspection, subjectivity PCI, ICI-C
Abbreviations: GCS, Glasgow Coma Scale; ICI-L, Ictal Consciousness Inventory-Level; CSS, Consciousness in Seizure Scale; PCI, Phenomenology of Consciousness Inventory; ICI-C, Ictal Consciousness Inventory-Contents. ⁎ Simple partial seizures or epileptic auras. § Complex partial seizures.
same derangement of consciousness was ascribed to these auras. The inclusion of ictal subjective experiences with retention of a degree of responsiveness (as in several psychic auras) within the SPS category is problematic as these seizures involve additional alterations of consciousness with respect to subjective experience (contents of consciousness) and are qualitatively different from purely motor or sensory SPS. 4. Current approaches to the assessment of ictal consciousness in epilepsy Both historical analysis and current evidence support the assessment of ictal consciousness in degrees of alteration with respect to levels of general awareness and subjective contents of consciousness (Table 2). The degree of impairment ranges across a wide spectrum according to seizure type. Complete loss of consciousness occurs in both generalized tonic–clonic and absence seizures. Selective and variable impairment is demonstrated in both SPS and CPS. The contents of consciousness can vary independently of the level of consciousness: various examples have been documented in the scientiﬁc literature where normal levels of responsiveness are coupled with minimal contents of consciousness. These instances are characterized by perceived ‘normal’ interaction with the external environment in an automatic and uncreative manner. A prime example is Hughlings-Jackson's famous case report of Dr. Z, a patient who displayed a ‘conscious’ and sophisticated behavior during epileptic seizures using his learnt medical knowledge. His recollection of the ictal phase, however, was evidently tampered . The complexity of a conceptual model for understanding alterations of consciousness which ‘cuts nature at its joints’ is reﬂected by the difﬁculties encountered by clinicians in assessing the ictal conscious state in patients with epilepsy. Within this framework, the bidimensional model of consciousness can prove a valuable conceptual tool for both the clinical assessment of ictal consciousness and the categorization of seizures [48–50]. The current approaches to the assessment of seizure-induced alterations of consciousness are directed towards a quantiﬁcation of the impact of the ictal activity on different aspects of consciousness. Speciﬁcally, in recent years two psychometric tools have been developed to assist the systematic assessment of consciousness in epilepsy populations. The Ictal Consciousness Inventory (ICI) was developed in 2008 to allow the quantitative analysis of the ictal state according to the bidimensional model (level versus contents) of consciousness during a given seizure . According to this model, the ICI has two ten-item subscales, ICI-L (level) and ICI-C (contents). The ICI-L assesses the level of general awareness/responsiveness (including general awareness of time, place and others; comprehension and responsiveness; gaze control; forced attention and voluntary initiative), while the ICI-C quantiﬁes the vividness of ictal subjective experiences (including derealization and dreamy states; ictal emotions; illusions and hallucinations). The Consciousness in Seizure Scale (CSS) was developed in 2009 based on eight criteria and, similarly to the ICI-L,
takes into account different aspects of the general level of consciousness in humans: unresponsiveness (Criteria 1 and 2); visual attention (Criterion 3); consciousness of the seizure (Criterion 4); adapted behavior (Criterion 5); amnesia (Criteria 6 and 7) . Both scales are patient-report and user friendly, however the criteria of the CSS are balanced with a ‘global appreciation criterion’, representing the global appreciation of loss of consciousness made by the epileptologist about the conscious state of the patient. Despite their intrinsic limitations (user compliance, ictal amnesia, recall bias, etc.), these psychometric tools represent the ﬁrst steps towards the description of the ictal conscious state in a systematic and standardized fashion. The ICI has proven helpful in assisting the differential diagnosis between alterations of consciousness in different types of epilepsy  and non-epileptic attack disorder . In general, these instruments will probably pave the way to a new generation of studies addressing anatomo-clinical correlations of altered consciousness in epilepsy. References  Blumenfeld H. Why do seizures cause loss of consciousness? Neuroscientist 2003;9:301–10.  Gloor P. Consciousness as a neurological concept in epileptology: a critical review. Epilepsia 1986;27:14–26.  Dennett D. Consciousness explained. Boston, MA: Little, Brown; 1991.  Markowitsch HJ. Cerebral basis of consciousness: a historical review. Neuropsychologia 1995;33:1181–92.  Searle J. The mystery of consciousness. London: Granta Book; 1997.  Zappulla RA. Epilepsy and consciousness. Semin Neurol 1997;17:113–9.  Zeman A. Consciousness. Brain 2001;124:1263–89.  Plum F, Posner JB. The diagnosis of stupor and coma. Contemporary Neurology Series. Philadelphia: Davis Company; 1980.  Avanzini G, De Curtis M, Pape HC, Spreaﬁco R. Intrinsic properties of reticular thalamic neurons relevant to genetically determined spike-wave generation. In: DelgadoEscueta AV, Wilson WA, Olsen RW, Porter RJ, editors. Jasper's Basic Mechanisms of the Epilepsies, 3rd ed. Philadelphia: Lippincott Williams & Wilkins; 1999. p. 297–309.  Dennett DC. Consciousness. In: Gregory RL, editor. The Oxford Companion to the Mind. Oxford: Oxford University Press; 1987. p. 160–4.  Chalmers D. The problems of consciousness. Adv Neurol 1998;77:7–18.  Churchland PS. Neurophilosophy. Cambridge, MA: MIT Press; 1986.  Churchland PM, Churchland PS. Recent work on consciousness: philosophical, theoretical, and empirical. Semin Neurol 1997;17:179–86.  Wolf P. The classiﬁcation of seizures and the epilepsies. In: Porter RJ, Morselli PL, editors. The epilepsies. London: Butterworths; 1985. p. 106–24.  Porter RJ. Disorders of consciousness and associated complex behaviors. Semin Neurol 1991;11:110–7.  Rees G, Kreiman G, Koch C. Neural correlates of consciousness in humans. Nat Rev Neurosci 2002;3:261–70.  Crick FC, Koch C. What are the neural correlates of consciousness? In: Van Hemmen L, Sejnowski TJ, editors. Problems in systems neuroscience. New York: Oxford University Press; 2003. p. 273–82.  Dennett D. Are we explaining consciousness yet? Cognition 2001;79:221–37.  Kalamangalam GP. Epilepsy and the physical basis of consciousness. Seizure 2001;10: 484–91.  Feinberg TE. The irreducibile perspectives of consciousness. Semin Neurol 1997;17: 85–93.  Gloor P. Mesial temporal sclerosis: historical background and an overview from a modern perspective. In: Luders HO, editor. Epilepsy surgery. New York: Raven; 1991. p. 689–703.  Commission on classiﬁcation and terminology of the International League Against Epilepsy. Proposal for revised clinical and electrographic classiﬁcation of epileptic seizures. Epilepsia 1981;22:489–501.
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