General

Influenced by Sir Edward Coke, Chief Justice of the King’s Bench (1613), Anglo-American law defines criminal offenses whereby a person must be in a certain mental state, called the mens rea (guilty mind), necessary to have committed a crime and have accomplished the criminal act, called the actus reus (guilty act). Traditionally, intention is found within mens rea, and the physical part of the offense resides within actus reus. It is necessary to prove both essential elements to secure a conviction.

Sir Nicolas Tindal established in 1843 what has become known as the M’Naghten Rules, which exculpates the defendant for an offense committed while the defendant was suffering from a disorder of reason or disease of the mind in a manner “as not to know the nature and quality of the act he was doing; or, if he did know it, that he did not know he was doing what was wrong.”^2,3 From a neuroscientific perspective, the criminal act or actus reus component of the crime is of less interest than the essential element of mens rea in regard to both culpability and mechanism of behavior. Implementation of the M’Naghten Rules thereby becomes a watershed moment concerning the influence of neuroscience on criminal law as the mind—or that most complex of all organs, the brain—firmly becomes the linchpin in criminal law from which all is determined and to what degree. Consequently, with the growth and advances seen since the 1980s, neuroscience has only recently begun to appreciate its vast influence on society.

Sleep

The first appearance of the “sleepwalking defense” in an American court of law came in Massachusetts v Tirrell⁴ in 1846. In this landmark case, Rufus Choate, a skilled orator, innovative legal tactician, and U.S. senator, successfully employed the “insanity of sleep” defense to convince the jury to acquit Tirrell of homicide although Tirrell brutally killed the victim with a razor, almost severing her head from her body, set the horrifically bloody crime scene ablaze, and attempted to flee the country.⁵ In the mid to late 1800s there were no plausible medical explanations to account for sleepwalking, let alone account for complex violent actions that apparently arose from sleep and led to misfortune. Though such tragic circumstances resulting in death appear to be exceedingly rare, when presented to a court of law, as in HMS Advocate v Fraser (1878)⁶ and Fain v Commonwealth (1879),⁷ a homicide charge may be defended by pleas of a temporary “defect of reason” or “disease of mind.”

Until physiologic aspects of sleep could be objectively measured and verified using validated neuroscientific instruments, defending, in the criminal court system, sleep-related violent, antisocial, and apparently bizarre behavior arising from sleep often meant associating such behavior with other, better-understood medical or psychiatric conditions for which sleep might not be related in that particular case, such as automatism versus insanity. A defense of automatism may be appropriate for allegations associated with behavior arising from epileptic seizures, fugue states, and limbic psychotic trigger reactions, whereas an insanity plea would likely find no opposition if the defendant acted in the throes of fulminant delusional paranoid schizophrenia. However, superimposing criminal allegations associated with sleep disorders upon the well-established legal models of “automatism” and “insanity” has led to unresolved ambiguities, uneven court processes, and ultimately unpredictable outcomes whereby even an acquittal can result in life-long incarceration in a mental health facility.

The legal community’s perspective toward sleep began to shift in 1968 with Roger Broughton’s seminal publication characterizing the relationship among somnambulism, nightmares, confusional states of arousal, and rapid eye movement (REM) sleep.⁸ By creating a clear demarcation between sleep disorders and other medical or psychiatric conditions, this appears to be the first scientific sleep-related publication with direct legal implications, as supported by the Regina v Parks (1992),⁹ where Broughton served as an expert witness on behalf of the defense. It has been documented in this criminal case that the defendant drove in the early morning hours to the house of his wife’s parents. Apparently while still sleepwalking, the defendant was provoked to attack by his in-laws’ physical contact, whereby he then attacked both of them with a kitchen knife, killing his mother-in-law and leaving his father-in-law seriously injured.¹⁰ The defendant was acquitted in a complete defense of all criminal charges, including homicide, in a courtroom jury trial whose rendering was eventually upheld by a landmark decision by the Supreme Court of Canada not to characterize sleepwalking as a mental health disorder.

Though inherently multidisciplinary, somnology, when addressing the mental state with the ephemeral nature of consciousness, is best categorized as a subset within the greater field of neuroscience. Yet, despite ongoing scientific and medical advances within the field, the legal community remains bewildered in its approach toward sleep.

Waking Consciousness

As mentioned, Anglo-American law has traditionally defined criminal offenses as requiring both an actus reus and a mens rea. The state (or prosecution) must prove both elements to secure a conviction. Regrettably, it has proved exceedingly difficult to establish either the precise meaning of these terms or the relationships connecting them. The American Law Institute’s Model Penal Code (MPC) attempts to provide guidance to these difficult relationships by substituting a relatively simplified set of terms and requirements for offense definitions. To secure a conviction in a criminal trial under the MPC, the state must prove all elements in the definition of the offense and must exhibit that the conduct was a voluntary act. Furthermore, the MPC includes a culpability requirement for each material element of the offense.

Criminal law presumes that most human behavior is voluntary and that individuals are consciously aware of their acts. All criminal liability is based upon a voluntary act, or an omission to engage in a voluntary act that the defendant would otherwise have been capable of performing, that is composed of three key elements governed by Aristotelian rules of syllogistic logic: an internal event (volition), an external event (demonstration), and a causal connection (internal plus external events). Voluntariness is the first step in establishing mens rea; if that is successfully proved, the state proceeds to assess liability according to the four levels of culpability: purpose, knowledge, recklessness, and negligence. In criminal law, the level of culpability determines the category of homicide (murder, manslaughter, or negligent homicide) and the category directly influences the severity of punishment.

Because voluntariness is absolutely fundamental to mens rea, it is surprising that the MPC never explicitly defines the term voluntary acts, but it does offer four examples of acts that are not voluntary including reflex convulsion; bodily movement during unconsciousness or sleep; bodily movement that is not otherwise not a product of the effort or determination of the actor, either conscious or habitual; and conduct during hypnosis or hypnotic suggestion.^11,12 The MPC Commentaries offer further explanations but maintain vagueness to allow each court to render its own interpretation, particularly when addressing what would constitute “conscious” and “unconscious” bodily movements. As voluntariness is to mens rea, consciousness is to voluntary conduct. Despite the lack of clarity, criminal law must attempt to explain consciousness, and in this the MPC provides a clue with its decision to specifically cite hypnotic suggestion as an involuntary act, a striking reminder of the potent strength of the sphere of Freudian thought on the MPC’s advisory committee members.¹²

A comprehensive review toward a neuroscience of consciousness is well beyond the scope of this chapter. First, consciousness is a term that has varied meanings to neuroscientists, though in the legal realm its definition has held steadfast. In science, for example, consciousness may be used to indicate whether or not an individual is in a conscious state, as in whether it has been altered, reduced, or even lost. On the other hand, consciousness may be a trait or an attribute of a psychological process, as in the ability to think, see, and feel consciously. With trait consciousness, further distinctions may be made between conscious representations, which are usually phenomenal and required conscious access. Unfortunately, a direct objective marker for the neural basis of state and trait consciousness that is independent of a person’s external expressions or behavior has yet to be determined. Nevertheless, the neuronal processes that mediate the required conscious access provide a prominent candidate in a network of frontoparietal cortical regions that play an important role in attentional and behavioral selection of incoming and stored information. Because the frontoparietal cortical regions govern behavioral selection, it is not surprising that this region becomes active when patients in a vegetative state recover or becomes further activated when healthy subjects perform demanding perceptual tasks.

Sleep is regularly and actively induced by a shift in neuronal activity and neurotransmitter balance in brainstem nuclei. Functional neuroimaging studies performed on sleeping subjects reveal that during both REM and non-REM (NREM) sleep the prefrontal and parietal cortical regions become deactivated in comparison to the resting wakeful state.^13–15 The most active regions during the resting wakeful state include the left dorsolateral and medial prefrontal areas, the inferior parietal cortex, and the posterior cingulate and precuneus.¹⁴ In REM sleep, despite overall increases in cerebral blood flow and energy demands, relatively low regional cerebral blood flow persists in prefrontal and parietal cortex.¹⁶ Consciousness involves awareness of our environment, awareness of our bodies, and introspection (self-awareness), and it can only fully occur when we are awake. Thus, in this regard, the frontal cortex would appear to be indispensable to consciousness.

Another important region is the dorsal thalamus, the “gateway to the cortex,” and its accompanying “guardian of the gateway,” the reticular complex (part of which is often called the perigeniculate nucleus).^17–20 Francis Crick believed that the input and output gating of the reticular complex were topographically arranged to approximate a map of the entire cortex. In his searchlight hypothesis, the reticular complex thereby was able to heat up the warmer parts of the thalamus and cool down the cooler parts so that “attention” would remain focused on the most active thalamocortical regions.²¹ Though the function of the thalamic reticular complex remains incompletely understood, as with the frontal cortex, it is essential for consciousness, whereas cerebellar circuits, in contrast, are not.

Dreaming Consciousness

The concept of consciousness was first put forth by influential American scientific psychologist and pragmatist William James (1842-1910). Consciousness has been subdivided into nine distinct components (Table 63-1), all of which are seamlessly integrated into our own personal conscious experience. What differentiates humans from other animals is language, which enriches the cognitive experience and allows humans to develop verbal and numeric abstractions. Thus, the animal models of consciousness are limited because they could never address the full range of human cognitive experience that resides in the comparatively enormous cerebral cortex.

Table 63-1 The Nine Components of Consciousness

It is obvious with sleep onset that sensory input is largely lost and our ability to interact with the external environment is curtailed. The conscious state paradigm outlined by J. Alan Hobson recognizes that all nine components of consciousness change to varying degrees as the brain changes state and does so in a repetitive and stereotyped manner over the sleep–wake cycle. Furthermore, consciousness is graded, and the state changes appear to be of such dramatic magnitude that strong inferences can be made about the major physiologic underpinnings of consciousness.²² The application of the conscious state paradigm has led Hobson to declare three important principles. First, as consciousness rides on the crest of the brain activation process, even a small perturbation in activation level leads to lapses in waking vigilance. Second, though consciousness may be largely deactivated, the brain remains highly active and is still capable of processing information. Functional imaging studies reveal that the brain remains about 80% active even when consciousness has largely subsided. Lastly, most brain activity is not associated with consciousness. In relation to its evanescence, consciousness “is a very poor judge of its own causation and of information processing by the brain.”²²

There have been seismic shifts in cognitive neuroscience that the legal system has yet to appreciate and incorporate into the legal arena. Rather confusingly, the terms “conscious” and “unconscious” are still used in the lexicon of neuroscience, but the ideas and principles behind these terms have been substantially altered and continue to be refined, with one such example being Tononi’s information integration theory of consciousness.^23,24 Advances in neuroscience since the 1980s support the existence of a continuum of conscious and unconscious processes and it has dispensed with Freudian-influenced psychoanalytic concepts and theories. The boundaries between our conscious and unconscious, as between wake and sleep, are permeable, dynamic, and interactive, and there is no valid scientific support for the sharp dichotomy as currently held by the MPC and the legal community. It is this model of permeability, or state dissociation, that will also assist in the explanation of unusual, irrational, or bizarre human behavior in sleep forensics.