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The AIM Model of Dreaming, Sleeping, and Waking Consciousness
The AIM Model of Dreaming, Sleeping, and Waking Consciousness 963
The AIM Model of Dreaming, Sleeping, and Waking Consciousness J A Hobson, Harvard Medical School, Boston, MA, USA ã 2009 Elsevier Ltd. All rights reserved.
Introduction When we go to sleep at night and dream, our conscious state changes radically. When we first become drowsy, fleeting dream images may occur. We then become oblivious and hard to rouse from deep sleep. Later in the night, when sleep lightens, we may experience vivid, bizarre dreams from which spontaneous or easily induced awakenings may occur. By studying the changes in the brain which are associated with these changes in our state of consciousness, we may learn more about the physiological mechanisms underlying our states of mind. During waking we can attend to events in the outside world, form perceptions of events, and/or direct our thoughts to those percepts or to other matters, such as the review of our behavior, our plans, or our feelings. When we go to sleep, we become unaware of the outside world and lose the ability to construct thoughts. These perceptual and cognitive defects persist even when we dream: perceptions are then almost entirely internally generated and we have difficulty reasoning about them; we almost always believe that we are awake instead of dreaming. From the vantage point of the cognitive neuroscience of consciousness, we can tentatively explain these phenomena as a function of three factors: 1. Factor A: the level of electrical activation in the brain. 2. Factor I: the status of gating information flow to and from the brain. 3. Factor M: the nature of the mode of information processing within the brain. The level of consciousness is thus low or high, depending upon the level of activation (A). The focus or direction of consciousness is either strongly external or strongly internal, depending on whether the input– output gates of the brain are open or closed to the flow of information (I). The mode (M) of information processing within the brain is set by the ratio of aminergic to cholinergic modulation. Since these three factors can be quantified using experimental data, it is possible to construct a three-dimensional state space model (Figure 1). The state of consciousness, a point with values A, I, and M, varies over time, the fourth dimension of the model. Normal sleep cycles appear as elliptical trajectories in the resulting state space.
Definition of Consciousness For the purpose of the conscious state paradigm, consciousness can be simply defined as awareness of the outside world, our bodies, and ourselves. Consciousness can be further distinguished in two ways. The first distinction is between primary consciousness (which does not depend upon language and may well be shared with many other mammals) and secondary consciousness (which does depend upon language and may be a uniquely human capability). The second distinction is between the components of consciousness, which are shown in Table 1. These components of consciousness vary significantly in strength over the normal wake–sleep–dream cycle. The functions listed in Table 1 are the aspects of consciousness which are commonly studied by cognitive neuroscientists. Here we investigate the common mechanisms by which all of these aspects are changed as a function of the changes in conscious state experienced by us as waking, sleeping, and dreaming.
Characteristics of Consciousness Consciousness is graded and its components vary in strength as the brain changes state over the course of each day of each life and over a lifetime. In other words, consciousness is more or less intense and its components change in relative strength as a function of the sleep–wake cycle. For example, in waking, perception can be exteroceptive, thought can be logical, and memory can be good. By contrast, in dreaming, all three of those cognitive functions are altered; internal perception is enhanced, emotion is intensified and confabulation runs wild, and logical thought and memory are greatly impaired. Table 2 lists some of the state-dependent consciousness components.
Changes in the Brain and in the Body during Sleep; Changes in Consciousness As shown in Figure 2, sleep onset is associated with thalamocortical deactivation. This deactivation is signaled, first, by electroencephalogram (EEG) slowing (stage I) and next by definitive blockage of thalamic transmission with the appearance of EEG spindles (stage II). After that there is a further slowing in frequency and an increase in amplitude of cortical slow waves (stages III and IV). Muscle tone decreases passively, postural shifts stop, and eye movements are greatly reduced as this pattern evolves. During the evolution of these stages of so-called nonrapid eye movement (NREM) sleep, individuals may have
964 The AIM Model of Dreaming, Sleeping, and Waking Consciousness High NE, 5-HT
M
Low NE, 5-HT External inputs I Internal inputs Low Model factor A-Activation: energy level of processing capacity
A
High
Psychological Word count Cognitive complexity, e.g., perceptual vividness, emotional intensity, narrative
Neurobiological EEG activation Firing level and synchrony of reticular, thalamic and cortical neurons
I-Information: source internal or external
Real world space, time and person referents and their stability Real vs. imagined action
Level of presynaptic and postsynaptic inhibition Excitability of sensorimotor pattern generators
M-Mode: organization of data
Internal consistency? Physical possibility? Linear logic?
Activity level of aminergic neurons
Figure 1 The activation/input source/neuromodulation (activation/information/mode; AIM) model. Illustration of three-dimensional state space and the psychological neurobiological correlates of each dimension.
Table 1 Components of consciousness Component
Definition
Attention Perception Memory Orientation Thought Narrative Emotion Instinct Intention Volition
Selection of input data Representation of input data Retrieval of stored representations Representation of time, place, and person Reflection upon representations Linguistic symbolization of representations Feelings about representations Innate propensities to act Representations of goals Decisions to act
fleeting dreams as their brains are disconnected from sensory input, but they soon become oblivious with little or no memorable mental activity. Measures of this deactivation process yield low values of factor A in the AIM model. At the same time that factor A decreases, factors I and M are also decreasing as the sensory gates close and aminergic modulation decreases. After 70–80 min, often signaled by a posture shift, the EEG is reactivated and reverses its downward
path, moving rapidly up through stages III and II to enter stage I. At the same time the electromyogram (EMG) is actively inhibited and the electooculogram (EOG) shows the increasingly clustered and intense eye movements that give REM sleep its name. The values of factor A activation increase to waking levels (and beyond), but sleep persists. But both factors I and M go to their lowest values in REM as the activated brain is actively put offline and further demodulated. The alternation of NREM and REM sleep continues throughout the night at 90- to 100-min intervals. As the night progresses the NREM periods become shorter and less deep while the REM periods become longer and more active. In the last two cycles the alternation is usually between stage II and stage I REM. This increasing brain activation is associated with an increase in dreaming. Although dreaming is always more intense in REM, it also occurs in NREM sleep, especially in the second half of the night.
Formal Analysis of Dream Content In order to compare with waking the nature of conscious experience in REM and light NREM sleep, it has
The AIM Model of Dreaming, Sleeping, and Waking Consciousness 965 Table 2 State-dependent consciousness components Function
Nature of difference
Causal hypothesis
Sensory input Perception (external) Perception (internal) Attention
Blocked Diminished Enhanced Lost
Memory (recent)
Diminished
Memory (remote)
Enhanced
Orientation
Unstable
Thought
Language (internal)
Reasoning ad hoc; logical rigor weak; processing hyperassociative Self-reflection lost (failure to recognize state as dreaming) Confabulatory
Presynaptic inhibition Blockade of sensory input Disinhibition of networks storing sensory representations Decreased aminergic modulation causes a (decrease in) signal-to-noise ratio Because of aminergic demodulation, activated representations are not restored in memory Disinhibition of networks storing mnemonic representations increases access to consciousness Internally inconsistent orienting signals are generated by cholinergic system Loss of attention, memory, and volition leads to failure of sequencing and rule inconstancy; analogy replaces analysis
Emotion
Episodically strong
Instinct
Episodically strong
Volition
Weak
Output
Blocked
Insight
Failure of attention, logic, and memory weakens second- and third-order representations Aminergic demodulation frees narrative synthesis from logical restraints Cholinergic hyperstimulation of amygdala and related temporal lobe structures triggers emotional storms, which are unmodulated by aminergic restraint Cholinergic hyperstimulation of hypothalamus and limbic forebrain triggers fixed-action motor programs, which are experienced fictively but not enacted Top-down motor control and frontal executive power cannot compete with disinhibited subcortical network activation Postsynaptic inhibition
Behavioral state
Wake
NREM
REM
Cognitive consequences Conscious Sensation and experience perception Thought
Acquisition of information Vivid, externally generated Logical progressive Continuous voluntary
Iteration of information Dull or absent
Integration of information Vivid, internally generated Illogical bizarre Commanded but inhibited
Movement Surface recordings
Logical perseverative Episodic involuntary
EMG EEG EOG
Single-cell depth recordings (cat)
PGO waves in lateral geniculate nucleus Aminergic systems (5-HT and NE) Cholinergic systems
REM off
REM on
Figure 2 Behavioral states of humans. States of waking, nonrapid eye movement (NREM) sleep, and REM sleep have behavioral, polygraphic, and psychological manifestations. The sequence of these stages is represented in the polygraph channel. Sample tracings of three variables used to distinguish state are also shown: the electromyogram (EMG) is at its highest in waking, intermediate in NREM sleep, and lowest in REM sleep; the electroencephalogram (EEG) and electooculogram (EOG), which are both activated in waking and REM sleep and inactivated in NREM sleep. PGO, pontogeniculooccipital; 5-HT, 5-hydroxytryptamine (serotonin); NE, norepinephrine.
966 The AIM Model of Dreaming, Sleeping, and Waking Consciousness
proved propitious to quantify such aspects of consciousness as (1) the sense modalities that are represented and the intensity of the internally generated percepts, (2) the occurrence and strength of self-reflective awareness and executive thought, (3) the dreamer’s orientation in time and space, and dream personnel, (4) the dreamer’s emotion profile (presence and strength of emotions such as elation, anxiety/fear, anger, shame, guilt, sadness, and eroticism), and (5) the identification by the dreamer of the possible memory sources of the dream content. This approach has led to the characterization of dream consciousness as having (1) strong sensorimotor perceptions (with a preponderance of vivid visual imagery as the dreamer moves through a fictive reality); (2) impoverishment of executive ego function (with the delusional belief that one is awake and a failure to develop or sustain logical thinking); (3) discontinuity and incongruity of plot features as the basis of bizarre cognition; (4) potentiation of anxiety, anger, and elation together with a weakening of shame, guilt, and sadness; and (5) inability to specify the memory source of the confabulated dream content in about 80% of the cases. Dreaming is thus characterized by visual hallucinations, by disorientation, by lack of insight and judgment, and by memory loss (with compensatory confabulation). These formal similarities are so strong as to lead to the hypothesis that dreaming, although normal, is a state akin to delirium. Since delirium is caused by diseases and by drugs which interfere with normal neuromodulation, it is natural to wonder if, in normal sleep, there are changes in neuromodulation during the wake–sleep cycle.
Cellular and Molecule Mechanisms of Mammalian Sleep All mammals share with humans the regular periods of NREM and REM sleep. This is so whether the animals are aquatic, terrestrial, or arboreal, and whether they are large surface-dwelling carnivores (e.g., lions) or small nest-dwelling herbivores (e.g., mice or rabbits). As an experimental model, the domestic cat has appealed to neurobiologists because it is so docile and so prodigious a sleeper. As experimental animals, cats are more expensive and more ethically problematic than are rats, but they are large enough to carry the microelectrode, microinjection, and microdialysis array, the equipment necessary to perform physiological and pharmacological experiments. They are well studied neuroanatomically so that stereotaxis is facilitated. Using cats, neuroscientists have shown that the two brain-activated states, waking and REM sleep (with high values of A), are at opposite poles with respect to
both input–output gating (high I in waking, low in REM) and neuromodulation (high M in waking, low M in REM). On all these dimensions, NREM sleep is quite different (low A and intermediate I and M). In addition to demonstrating that aminergic levels decline in NREM sleep and reach their nadir in REM, it has been shown that the cholinergic level declines as animals go from waking to NREM, but rises again and reaches its highest level, in REM sleep, especially in the brain stem. This gives factor M (defined as the ratio of aminergic to cholinergic modulation) a highly differentiating power for distinguishing the three states: M is highest in waking, intermediate in NREM sleep, and lowest in REM sleep. This finding is potentially relevant to our understanding of the brain basis of the many phenomenologic distinctions between waking, sleeping, and dreaming. The mode of information processing has changed dramatically. The importance to REM of the pontine brain stem is demonstrated by the presence of the cell bodies of both cholinergic and aminergic neurons there. Furthermore, it has now been conclusively demonstrated that the microinjection into the pontine tegmentum of both cholinergic agonists and cholinesterase antagonists produces dramatic increases in REM sleep. All of these effects are blocked by pretreatment of the injection sites by atropine. There is no longer any doubt that compared to waking and NREM sleep, REM sleep is hypoaminergic and hypercholinergic. This robust physiological difference correlates with – and hypothetically causes – the psychological differences. Based upon new studies in rats, a flip-flop switch for REM sleep triggering has recently been proposed. Each side of the switch contains g-aminobutyric acid (GABA)ergic neurons, and this resulting mutual inhibition guarantees that when one side is on, the other is off. The REM-on population contains two populations of glutaminergic neurons: one population projects to the basal forebrain and produces the forebrain activation while the other projects to the medulla and spinal cord, producing atonia. The cholinergic system is activated as part of the REM-on switch and can, in turn, activate that side of the switch. The REM-off population includes the dorsal raphe nuclei. At a still deeper level, the activation of protein kinase in the pontine tegmentum has been shown to accompany REM sleep, suggesting that pedunculopontine intracellular protein kinase A (PKA) activation is involved in REM sleep generation.
Input–Output Gating Michel Jouvet called REM sleep ‘paradoxical’ because sleep persists despite the EEG evidence for strong brain activation. A partial explanation of the paradox is
The AIM Model of Dreaming, Sleeping, and Waking Consciousness 967
the simultaneous blockade of sensory input and motor output, the neurophysiological mechanisms of which are now well understood. Ottavio Pompeiano used classical Sherrington reflexology techniques to show that motor output is blocked in REM by descending inhibition from the pontomedullary brain stem to the anterior bone cells of the spinal cord. That this inhibition is induced by powerful and active postsynaptic inhibition of the final common path motor neurons was shown by Michael Chase. Chase also demonstrated that the spinal inhibition of REM is mediated by glycine. As for the inhibition of sensory input, it was also Pompeiano who demonstrated that presynaptic inhibition is associated with the clusters of eye movement during REM sleep. An associated occlusion of sensory input excitation also accompanied the REMs. This cooption of input-processing channels (including the allimportant thalamocortical system) is effected by the internally generated pontogeniculooccipital (PGO) waves, first described by Jouvet. These cortical activation waves were later shown to be of entirely internal origin and were enhanced by cholinergic microstimulation. PGO wave generation is inhibited by noradrenaline and serotonin. The emerging picture of REM sleep is a high level of activation in a brain which is not only off-line by virtue of sensory input and motor output blockade, but is also stimulated by phasic activation signals of its own devising. The coactivated mind is therefore fooled by its own parasitic excitation; the brain-mind then develops the illusion or fictive experience of perceiving and moving through dream space.
Efferent Copy Generation The PGO waves of REM sleep not only constitute internally generated phasic activation signals for the dreaming brain-mind, but they also convey to the thalamus and cortex feed-forward information about the direction of the upcoming eye movements. As such, they are classical efferent copy stimuli from the oculomotor circuits to the visual forebrain. Such eye movement activity can also be recorded in waking when it forms an integral part of the startle response. In waking, the PGO waves rapidly habituate as the startle response diminishes. The second and third stimuli of a train evoke a much weaker or no response because they are no longer novel. The mechanism of this attenuation is thought to be aminergic inhibition of the cholinergic-modulated PGO generator neurons of the lateral pons. The relative continuity of waking consciousness is, in part, a function of PGO wave damping, whereas the bizarre discontinuity of dream consciousness
is a function of PGO wave disinhibition. Dream consciousness reflects this dishabituation by the increase in the emotions of surprise and anxiety. These dream features could be mediated by excitation of the amygdala, a major target of the PGO waves. In REM sleep, the efferent copy information about the direction of eye movement that is conveyed by the PGO system is not integrated with changes in visual input, as occurs in waking, because in sleep there is no visual input. It is tempting to speculate that the efferent copy information that is generated in REM sleep is not only a physiological cause of dream surprise, but is also used in perceptual aspects of dream plot construction. The oculomotor system of the pons is only one of many motor program generators that are activated in REM sleep. Locomotion is commanded but, because the anterior horn cells are hyperpolarized, real motor behavior is not generated and REM sleep dreams reflect this by the intensity of fictive motoric action in dreams. There is hardly a sentence in the REM sleep dream report that does not contain an action verb. We are always walking, running, flying, or swimming in our dreams. Even if we lead sedentary waking lives, stationary activity is not represented in our dreams. The finding of motor pattern generator activation in REM sleep and its correlation with the fictive motility of dreaming is a good example of how the close study of neurophysiology can provide dream theory with a new paradigm and new hypotheses regarding the origin of dream plots. Of course, the approach does not allow us to propose why a given dreamer has a given dream or what that dream might mean. But it does provide encouragement for an alternative way of approaching even interpretive questions. For example, our dreams are full of movement because brain motor pattern generators are activated in REM sleep. Further evidence that this theory may be correct is given by experimental and clinical discoveries, both of which reveal unexpected and unwanted enactment of REM sleep motor commands. The experiments of Michel Jouvet and of Adrian Morrison showed that cats with lesions in the vicinity of the locus coeruleus in the pons evinced REM sleep without atonia. In other words, the cats showed sleep with EEG activation REMs but suddenly stood up and evinced a wide variety of attack and defense behaviors. They were then in a dissociated state of REM sleep in which they expressed automatic behaviors that are normally suppressed by the motor inhibition of REM. On the basis of these observations, Jouvet boldly proposed that the cats were acting out their dreams. That idea gained credence when it was reported by Carlos Schenk and Mark Mahowald that humans
968 The AIM Model of Dreaming, Sleeping, and Waking Consciousness
did precisely the same thing when they became afflicted by what they called the REM ‘sleep behavior disorder.’ Schenk’s and Mahowald’s patients, mostly >50-year-old males, performed motor acts in sleep that corresponded to their dream reports. One patient, dreaming that he was playing football, got up out of bed and tried to tackle a chest of drawers. Another, dreaming that he was diving, stood up on the side of the bed and propelled himself into the baseboard of his bedroom, which he imagined to be a swimming pool. Presumably, these experimental and natural pathological conditions of REM sleep without atonia are due to damage of that subpopulation of glutaminergic REM-on neurons that convey inhibitory commands from the flip-flop switch to the spinal cord. These examples would seem to make more plausible the suggestion that dream consciousness is a function of brain activation in sleep and that the important differences between the dreaming and waking states of consciousness are determined by specifiable differences between the mechanisms of brain activation in the two states. In particular, it is the presence or absence in input–output gating that determines the relationship between the outside world and internal perceptions, beliefs, and actions.
Differences in Regional Brain Activation EEG evidence had long suggested that the brain was similarly activated in waking and REM sleep dreaming. The recent advent of PET imaging technology revealed that this was an oversimplified conclusion. Most brain regions are less active in NREM sleep than in either the wake or REM sleep state. But when REM is compared to the wake state, differences emerge which are of great relevance to studies of conscious state determination. Certain brain regions are more active in REM than in waking. They include the pontine tegmentum (which animal studies have shown to be the probable site of the REM sleep and PGO wave generator), the amygdala (which animal studies have shown to be involved in mediating emotion, especially the anxiety which is so common in dreaming), the parietal operculum (which is thought to mediate visuomotor integration of cardinal perceptual feature of dreaming), and the parahippocampal and deep frontal cortices (which may process emotional data and integrate it with cognitive information). One brain region is notably less active in REM than in waking. The dorsolateral prefrontal cortex (DLPFC) remains at the same low level seen in NREM sleep. Other human studies have implicated the DLPFC in the executive ego functions that are so conspicuously deficient in dreaming: short-term memory,
self-reflective awareness, intentional decision making, and volitional action. The brain lesion studies done by Mark Solms have revealed that two of the structures selectively activated in REM sleep are, when damaged, associated with a complete cessation of dream recall. They are the parietal operculum (damage to which causes problems with sensorimotor integration) and the deep frontal white matter (damage to which causes emotional apathy). Patients often complain of cessation of dreaming following lobotomy, which consists of severance of the deep frontal white matter.
Field Studies of Waking, Sleeping, and Dreaming Consciousness The invention of the ‘Nightcap’, a two-channel event recorder, has made possible the field study of conscious experience in humans as they lead their otherwise normal waking and sleeping lives. In addition to wearing the Nightcap for recording their head and eye movements while asleep, participants carried radio beepers so that they could be contacted throughout the day and night to collect reports of conscious experience (see Figure 3(a)). This combination of techniques allowed us, for the first time, to collect reports of consciousness experience in the same persons, from several brain states, around the clock. Over 3000 reports from ten people ages 20–40 years were elicited from active and quiet waking states, from five intervals during sleep onset and from both NREM and REM sleep. The reports were transcribed and scored for dimensions such as word count (REM reports were 6 times as long as NREM reports), internally generated percepts (REM sleep highest, active waking lowest). These data, shown in Figure 3(b), suggest a general psychophysiological law: thinking is incompatible with hallucination and vice versa. The implications of these findings for conscious state control and for psychiatry are loud and clear. One striking finding was a reciprocal increase in internally generated perception and a decrease in thinking across the five states.
Convergence of Physiology, Psychology, and Philosophy The integration of the fields of psychology and physiology, envisaged by William James and the young Freud over 100 years ago, is now beginning, with sleep and dream science leading the way. The Finnish philosopher of science Antti Revonsuo has recently championed the theory, first put forth by Michael Jouvet, that REM sleep dreaming allows the sleeping brain to run adaptive behavioral programs of fight and flight. According to this view, REM sleep dreaming has a Darwinian function even if dream behavior
The AIM Model of Dreaming, Sleeping, and Waking Consciousness 969 Eyelid movements
Wake REM NREM
Head movements
1:00 2:00 3:00 4:00 5:00 6:00 7:00 Time
a Thoughts
Hallucinations 100 Reports with halluclnations (%)
Reports with thoughts (%)
100 80 60 40 20 0 b
80 60 40 20 0
Active Quiet Sleep NREM REM wake wake onset
Active Quiet Sleep NREM REM wake wake onset
Figure 3 (a) Central arousal accompanying the activated states of rapid eye movement (REM) sleep and waking can be measured using the ‘Nightcap,’ a simple ambulatory monitor. The Nightcap is a two-channel recording device that distinguishes waking, REM and NREM sleep. One channel of the Nightcap monitors eye movement and the other monitors body movements. The Nightcap eyelidmovement readout is thought to reflect activity in portions of the brain stem oculomotor nucleus that innervate the eyelid and are adjacent to portions of the medial brain stem ascending reticular system, the activity of which, in turn, generates forebrain activation. (b) Decline in directed thought and reciprocal increase in hallucinations during progression from active waking through sleep onset and NREM to REM sleep.
is fictive. For the German philosopher Thomas Metzinger, the occurrence of lucid dreaming, out-ofbody experience and dreaming itself, supports his phenomenal self-model of consciousness. The phenomenal self is a constantly renewed functional state of the brain whose vicissitudes can, for the first time in human history, begin to be explained.
AIM: An Integrated Model of the Human Brain Mind Using physiological measures, it is now possible to create a three-dimensional model of brain-mind state space (see Figures 1 and 4). Activation, assessed from EEG and/or thalamocortical cellular activity, gives values and axis A, running from left (low) to right (high) across the front wall of the state space. Input– output gating is measured as EMG activity, values of H-reflex, and PGO waves. It runs from the front to the back of the state space. The vertical axis, M, measures the ratio of the strength of aminergic to cholinergic neuron modulation. Unfortunately, factor
A
Low
High w
Aminergic Sleep cycle 1 2 NREM 3 4 M External REM
I
Cholinergic Internal Figure 4 The three-dimensional activation/information/mode (AIM) state space model showing normal transitions within the AIM state space, from wake, to non-rapid eye movement (NREM), and then to REM sleep. REM occupies the lower righthand front corner, in which activation is high, input is entirely internal, and the forebrain is cholinergically activated and aminergically demodulated. ACh, acetylcholine; NE, norepinephrine; 5-HT, 5-hydroxytryptamine.
970 The AIM Model of Dreaming, Sleeping, and Waking Consciousness
M cannot yet be measured in humans, but pharmacological studies indicate that inferences from neurobiological studies in animals are valid. In the model, time is the fourth dimension and the solution of AIM is constantly changing, even in the waking domain (at the far right, upper, rear corner of the state space) as we change the focus of attention, day dream, or enter altered states such as hypnosis. We may become drowsy, doze, or fall frankly asleep, in which case AIM moves down, forward, and to the left and then occupies the NREM sleep domain in the center of the state space. Finally, AIM moves to the REM sleep domain in the right front lower corner of the state space. During a normal night of sleep, AIM function follows an elliptical trajectory that repeats itself 4 or 5 times per night. The ellipse shifts sequentially to the right and to deeper parts of the state space in successive cycles. These elliptical orbits in AIM state space conform to the mathematical description of the reciprocal interaction model, giving an internally consistent picture of sleep physiology. Consciousness is most intense in the right portion of the state space and lowest on the left. It is interoceptive toward the front of the state space and exteroceptive toward the back. The kind of consciousness is given by the mode dimension. It is highest at the top of the state space and lowest at the bottom. Abnormal states of consciousness such as narcolepsy, the REM sleep behavior disorder, delirium, and other psychoses can also be modeled in the normally forbidden zones of AIM state space. See also: Dream Function; Dreams and Dreaming: Incorporation of Waking Events; Dreams and Nightmares
in PTSD; Dreams, Dreaming Theories and Correlates of Nightmares; Sleep and Sleep States: Phylogeny and Ontogeny; Sleep Mentation in REM and NREM: A Neurocognitive Perspective; Sleep Research and Sleep Medicine in Historical Perspective.
Further Reading Amini-Sereshki L and Morrison AR (1986) Effects of pontine tegmental lesions that induce paradoxical sleep without atonia on thermoregulation in cats during wakefulness. Brain Research 384(1): 23–28. Bandyopadhya RS, Datta S, and Saha S (2006) Activation of pedunculopontine tegmental protein kinase A: A mechanism for rapid eye movement sleep generation in the freely moving rat. Journal of Neuroscience 26(35): 8931–8942. Hobson JA, Pace-Schott EF, and Stickgold R (2000) Dreaming and the brain: Toward a cognitive neuroscience of conscious states. Behavioral and Brain Sciences 23: 793–842. Jouvet M (1962) Recherche sur les structures nerveuses et les mechanismes responsables des differentes phases du sommeil physiologique. Archives Italiennes de Biologie 100: 125–206. Jouvet M (1973) Essai sur le reve. Archives Italiennes de Biologie 111: 564–576. Jouvet M, Vimont P, and Delorme F (1965) Elective suppression of paradoxical sleep in the cat by monoamine oxidase inhibitors. Comptes Rendus des Seances de la Societe de Biologie et de ses Filiales 159(7): 1595–1599. Lu J, Sherman D, Devor M, et al. (2006) A putative flip-flop switch for control of REM sleep. Nature 441(7093): 589–594. Metzinger T (2003) On Being No One. Cambridge: MIT Press. Revonsuo A (2005) Inner Presence: Consciousness as a Biological Marker. Cambridge, MA: MIT Press. Schenck CH and Mahowald MW (1996) REM sleep parasomnias. Neurological Clinics 14: 697–720. Solms M (1997) The Neuropsychology of Dreams: a ClinicoAnatomical Study. Mahwah, NJ: Lawrence Erlbaum Associates. Yamuy J, Fung SJ, Xi M, et al. (2004) Hypocretinergic control of spinal cord motor neurons. Journal of Neuroscience 24(23): 5336–5345.
The AIM Model of Dreaming, Sleeping, and Waking Consciousness J A Hobson, Harvard Medical School, Boston, MA, USA ã 2009 Elsevier Ltd. All rights reserved.
Introduction When we go to sleep at night and dream, our conscious state changes radically. When we first become drowsy, fleeting dream images may occur. We then become oblivious and hard to rouse from deep sleep. Later in the night, when sleep lightens, we may experience vivid, bizarre dreams from which spontaneous or easily induced awakenings may occur. By studying the changes in the brain which are associated with these changes in our state of consciousness, we may learn more about the physiological mechanisms underlying our states of mind. During waking we can attend to events in the outside world, form perceptions of events, and/or direct our thoughts to those percepts or to other matters, such as the review of our behavior, our plans, or our feelings. When we go to sleep, we become unaware of the outside world and lose the ability to construct thoughts. These perceptual and cognitive defects persist even when we dream: perceptions are then almost entirely internally generated and we have difficulty reasoning about them; we almost always believe that we are awake instead of dreaming. From the vantage point of the cognitive neuroscience of consciousness, we can tentatively explain these phenomena as a function of three factors: 1. Factor A: the level of electrical activation in the brain. 2. Factor I: the status of gating information flow to and from the brain. 3. Factor M: the nature of the mode of information processing within the brain. The level of consciousness is thus low or high, depending upon the level of activation (A). The focus or direction of consciousness is either strongly external or strongly internal, depending on whether the input– output gates of the brain are open or closed to the flow of information (I). The mode (M) of information processing within the brain is set by the ratio of aminergic to cholinergic modulation. Since these three factors can be quantified using experimental data, it is possible to construct a three-dimensional state space model (Figure 1). The state of consciousness, a point with values A, I, and M, varies over time, the fourth dimension of the model. Normal sleep cycles appear as elliptical trajectories in the resulting state space.
Definition of Consciousness For the purpose of the conscious state paradigm, consciousness can be simply defined as awareness of the outside world, our bodies, and ourselves. Consciousness can be further distinguished in two ways. The first distinction is between primary consciousness (which does not depend upon language and may well be shared with many other mammals) and secondary consciousness (which does depend upon language and may be a uniquely human capability). The second distinction is between the components of consciousness, which are shown in Table 1. These components of consciousness vary significantly in strength over the normal wake–sleep–dream cycle. The functions listed in Table 1 are the aspects of consciousness which are commonly studied by cognitive neuroscientists. Here we investigate the common mechanisms by which all of these aspects are changed as a function of the changes in conscious state experienced by us as waking, sleeping, and dreaming.
Characteristics of Consciousness Consciousness is graded and its components vary in strength as the brain changes state over the course of each day of each life and over a lifetime. In other words, consciousness is more or less intense and its components change in relative strength as a function of the sleep–wake cycle. For example, in waking, perception can be exteroceptive, thought can be logical, and memory can be good. By contrast, in dreaming, all three of those cognitive functions are altered; internal perception is enhanced, emotion is intensified and confabulation runs wild, and logical thought and memory are greatly impaired. Table 2 lists some of the state-dependent consciousness components.
Changes in the Brain and in the Body during Sleep; Changes in Consciousness As shown in Figure 2, sleep onset is associated with thalamocortical deactivation. This deactivation is signaled, first, by electroencephalogram (EEG) slowing (stage I) and next by definitive blockage of thalamic transmission with the appearance of EEG spindles (stage II). After that there is a further slowing in frequency and an increase in amplitude of cortical slow waves (stages III and IV). Muscle tone decreases passively, postural shifts stop, and eye movements are greatly reduced as this pattern evolves. During the evolution of these stages of so-called nonrapid eye movement (NREM) sleep, individuals may have
964 The AIM Model of Dreaming, Sleeping, and Waking Consciousness High NE, 5-HT
M
Low NE, 5-HT External inputs I Internal inputs Low Model factor A-Activation: energy level of processing capacity
A
High
Psychological Word count Cognitive complexity, e.g., perceptual vividness, emotional intensity, narrative
Neurobiological EEG activation Firing level and synchrony of reticular, thalamic and cortical neurons
I-Information: source internal or external
Real world space, time and person referents and their stability Real vs. imagined action
Level of presynaptic and postsynaptic inhibition Excitability of sensorimotor pattern generators
M-Mode: organization of data
Internal consistency? Physical possibility? Linear logic?
Activity level of aminergic neurons
Figure 1 The activation/input source/neuromodulation (activation/information/mode; AIM) model. Illustration of three-dimensional state space and the psychological neurobiological correlates of each dimension.
Table 1 Components of consciousness Component
Definition
Attention Perception Memory Orientation Thought Narrative Emotion Instinct Intention Volition
Selection of input data Representation of input data Retrieval of stored representations Representation of time, place, and person Reflection upon representations Linguistic symbolization of representations Feelings about representations Innate propensities to act Representations of goals Decisions to act
fleeting dreams as their brains are disconnected from sensory input, but they soon become oblivious with little or no memorable mental activity. Measures of this deactivation process yield low values of factor A in the AIM model. At the same time that factor A decreases, factors I and M are also decreasing as the sensory gates close and aminergic modulation decreases. After 70–80 min, often signaled by a posture shift, the EEG is reactivated and reverses its downward
path, moving rapidly up through stages III and II to enter stage I. At the same time the electromyogram (EMG) is actively inhibited and the electooculogram (EOG) shows the increasingly clustered and intense eye movements that give REM sleep its name. The values of factor A activation increase to waking levels (and beyond), but sleep persists. But both factors I and M go to their lowest values in REM as the activated brain is actively put offline and further demodulated. The alternation of NREM and REM sleep continues throughout the night at 90- to 100-min intervals. As the night progresses the NREM periods become shorter and less deep while the REM periods become longer and more active. In the last two cycles the alternation is usually between stage II and stage I REM. This increasing brain activation is associated with an increase in dreaming. Although dreaming is always more intense in REM, it also occurs in NREM sleep, especially in the second half of the night.
Formal Analysis of Dream Content In order to compare with waking the nature of conscious experience in REM and light NREM sleep, it has
The AIM Model of Dreaming, Sleeping, and Waking Consciousness 965 Table 2 State-dependent consciousness components Function
Nature of difference
Causal hypothesis
Sensory input Perception (external) Perception (internal) Attention
Blocked Diminished Enhanced Lost
Memory (recent)
Diminished
Memory (remote)
Enhanced
Orientation
Unstable
Thought
Language (internal)
Reasoning ad hoc; logical rigor weak; processing hyperassociative Self-reflection lost (failure to recognize state as dreaming) Confabulatory
Presynaptic inhibition Blockade of sensory input Disinhibition of networks storing sensory representations Decreased aminergic modulation causes a (decrease in) signal-to-noise ratio Because of aminergic demodulation, activated representations are not restored in memory Disinhibition of networks storing mnemonic representations increases access to consciousness Internally inconsistent orienting signals are generated by cholinergic system Loss of attention, memory, and volition leads to failure of sequencing and rule inconstancy; analogy replaces analysis
Emotion
Episodically strong
Instinct
Episodically strong
Volition
Weak
Output
Blocked
Insight
Failure of attention, logic, and memory weakens second- and third-order representations Aminergic demodulation frees narrative synthesis from logical restraints Cholinergic hyperstimulation of amygdala and related temporal lobe structures triggers emotional storms, which are unmodulated by aminergic restraint Cholinergic hyperstimulation of hypothalamus and limbic forebrain triggers fixed-action motor programs, which are experienced fictively but not enacted Top-down motor control and frontal executive power cannot compete with disinhibited subcortical network activation Postsynaptic inhibition
Behavioral state
Wake
NREM
REM
Cognitive consequences Conscious Sensation and experience perception Thought
Acquisition of information Vivid, externally generated Logical progressive Continuous voluntary
Iteration of information Dull or absent
Integration of information Vivid, internally generated Illogical bizarre Commanded but inhibited
Movement Surface recordings
Logical perseverative Episodic involuntary
EMG EEG EOG
Single-cell depth recordings (cat)
PGO waves in lateral geniculate nucleus Aminergic systems (5-HT and NE) Cholinergic systems
REM off
REM on
Figure 2 Behavioral states of humans. States of waking, nonrapid eye movement (NREM) sleep, and REM sleep have behavioral, polygraphic, and psychological manifestations. The sequence of these stages is represented in the polygraph channel. Sample tracings of three variables used to distinguish state are also shown: the electromyogram (EMG) is at its highest in waking, intermediate in NREM sleep, and lowest in REM sleep; the electroencephalogram (EEG) and electooculogram (EOG), which are both activated in waking and REM sleep and inactivated in NREM sleep. PGO, pontogeniculooccipital; 5-HT, 5-hydroxytryptamine (serotonin); NE, norepinephrine.
966 The AIM Model of Dreaming, Sleeping, and Waking Consciousness
proved propitious to quantify such aspects of consciousness as (1) the sense modalities that are represented and the intensity of the internally generated percepts, (2) the occurrence and strength of self-reflective awareness and executive thought, (3) the dreamer’s orientation in time and space, and dream personnel, (4) the dreamer’s emotion profile (presence and strength of emotions such as elation, anxiety/fear, anger, shame, guilt, sadness, and eroticism), and (5) the identification by the dreamer of the possible memory sources of the dream content. This approach has led to the characterization of dream consciousness as having (1) strong sensorimotor perceptions (with a preponderance of vivid visual imagery as the dreamer moves through a fictive reality); (2) impoverishment of executive ego function (with the delusional belief that one is awake and a failure to develop or sustain logical thinking); (3) discontinuity and incongruity of plot features as the basis of bizarre cognition; (4) potentiation of anxiety, anger, and elation together with a weakening of shame, guilt, and sadness; and (5) inability to specify the memory source of the confabulated dream content in about 80% of the cases. Dreaming is thus characterized by visual hallucinations, by disorientation, by lack of insight and judgment, and by memory loss (with compensatory confabulation). These formal similarities are so strong as to lead to the hypothesis that dreaming, although normal, is a state akin to delirium. Since delirium is caused by diseases and by drugs which interfere with normal neuromodulation, it is natural to wonder if, in normal sleep, there are changes in neuromodulation during the wake–sleep cycle.
Cellular and Molecule Mechanisms of Mammalian Sleep All mammals share with humans the regular periods of NREM and REM sleep. This is so whether the animals are aquatic, terrestrial, or arboreal, and whether they are large surface-dwelling carnivores (e.g., lions) or small nest-dwelling herbivores (e.g., mice or rabbits). As an experimental model, the domestic cat has appealed to neurobiologists because it is so docile and so prodigious a sleeper. As experimental animals, cats are more expensive and more ethically problematic than are rats, but they are large enough to carry the microelectrode, microinjection, and microdialysis array, the equipment necessary to perform physiological and pharmacological experiments. They are well studied neuroanatomically so that stereotaxis is facilitated. Using cats, neuroscientists have shown that the two brain-activated states, waking and REM sleep (with high values of A), are at opposite poles with respect to
both input–output gating (high I in waking, low in REM) and neuromodulation (high M in waking, low M in REM). On all these dimensions, NREM sleep is quite different (low A and intermediate I and M). In addition to demonstrating that aminergic levels decline in NREM sleep and reach their nadir in REM, it has been shown that the cholinergic level declines as animals go from waking to NREM, but rises again and reaches its highest level, in REM sleep, especially in the brain stem. This gives factor M (defined as the ratio of aminergic to cholinergic modulation) a highly differentiating power for distinguishing the three states: M is highest in waking, intermediate in NREM sleep, and lowest in REM sleep. This finding is potentially relevant to our understanding of the brain basis of the many phenomenologic distinctions between waking, sleeping, and dreaming. The mode of information processing has changed dramatically. The importance to REM of the pontine brain stem is demonstrated by the presence of the cell bodies of both cholinergic and aminergic neurons there. Furthermore, it has now been conclusively demonstrated that the microinjection into the pontine tegmentum of both cholinergic agonists and cholinesterase antagonists produces dramatic increases in REM sleep. All of these effects are blocked by pretreatment of the injection sites by atropine. There is no longer any doubt that compared to waking and NREM sleep, REM sleep is hypoaminergic and hypercholinergic. This robust physiological difference correlates with – and hypothetically causes – the psychological differences. Based upon new studies in rats, a flip-flop switch for REM sleep triggering has recently been proposed. Each side of the switch contains g-aminobutyric acid (GABA)ergic neurons, and this resulting mutual inhibition guarantees that when one side is on, the other is off. The REM-on population contains two populations of glutaminergic neurons: one population projects to the basal forebrain and produces the forebrain activation while the other projects to the medulla and spinal cord, producing atonia. The cholinergic system is activated as part of the REM-on switch and can, in turn, activate that side of the switch. The REM-off population includes the dorsal raphe nuclei. At a still deeper level, the activation of protein kinase in the pontine tegmentum has been shown to accompany REM sleep, suggesting that pedunculopontine intracellular protein kinase A (PKA) activation is involved in REM sleep generation.
Input–Output Gating Michel Jouvet called REM sleep ‘paradoxical’ because sleep persists despite the EEG evidence for strong brain activation. A partial explanation of the paradox is
The AIM Model of Dreaming, Sleeping, and Waking Consciousness 967
the simultaneous blockade of sensory input and motor output, the neurophysiological mechanisms of which are now well understood. Ottavio Pompeiano used classical Sherrington reflexology techniques to show that motor output is blocked in REM by descending inhibition from the pontomedullary brain stem to the anterior bone cells of the spinal cord. That this inhibition is induced by powerful and active postsynaptic inhibition of the final common path motor neurons was shown by Michael Chase. Chase also demonstrated that the spinal inhibition of REM is mediated by glycine. As for the inhibition of sensory input, it was also Pompeiano who demonstrated that presynaptic inhibition is associated with the clusters of eye movement during REM sleep. An associated occlusion of sensory input excitation also accompanied the REMs. This cooption of input-processing channels (including the allimportant thalamocortical system) is effected by the internally generated pontogeniculooccipital (PGO) waves, first described by Jouvet. These cortical activation waves were later shown to be of entirely internal origin and were enhanced by cholinergic microstimulation. PGO wave generation is inhibited by noradrenaline and serotonin. The emerging picture of REM sleep is a high level of activation in a brain which is not only off-line by virtue of sensory input and motor output blockade, but is also stimulated by phasic activation signals of its own devising. The coactivated mind is therefore fooled by its own parasitic excitation; the brain-mind then develops the illusion or fictive experience of perceiving and moving through dream space.
Efferent Copy Generation The PGO waves of REM sleep not only constitute internally generated phasic activation signals for the dreaming brain-mind, but they also convey to the thalamus and cortex feed-forward information about the direction of the upcoming eye movements. As such, they are classical efferent copy stimuli from the oculomotor circuits to the visual forebrain. Such eye movement activity can also be recorded in waking when it forms an integral part of the startle response. In waking, the PGO waves rapidly habituate as the startle response diminishes. The second and third stimuli of a train evoke a much weaker or no response because they are no longer novel. The mechanism of this attenuation is thought to be aminergic inhibition of the cholinergic-modulated PGO generator neurons of the lateral pons. The relative continuity of waking consciousness is, in part, a function of PGO wave damping, whereas the bizarre discontinuity of dream consciousness
is a function of PGO wave disinhibition. Dream consciousness reflects this dishabituation by the increase in the emotions of surprise and anxiety. These dream features could be mediated by excitation of the amygdala, a major target of the PGO waves. In REM sleep, the efferent copy information about the direction of eye movement that is conveyed by the PGO system is not integrated with changes in visual input, as occurs in waking, because in sleep there is no visual input. It is tempting to speculate that the efferent copy information that is generated in REM sleep is not only a physiological cause of dream surprise, but is also used in perceptual aspects of dream plot construction. The oculomotor system of the pons is only one of many motor program generators that are activated in REM sleep. Locomotion is commanded but, because the anterior horn cells are hyperpolarized, real motor behavior is not generated and REM sleep dreams reflect this by the intensity of fictive motoric action in dreams. There is hardly a sentence in the REM sleep dream report that does not contain an action verb. We are always walking, running, flying, or swimming in our dreams. Even if we lead sedentary waking lives, stationary activity is not represented in our dreams. The finding of motor pattern generator activation in REM sleep and its correlation with the fictive motility of dreaming is a good example of how the close study of neurophysiology can provide dream theory with a new paradigm and new hypotheses regarding the origin of dream plots. Of course, the approach does not allow us to propose why a given dreamer has a given dream or what that dream might mean. But it does provide encouragement for an alternative way of approaching even interpretive questions. For example, our dreams are full of movement because brain motor pattern generators are activated in REM sleep. Further evidence that this theory may be correct is given by experimental and clinical discoveries, both of which reveal unexpected and unwanted enactment of REM sleep motor commands. The experiments of Michel Jouvet and of Adrian Morrison showed that cats with lesions in the vicinity of the locus coeruleus in the pons evinced REM sleep without atonia. In other words, the cats showed sleep with EEG activation REMs but suddenly stood up and evinced a wide variety of attack and defense behaviors. They were then in a dissociated state of REM sleep in which they expressed automatic behaviors that are normally suppressed by the motor inhibition of REM. On the basis of these observations, Jouvet boldly proposed that the cats were acting out their dreams. That idea gained credence when it was reported by Carlos Schenk and Mark Mahowald that humans
968 The AIM Model of Dreaming, Sleeping, and Waking Consciousness
did precisely the same thing when they became afflicted by what they called the REM ‘sleep behavior disorder.’ Schenk’s and Mahowald’s patients, mostly >50-year-old males, performed motor acts in sleep that corresponded to their dream reports. One patient, dreaming that he was playing football, got up out of bed and tried to tackle a chest of drawers. Another, dreaming that he was diving, stood up on the side of the bed and propelled himself into the baseboard of his bedroom, which he imagined to be a swimming pool. Presumably, these experimental and natural pathological conditions of REM sleep without atonia are due to damage of that subpopulation of glutaminergic REM-on neurons that convey inhibitory commands from the flip-flop switch to the spinal cord. These examples would seem to make more plausible the suggestion that dream consciousness is a function of brain activation in sleep and that the important differences between the dreaming and waking states of consciousness are determined by specifiable differences between the mechanisms of brain activation in the two states. In particular, it is the presence or absence in input–output gating that determines the relationship between the outside world and internal perceptions, beliefs, and actions.
Differences in Regional Brain Activation EEG evidence had long suggested that the brain was similarly activated in waking and REM sleep dreaming. The recent advent of PET imaging technology revealed that this was an oversimplified conclusion. Most brain regions are less active in NREM sleep than in either the wake or REM sleep state. But when REM is compared to the wake state, differences emerge which are of great relevance to studies of conscious state determination. Certain brain regions are more active in REM than in waking. They include the pontine tegmentum (which animal studies have shown to be the probable site of the REM sleep and PGO wave generator), the amygdala (which animal studies have shown to be involved in mediating emotion, especially the anxiety which is so common in dreaming), the parietal operculum (which is thought to mediate visuomotor integration of cardinal perceptual feature of dreaming), and the parahippocampal and deep frontal cortices (which may process emotional data and integrate it with cognitive information). One brain region is notably less active in REM than in waking. The dorsolateral prefrontal cortex (DLPFC) remains at the same low level seen in NREM sleep. Other human studies have implicated the DLPFC in the executive ego functions that are so conspicuously deficient in dreaming: short-term memory,
self-reflective awareness, intentional decision making, and volitional action. The brain lesion studies done by Mark Solms have revealed that two of the structures selectively activated in REM sleep are, when damaged, associated with a complete cessation of dream recall. They are the parietal operculum (damage to which causes problems with sensorimotor integration) and the deep frontal white matter (damage to which causes emotional apathy). Patients often complain of cessation of dreaming following lobotomy, which consists of severance of the deep frontal white matter.
Field Studies of Waking, Sleeping, and Dreaming Consciousness The invention of the ‘Nightcap’, a two-channel event recorder, has made possible the field study of conscious experience in humans as they lead their otherwise normal waking and sleeping lives. In addition to wearing the Nightcap for recording their head and eye movements while asleep, participants carried radio beepers so that they could be contacted throughout the day and night to collect reports of conscious experience (see Figure 3(a)). This combination of techniques allowed us, for the first time, to collect reports of consciousness experience in the same persons, from several brain states, around the clock. Over 3000 reports from ten people ages 20–40 years were elicited from active and quiet waking states, from five intervals during sleep onset and from both NREM and REM sleep. The reports were transcribed and scored for dimensions such as word count (REM reports were 6 times as long as NREM reports), internally generated percepts (REM sleep highest, active waking lowest). These data, shown in Figure 3(b), suggest a general psychophysiological law: thinking is incompatible with hallucination and vice versa. The implications of these findings for conscious state control and for psychiatry are loud and clear. One striking finding was a reciprocal increase in internally generated perception and a decrease in thinking across the five states.
Convergence of Physiology, Psychology, and Philosophy The integration of the fields of psychology and physiology, envisaged by William James and the young Freud over 100 years ago, is now beginning, with sleep and dream science leading the way. The Finnish philosopher of science Antti Revonsuo has recently championed the theory, first put forth by Michael Jouvet, that REM sleep dreaming allows the sleeping brain to run adaptive behavioral programs of fight and flight. According to this view, REM sleep dreaming has a Darwinian function even if dream behavior
The AIM Model of Dreaming, Sleeping, and Waking Consciousness 969 Eyelid movements
Wake REM NREM
Head movements
1:00 2:00 3:00 4:00 5:00 6:00 7:00 Time
a Thoughts
Hallucinations 100 Reports with halluclnations (%)
Reports with thoughts (%)
100 80 60 40 20 0 b
80 60 40 20 0
Active Quiet Sleep NREM REM wake wake onset
Active Quiet Sleep NREM REM wake wake onset
Figure 3 (a) Central arousal accompanying the activated states of rapid eye movement (REM) sleep and waking can be measured using the ‘Nightcap,’ a simple ambulatory monitor. The Nightcap is a two-channel recording device that distinguishes waking, REM and NREM sleep. One channel of the Nightcap monitors eye movement and the other monitors body movements. The Nightcap eyelidmovement readout is thought to reflect activity in portions of the brain stem oculomotor nucleus that innervate the eyelid and are adjacent to portions of the medial brain stem ascending reticular system, the activity of which, in turn, generates forebrain activation. (b) Decline in directed thought and reciprocal increase in hallucinations during progression from active waking through sleep onset and NREM to REM sleep.
is fictive. For the German philosopher Thomas Metzinger, the occurrence of lucid dreaming, out-ofbody experience and dreaming itself, supports his phenomenal self-model of consciousness. The phenomenal self is a constantly renewed functional state of the brain whose vicissitudes can, for the first time in human history, begin to be explained.
AIM: An Integrated Model of the Human Brain Mind Using physiological measures, it is now possible to create a three-dimensional model of brain-mind state space (see Figures 1 and 4). Activation, assessed from EEG and/or thalamocortical cellular activity, gives values and axis A, running from left (low) to right (high) across the front wall of the state space. Input– output gating is measured as EMG activity, values of H-reflex, and PGO waves. It runs from the front to the back of the state space. The vertical axis, M, measures the ratio of the strength of aminergic to cholinergic neuron modulation. Unfortunately, factor
A
Low
High w
Aminergic Sleep cycle 1 2 NREM 3 4 M External REM
I
Cholinergic Internal Figure 4 The three-dimensional activation/information/mode (AIM) state space model showing normal transitions within the AIM state space, from wake, to non-rapid eye movement (NREM), and then to REM sleep. REM occupies the lower righthand front corner, in which activation is high, input is entirely internal, and the forebrain is cholinergically activated and aminergically demodulated. ACh, acetylcholine; NE, norepinephrine; 5-HT, 5-hydroxytryptamine.
970 The AIM Model of Dreaming, Sleeping, and Waking Consciousness
M cannot yet be measured in humans, but pharmacological studies indicate that inferences from neurobiological studies in animals are valid. In the model, time is the fourth dimension and the solution of AIM is constantly changing, even in the waking domain (at the far right, upper, rear corner of the state space) as we change the focus of attention, day dream, or enter altered states such as hypnosis. We may become drowsy, doze, or fall frankly asleep, in which case AIM moves down, forward, and to the left and then occupies the NREM sleep domain in the center of the state space. Finally, AIM moves to the REM sleep domain in the right front lower corner of the state space. During a normal night of sleep, AIM function follows an elliptical trajectory that repeats itself 4 or 5 times per night. The ellipse shifts sequentially to the right and to deeper parts of the state space in successive cycles. These elliptical orbits in AIM state space conform to the mathematical description of the reciprocal interaction model, giving an internally consistent picture of sleep physiology. Consciousness is most intense in the right portion of the state space and lowest on the left. It is interoceptive toward the front of the state space and exteroceptive toward the back. The kind of consciousness is given by the mode dimension. It is highest at the top of the state space and lowest at the bottom. Abnormal states of consciousness such as narcolepsy, the REM sleep behavior disorder, delirium, and other psychoses can also be modeled in the normally forbidden zones of AIM state space. See also: Dream Function; Dreams and Dreaming: Incorporation of Waking Events; Dreams and Nightmares
in PTSD; Dreams, Dreaming Theories and Correlates of Nightmares; Sleep and Sleep States: Phylogeny and Ontogeny; Sleep Mentation in REM and NREM: A Neurocognitive Perspective; Sleep Research and Sleep Medicine in Historical Perspective.
Further Reading Amini-Sereshki L and Morrison AR (1986) Effects of pontine tegmental lesions that induce paradoxical sleep without atonia on thermoregulation in cats during wakefulness. Brain Research 384(1): 23–28. Bandyopadhya RS, Datta S, and Saha S (2006) Activation of pedunculopontine tegmental protein kinase A: A mechanism for rapid eye movement sleep generation in the freely moving rat. Journal of Neuroscience 26(35): 8931–8942. Hobson JA, Pace-Schott EF, and Stickgold R (2000) Dreaming and the brain: Toward a cognitive neuroscience of conscious states. Behavioral and Brain Sciences 23: 793–842. Jouvet M (1962) Recherche sur les structures nerveuses et les mechanismes responsables des differentes phases du sommeil physiologique. Archives Italiennes de Biologie 100: 125–206. Jouvet M (1973) Essai sur le reve. Archives Italiennes de Biologie 111: 564–576. Jouvet M, Vimont P, and Delorme F (1965) Elective suppression of paradoxical sleep in the cat by monoamine oxidase inhibitors. Comptes Rendus des Seances de la Societe de Biologie et de ses Filiales 159(7): 1595–1599. Lu J, Sherman D, Devor M, et al. (2006) A putative flip-flop switch for control of REM sleep. Nature 441(7093): 589–594. Metzinger T (2003) On Being No One. Cambridge: MIT Press. Revonsuo A (2005) Inner Presence: Consciousness as a Biological Marker. Cambridge, MA: MIT Press. Schenck CH and Mahowald MW (1996) REM sleep parasomnias. Neurological Clinics 14: 697–720. Solms M (1997) The Neuropsychology of Dreams: a ClinicoAnatomical Study. Mahwah, NJ: Lawrence Erlbaum Associates. Yamuy J, Fung SJ, Xi M, et al. (2004) Hypocretinergic control of spinal cord motor neurons. Journal of Neuroscience 24(23): 5336–5345.