Metzinger
patterns of brain activity in dreaming
the functional benefits of dreaming
Borges
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As a consequence of deactivation of the dorsolateral prefrontal cortex (DLPFC) during sleep, executive functions such as self-consciousness and analytical thought are severely impaired in NREM sleep and are weak in REM sleep."
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The changes in EEG activity throughout the sleep-wake cycle.
Brodmann areas considered to form (a) the dorsolateral prefrontal cortex (DLPFC; dorsal surface of the left hemisphere is shown), and (b) the ventromedial prefrontal cortex (VMPFC; median plane cut of the right hemisphere).
DLPFC: working memory.
VMPFC: decision making; somatic marker.
Executive functions of the prefrontal cortex that are most relevant to the self-conscious awareness: self-observation, planning, prioritizing and decision-making.
These are, in turn, based upon more basic cognitive capacities such as attention, working memory, temporal memory and behavioral inhibition.
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The AIM model, after Hobson, J. Allan, Pace-Schott, E. and Stickgold, R. (2000), DREAMING and the BRAIN: Toward a Cognitive Neuroscience of Conscious States, Behavioral and Brain Sciences 23 (6).
The activation parameter (A) is derived from the inverse of the voltage amplitude of the EEG which varies from 25-50 mV in waking to 150-200 mV in stage IV NREM sleep in humans (x4 range).
The input (I) source parameter can be derived from arousal threshold or H-reflex amplitude in humans (x4 range).
The modulatory parameter (M) is derived from the mean discharge rate of the aminergic populations (2-4 c/s in waking, 1-2 c/s in NREM, 0.01-0.1 c/s in REM) or from the concentration of norepinephrine, serotonin or acetylcholine in microdialysis studies (x10 range).
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Roughly speaking, the three posited dimensions are meant to capture respectively:
NE: norepinephrine;
5-HT: serotonin
(5-hydroxytryptamine).
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One use of the AIM model is to depict the highly dynamic and variable nature of human consciousness, and thus to visually plot specific "states" of consciousness within the state space. As an example, normal consciousness, at the coarsest level, can be divided into the states of waking, REM and NREM sleep. Each of these states can be characterized both by distinct physiologies and by distinct differences in mentation.
The positions of these three states in the AIM state space, as well as the trajectory from waking through NREM into REM sleep, are shown here.
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Each individual will take a unique path through the state space from waking to NREM, depending on both the relative and absolute rates of decline of each of the three state space parameters.
For example, if an individual is drowsy before retiring, values for "A" and perhaps also "M" will begin to drop well before the subject even goes to bed, while "I" remains high, placing one in the center of the back surface of the cube.
In contrast, if an individual is quite alert when going to bed, "I" might drop before either "A" or "M" (not shown), followed by a small drop in "A" as alpha patterns appear in the EEG.
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As the subject moves from wake to sleep onset, further movement occurs within the state space. The box labeled "Rapid" represents a possible initial sleep onset state when the transition from waking to sleep is precipitous following sleep deprivation. In this case, the transition occurs before there is time for aminergic neuromodulatory levels to decrease. As a result, the "M" function remains on the top surface of the cube (modulation highly aminergic) while brain activation and external inputs diminish.
In contrast, the box labeled "Slow" represents a gradual transition from waking to sleep as might be seen in situational insomnia. In this case, decreases in aminergic neuromodulation and external inputs might occur prior to the decrease in brain activation. In both cases, AIM would then move into the standard NREM position.
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Under normal circumstances, dreamers believe themselves to be awake but occasionally individuals become aware that they are dreaming. In this state of "lucid dreaming" (Laberge 1990, 1992) waking insight combines with dream hallucinosis in an intriguing and informative dissociation. We assume that for lucidity to occur, the normally deactivated prefrontal cortex must be reactivated but not so strongly as to suppress the pontolimbic systems signals to it. This dissociation is represented in the AIM model by splitting AIM so the portion representing prefrontal cortex can take a position dissociated from that of the rest of the brain. When this occurs, internally generated images are seen for what they are and are not misinterpreted as coming from the outside world.
The phenomenon of lucidity clearly illustrates the always statistical and always dissociable quality of brain-mind states. AIM accommodates these features very well by proposing that lucid dreaming is a hybrid state lying across the wake-REM interface.
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In the REM sleep behavior disorder, the normal inhibition of motor output during REM fails. Motor behaviors normally seen only in waking now arise completely involuntarily and automatically during REM, and patients physically act out their dreams. The historically oriented reader will recognize the similarity between this disorder and the dissociative phenomena that interested Charcot, Janet and Freud.
During REM sleep, automatic motor cortex activation produces outputs similar to those seen in waking, but in response to exclusively internal inputs. Since the inhibition of spinal motorneurons usually occurs in concert with motor cortex activation, our single "I" parameter normally reflects the net inhibition of motor output. But in this case (as in the case of lucid dreaming) we represent this regional dissociation by a fragmenting of the AIM icon. In this case, the lower back quarter of the icon, representing brainstem output systems, has moved back in the state space toward a waking level of output. It is this dissociation which produces the REM sleep behavior disorder.
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Drugs which, like LSD, interfere with serotonergic neuromodulation create dreamlike distortions of imagery and inhibit executive prefrontal cortical functions during waking, while anticholinergics (e.g., scopolamine) produce a delirious waking state with dream-like hallucinosis, disorientation, anxiety and confabulation.
As seen here, scopolamine pushes AIM above the normal state space, pharmacologically reducing the levels of cholinergic neuromodulation below any normal physiological levels. At the same time, AIM splits as both external and internal inputs are activated.
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Three major questions seem to us to be ripe for resolution through constructive debate:
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During dreaming, prefrontal deactivation leads to illogical thinking (ad hoc explanations, prominent mnemonic deficits, bizarre uncertainties).
Hypofrontality is associated with pathological temporal limbic activation in epilepsy; reciprocal inhibition between frontal and limbic areas has been linked to depression and schizophrenia.
REM dreaming might be a normal physiological state that is analogous to psychopathological conditions in which limbic hyperactivation is combined with frontal hypoactivation.
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(A). Perform an action (initially random; later, it is the best action found in (C)).
(B). Generate several self-models to match sensor data collected earlier.
(C). Generate several possible actions that disambiguate competing self-models.
(D). Use the currently best model to generate locomotion sequences through optimization.
(E). Execute the best locomotion sequence by the physical actuator.
(F). Continue to refine models (B), or to create new behaviors (D).
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The robot performs a random action (A). A set of random models, such as (B), is synthesized into approximate models (C). A new action is then synthesized to maximize model disagreement and is carried out (D), after which further modeling ensues. This cycle continues for a fixed period or until no further model improvement is possible (E and F).
The best model is then used to synthesize a behavior. In this case, the behavior is forward locomotion, the first few movements of which are shown (G to I). This behavior is then carried out (J to L). Next, the robot suffers damage [the lower part of the right leg breaks off (M)]. Modeling recommences with the best model so far (N), and using the same process of modeling and experimentation, eventually discovers the damage (O). The new model is used to synthesize a new behavior (P to R), which is executed by the physical robot (S to U), allowing it to recover functionality despite the unanticipated change.
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Distance traveled during optimized versus random behaviors.
Dots indicate the final location of the robot's center of mass, when it starts at the origin. Red dots indicate final positions of the physical robot when executing random behaviors. Black dots indicate final expected positions predicted by the 30 optimized behaviors when executed on the self-model (Fig. 2F). Blue dots denote the actual final positions of the physical robot after executing those same behaviors in reality. The behaviors corresponding to the circled dots are depicted in Fig. 2, G to L. Squares indicate mean final positions. Vertical and horizontal lines indicate 2 SD for vertical and horizontal displacements, respectively.
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LaBerge (1990): "Lucid" dreamers (the term derives from van Eeden, 1913) report being able to freely remember the circumstances of waking life, to think clearly, and to act deliberately upon reflection, all while experiencing a dream world that seems vividly real.
About 20% of the population reports having lucid dreams once a month or more.
We [LaBerge et al.] provided the necessary verification by instructing subjects to signal the onset of lucid dreams with specific dream actions that would be observable on a polygraph (i.e., eye movements and fist clenches). Using this approach, LaBerge, Nagel, Dement & Zarcone (1981) reported that the occurrence of lucid dreaming during unequivocal REM sleep had been demonstrated for five subjects. After being instructed in the method of lucid dream induction (MILD) described by LaBerge (1980b) the subjects were recorded from 2 to 20 nights each. In the course of the 34 nights of the study, 35 lucid dreams were reported subsequent to spontaneous awakening from various stages of sleep.
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It might be objected that lucid dreamers might simply not be attending to the environment.
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The evidence is clear: lucid dreaming is an experiential and physiological reality; though perhaps paradoxical, it is clearly a phenomenon of sleep.
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For the first lucid epoch, beginning with the initiation of the signal, the sleep stage was unequivocal REM in 70 cases (92%). The remaining six SVLDs were less than 30 s long and hence technically unscorable "by the book". For these cases, the entire SVLD was scored as a single epoch; with this modification, all SVLDs qualified as REM. The lucid dream signals were followed by an average of 115 s (range: 5 to 490 s) of uninterrupted REM sleep. Physiological comparison of EM, HR, RR, and SP for lucid vs. non-lucid epochs revealed that the lucid epochs of the SVLD REM periods had significantly higher levels of physiological activation than the preceding epochs of non-lucid REM from the same REM period.
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There are two distinct ways in which lucid dreams are initiated. In the usual case, subjects report having been in the midst of a dream when a bizarre occurrence causes sufficient reflection to yield the realization that they are dreaming. In the other, less frequent case, subjects report having briefly awakened from a dream and then falling back asleep directly entering the dream with no (or very little) break in consciousness. Here is an example of a wake-initiated lucid dream:
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Four channels of physiological data (central EEG [C3-A2], left and right eye-movements [LOC and ROC], and chin muscle tone [EMG]) from the last 8 min of a 30 min REM period. Calibrations are 50 microV and 5 s.
Upon awakening the subject reported having made five eye movement signals (labeled 1-5 in figure).
The first signal (1, LRLR) marked the onset of lucidity. During the following 90 s the subject "flew about" exploring his dream world until he believed he had awakened, at which point he made the signal for awakening (2, LRLRLRLR).
After another 90 s, the subject realized he was still dreaming and signaled (3) with three pairs of eye movements. Realizing that this was too many, he correctly signaled with two pairs (4).
Finally, upon awakening 100 s later he signaled appropriately (5, LRLRLRLR).
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Example: addressing the question of how long do dreams take.
The ratio of dreaming/reality time can be estimated as follows: have the subjects track the tip of their fingers moving slowly left to right during four conditions: 1) awake, eyes open; 2) awake, eyes closed mental imagery; 3) lucid dreaming; and 4) imagination ("dream eyes closed") during lucid dreaming. The subjects showed saccadic eye movements in the two imagination conditions (2 and 4), and smooth tracking eye movements during dreamed or actual tracking (conditions 1 and 3).
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Sixteen channels of physiological data, including EEG, EOG, EMG, respiration, skin conductance level (SCL), heart rate, vaginal EMG (VEMG) and vaginal pulse amplitude (VPA), were recorded from a single subject. The experimental protocol called for her to make specific eye movement signals at the following points: when she realized she was dreaming (i.e., the onset of the lucid dream); when she began sexual activity (in the dream); and when she experienced orgasm.
The subject reported a lucid dream in which she carried out the experimental task exactly as agreed upon. Data analysis revealed a significant correspondence between her subjective report and all but one of the autonomic measures; during the 15 second orgasm epoch, mean levels for VEMG activity, VPA, SCL, and respiration rate reached their highest values and were significantly elevated compared to means for other REM epochs. Contrary to expectation, heart rate increased only slightly and non-significantly.
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Cf. Wittgenstein (On Certainty, prop. 90e):
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Oh, incompetence! Never can my dreams engender the wild beast I long for. The tiger indeed appears, but stuffed or flimsy, or with impure variations of shape, or of an implausible size, or all too fleeting, or with a touch of the dog or the bird.