Some background: I recently went to see Christopher Nolan's film Inception with a large group of friends. As the only neuroscientist in the group, I was, of course, asked my opinion of the films scientific plausibility. Asking for some time to formulate a thought out response, I realized that a short review would make for a perfect blog post. Four days and six pages of typing later, I'm posting some of my thoughts. [Authors note. A few official caveats: first, the post below contains some spoilers, and so would most likely be enjoyed most by someone who has already seen the film. Secondly, I am not a sleep researcher, and so am in no way an expert on the complex biological processes occurring during sleep. Lastly, much of my knowledge of the biology of sleep is gained from the excellent textbook Fundamental Neuroscience 3rd ed. Edited by Squire et al. 2008.]
I really enjoyed Inception. I think it’s a challenging film that assumes, even demands, an audience comprised of intelligent individuals. While the film did contain the pyrotechnics we expect from a filmmaker with Christopher Nolan’s CV, the action was gratifyingly overshadowed by the prevalent psychological themes. From my theatre seat, the themes of Inception were that an individual’s dreams are both an infinite battlefield and a powerful weapon, and that our conscious perception of reality is a mercurially fragile construct. Given this, the plot could hardly have avoided making basic assumptions about the nature of dreams and consciousness. Furthermore, given the specific story, I fully expected to be presented with various fictional technologies that would allow Nolan’s character to enact their mental shenanigans; for the record, I was not disappointed. In the past, I have found that the best way to watch films whose plots stray into the realm of neuroscience is to firmly suspect disbelief; this saves me a lot of mental pain when I compare the reality of our knowledge/technology with the principles (both theoretical and practical) that are presented to the audience within the confines of a fictional film.
Nevertheless, in the case of Inception, I am more than willing to provide a brief analysis of the various principles feature within the film. As with most complex storylines, the plausibility of these various bits vary between complete flights of fancy to moderately based on current knowledge. Inception is a long film – to exhaustively deconstruct the biological plausibility behind ever scene would require a considerable effort. I will therefore discuss only the most prominent examples of neuroscience-themed plot points within the film, also spending some time discussing what neuroscience knows about sleep and dreams. I would caution those who have not yet seen the film to avoid reading further, as there will invariably be spoilers below the break.
As I commented before, Inception was a long film containing many concepts loosely related to the neuroscience of dreaming. I will not attempt to cover all the concepts touched upon in the film – however I hope to highlight a few of the more interesting ones. Of course, the most glaring example of pseudo-neuroscience is the concept of shared dream states, upon which the entire film is based. Our introduction to this guiding principal occurs at the very beginning of the film, and although the script spends some energy explaining other aspects of the dream state (e.g. the role of the Architect in creating the dream landscape), at no time is the underlying principle questioned or discussed, that individuals can share dreams without the aid of any external technology. Examining this assumption is a blog post in and of itself, one likely to be a rather lengthy discussion of the nature of dreaming and consciousness. As I gear up to tackling these subjects (which will most likely appear in a later post), I will first set them aside to examine a few of the other neuroscience-related plot details contained within Inception. First, I’ll briefly discuss the sleep cycle, comparing what research has demonstrated with Inceptions version. Next I’ll talk about which brain areas are active during dreaming, and whether the remarkable levels of cognition displayed by Inceptions dreaming characters are possible given what we know about the sleeping brain. Lastly, I’ll talk about the technology (or lack thereof) used to facilitate Inceptions dream states.
The Sleep Cycle:
The advent of neuroimaging techniques such as functional MRI allowed neuroscientists to view brain activity during classic states, including sleep. We therefore have a pretty good understanding of what brain regions are active during sleep. Classic studies of brain activity during sleep identified multiple stages of sleep (non-REM, which is divided into the sub-stages of N1, N2 and slow-wave sleep, and REM) each possessing a characteristic profile of brain activity. The sleep seen during Inception is remarkably homogenous. Research has shown us that, generally, dreams only occur during REM sleep (although night terrors do occur during non-REM sleep). Furthermore, the progression through the various sleep stages during a sleep cycle (generally described as N1 to N2 to slow-wave to N2 to REM) is highly periodic, with the cycle lasting for 90-100 minutes. Any individual sleep cycle (a sleep will experience multiple cycles during a nights worth of sleep), will be 20-25% REM sleep, with the remaining time taken up by non-REM sleep (Squire et al, 2008). The ratio between REM and non-REM sleep evolves over the course of the night, with earlier sleep cycles dominated by non-REM sleep, with REM sleep (and therefore dreaming) brief or nonexistent. This ratio reverses during the final cycles of the night. During the course of Inception, the immediate entrance into a dream state by the actors is somewhat implausible – we might expect real sleepers to go through multiple sleep cycles before experiencing a dream, or at least hang around in non REM sleep before entering REM sleep (with a possible exception discussed below).
The Sleeping Brain:
The transition between wakefulness and sleep is characterized by widespread deactivation of the brain, in particular the forebrain and brain stem. Brain activity further decreases as sleep transitions from non-REM sleep stage N1 to non-REM sleep stage N2 and then on to slow-wave sleep. During REM sleep, when dreaming occurs, selective brain regions show reactivation to levels equivalent or above waking levels; these regions include areas in the brain stem, diencephalic, subcortical limbic, cortico-limbic, and selected cortical association areas. Additionally, REM sleep is characterized by active suppression of motor activity and presynaptic inhibition of sensory signals (Squire et al 2008).
These patterns of activity (or lack thereof) have been directly associated with the features of dreams that distinguish the dream perceptual experience from wakefulness. The phenomenology of the dream-state was poetically described: “Perception, instead of being shaped by external forms, becomes hallucinatory. Cognition is similarly deranged. Instead of being oriented, the dreaming mind looses track of time place and person. Instead of thinking actively and critically, the dreaming mind indulges in non-sequiturs, ad-hoc explanations, and other illogical whims. Memory, during dreams, is fragmented in its disconnection from current events and globally deficient in recalling them. Emotion, instead of being restrained and focuses in response to percepts and thoughts, comes to dominate and organize dreaming consciousness often in strikingly salient ways.” (Squire et al. 2008) Activation of the limbic brain is thought to underlie the strong emotional salience of dreams, whereas continued deactivation of prefrontal regions results in the illogical nature of dreams, as well as the deficits in cognition and memory. Selective activation of multimodal association cortices may underlie the hyper-associative quality of dreaming. Active motor suppression prevents the acting out of dreams, and presynaptic inhibition of sensory signals prevents the processing of external sensory signals.
We can compare some of the specific details of Inceptions dream states with the neuroscience based principles of dreaming suggested from the observed patterns of brain activity during dreaming. A prime example is the comment by DiCaprio’s character regarding time flow and logic within the dream. [Spoiler warning]. In the scene where DiCaprio introduces Ellen Page’s character to the dream state, he demonstrates (at the Parisian café) the non-linearity of dream, specifically how the flow of time within a dream is often interrupted by unpredictable jumps. However, despite this verbal acknowledgement, action within the dream states proceeds with remarkable logic with the dreamers displaying a level of cognition, orientation, and memory that neuroscience would not predict given the wide ranging inactivation of prefrontal brain regions during REM sleep.
Another instance of partial plausibility is the focus on the emotional content of dreams. [Spoiler warning]. A major plot point concerns DiCaprio’s subconsciousness infiltrating the content of his dreams with his emotions regarding the death of his wife. During REM sleep, limbic structures such as the amygdale show high levels of activation, and dream content is generally highly emotionally valiant. However, given the deactivation of memory regions, dreams would be unlikely to feature the highly detailed memories and focused emotional construct so specifically produced by DiCaprio’s subconciousness. More plausible would have been an overarching emotional valiance, and the appearance of constructs associated with the emotional content; if the specific emotional event (the wife’s death) were to be replayed in the dream state, we would expect that memory to be fragmented. Furthermore, neuroscience would predict that while dreaming, DiCaprio’s character would exhibit global deficits in recalling the specific memories underlying his emotions, rather than the highly specific recall he displays in the scene where Page’s character enters his dreams.
A point I wanted to briefly mention is the idea of transitioning out of sleep. Given the length of this post, I’m going to address sleep-to-wake transitions in a later post, but I did want to lay some groundwork. Inception is highly concerned with the sleep-to-wake transition. Indeed, the woken sleepers ability to recognize this transition is at the heart of the emotional arc of DiCaprio’s character. Research has shown us that, contrary to the elaborate efforts displayed during the film, a person is easily awakened from REM sleep by meaningful stimuli (such as their name), although they will not react to other external noises. Again, in a later post, I plan to discuss what we know about the biology behind the sleep-to-wake transition, whether Nolan really needed to dump DiCaprio in a bathtub of cold water, and the potential existence of sleep disorders similar to that afflicting DiCaprio’s wife.
Returning now to a point made above, that Inception’s instant entrance into a dreaming state ignores neurosciences evidence that the progression from wakefulness to REM sleep and dreaming involves a series of transitions through a variety of brain states. It is worth noting, that studies of lucid dreaming report the occurrence of direct transitions between sleep and dreaming states. The idea of lucid dreaming appears to be a guiding principle behind the dream states of Inception. A lucid dream is defined as a dream in which the sleeper is aware that he/she is dreaming. Unfortunately, studies of lucid dreaming do not have a strong presence in reputable scientific journals (although in the a graduate of Stanford University, Dr. Stephen LaBerge made initial steps in the late ‘70s to bring lucid dreaming into the realm of peer-review psychophysiology – a note that Dr. LaBerge has since founded a company, the Lucidity Institute, dedicated to teaching the art of lucid dreaming). A PubMed search for “lucid dreaming” returns only 40 results, with the 3 most recent articles published in the Australian and New Zealand Journal of Psychiatry (Been and Garg, 2010, a case study where PTSD nightmares were treated with psychoeducation on lucid dreaming), Conscious Cognition (Soffer-Dudek and Shahar, 2009, a longitudinal study of co-occurrence of sleep-related experience and life events in young adults), and Sleep (Voss et al. 2009, the only published study locatable on PubMed in which brain activity was measured (by EEG) during lucid dreaming). In this last study, researchers made 19-channel EEG recordings from sleeping participants, observing an increase in the power of various frequency bands (especially in the 40-Hz frequency band) and greater synchrony between activity from different electrodes, when comparing activity during lucid dreaming to activity during REM sleep. From their results, the authors conclude that brain activity during lucid dreaming share similarities to activity observed during waking, and speculate that lucid dreaming involves activation of prefrontal regions, an area that is normally inactive during REM-sleep. Unfortunately, direct testing of their hypothesis that lucid dreaming involved reactivation of prefrontal regions was not possible given their use of EEG (which does not allow a fine degree of signal localization). I was unable to find evidence of published fMRI studies of brain activity during lucid dreaming; it is highly likely that such studies have not been undertaken, leaving neuroscience with little to say on the subject of the underlying mechanisms of lucid dreams and whether Inceptions dream states are a) meant to be examples of lucid dreams and b) if so, whether such states are biologically plausible.
A third comment is regarding the technology being used. The transition between wakefulness and unconsciousness is a complex biochemical process, which involves the coordinated activity of multiple brain regions and neural chemicals. To date, all the interactions are not fully understood; however there is a large body of research describing both intrinsic neurochemicals playing a role in sleep, as well as medically relevant compounds capable of promoting the brain to enter an unconscious state.
The neural mechanisms responsible for transitions between wakefulness and the various sleep stages are of decided interest to several research laboratories, and there is a growing body of work describing the various brain regions and chemicals responsible. I won’t go into specifics here, but will mention that there are multiple, complex interactions underlying the sleep cycle. In the context of the film, which for the most part avoids discussing the heterogeneity of sleep itself (see above), I will mention that finding that certain chemicals can promote different sleep stages – critical for the potential plausibility of Inception is the finding that organophosphate insecticides directly activate the neural circuits responsible for dreaming, and have therefore been reported to induce vivid dreams and dream-like hallucinations during wakefulness.
Within the film, the importance of heavy sedation for the establishment of rich dream states is an important plot point. The script is understandably cautious about naming specific chemicals, as the biological mechanisms of most commonly used sedatives are complex. Furthermore, most of the chemicals used in medical procedures do no result in the enhancement of dream-like states. However, classes of drugs called dissociatives have been reported to induce cognitive states similar those that desired in the film. Distinct from psychedelics (where users experience cognitive alterations while fully alert), most dissociatives act as sedatives, additionally producing vivid dream-like states, potentially by reducing signaling between conscious perception and other brain regions. However, there is relatively little scientific research on the effects of these chemicals on human brains, seeing as how many dissociative compounds enjoy a dubious legal status. Nevertheless, we might imagine that the sedative drug displayed during Inception could act as an inducer of such a dream-like state. Alternatively, these fictional chemicals could act to promote the transition from wakefulness to REM sleep, with a further action to prevent the natural procession of sleep-states, effectively holding the sleeper in REM sleep.
The Purpose of Dreams:
One of the guiding questions I was asked immediately after the film was “why do we dream?” It’s a good question. Although neuroimaging has provided a solid glimpse into which brain areas function during sleep and dreaming, a major unresolved question is the exact function of sleep and dreaming. Many studies have sought to answer this question, and have shown that sleep is required for the maintenance of metabolic caloric balance, thermal equilibrium, immune competence, and consolidation of recently formed memories. This last function has been extensively studied, with research showing that different stages of sleep are critical for the consolidation of different forms of memory: REM sleep for procedural memories, slow wave sleep for explicit/declarative memory, both REM and slow wave for emotional memories. As for dreaming, a study tracking REM sleep dream content has been shown to predict the occurrence of clinical depression following martial divorce/separation (Cartwright et al, 1998), which may suggest that dreaming serves to modulate emotional states during waking. Additionally, dreaming is thought to play a critical role in strengthening associative memory networks, with evidence coming from studies showing that people woken from REM sleep show preferential activation of more distantly related associations than seen during waking or after non-REM sleep (Stickgold et al, 1999). But despite several lines of sleep research, neuroscience still lacks an overarching explanation of why we sleep and dream.
Here ends this review – as promised multiple times above, I hope to conclude with a second part discussing the transition between sleep and wakefulness and the concept of shared dreams.