Is anyone in there?
How can we tell if someone is aware of what is going on around them? One strategy is to look at their eyes. Eye contact and dilated pupils are a good sign someone is actively engaged in a conversation. If they’re staring off into space or flickering open and shut, it’s a good sign they aren’t fully present. Things aren’t always as simple: that stranger next to you on the bus with their earphones in could be completely blocked off from their surroundings, or they could be covertly eavesdropping on your personal phone call. In these cases, we have the option of probing the individual, perhaps by saying something surprising to get a better sense of their state of awareness. Things become a bit more complicated if we want to know if someone is aware of their surroundings but they are unable to respond. This exact case can arise in Guillain-Barre syndrome (GBS) an inflammatory condition where both sensory inputs and motor outputs, including eye movements, are blocked. The state where a brain can be shut off from both inputs and outputs while still aware of its own existence has been termed an ‘Island of Awareness’ and is the topic of a recent opinion piece published in Trends in Neurosciences (Bayne, et al. 2019).
The authors describe an island of awareness as “conscious states that are neither shaped by sensory input nor able to be expressed by motor output”. As an example, we enter a similar state each night when we enter REM sleep. Neuromodulators gate sensory inputs and motor outputs effectively isolating the brain. While detached from the world, a conscious internal state generates vivid hallucinations we call dreams. We are aware of something, but that something has no basis in the outside world and we have no way of acting upon it (except in the case of sleep walking). Dreaming, however, is not a true island of awareness in the sense that strong sensory inputs can still penetrate our awareness and reconnect us with the outside world, and that we can then share the stories of our nocturnal hallucinations.
A dramatically different situation arises when a brain, or part thereof, is truly isolated from all of its surroundings. This situation arises following a hemisphereotomy to treat adolescent epilepsy in which an entire hemisphere of the brain is disconnected from the rest of the brain, including the brain stem (where motor commands are sent) and the thalamus (where most sensory information is relayed). While the healthy half of the brain is able to continue to function normally (displaying a remarkable amount of plasticity in picking up the slack), the pathological half is kept alive with normal blood flow maintained. This island of brain has no inputs from the outside world and no ability to command an output, but it still may have an internal sense of what it once was: a part of a complete whole, with memories and desires. Would this large chunk of tissue, which pre-surgery was part of the whole that was ‘you’, notice something was missing? Would it continue dreaming, meditating, or ruminating about the last hours or moments it had before going under general anesthesia? Or would the lack of sensory input or sense of agency quickly push it towards a state as interesting as the appendix, a piece of vestigial tissue, preserved but doing nothing and definitely not questioning its own purpose.
These are questions that are, by construction, very hard to answer. One way to infer the internal state of a piece of neural tissue is to look at its gross electrical activity to see how it compares to a normal, fully connected, piece of tissue. If it shows no activity, or highly aberrant activity relative to normal function, than we can infer that the island of tissue is not functioning in any standard way and is highly unlikely to to be aware. If, on the other hand, neural activity that closely resembles that of an intact brain is found inside a cortical island, than it becomes more plausible that some level of awareness has persisted. Unfortunately for those of us who fear one day finding that we are functionally buried alive in our own heads, evidence is pointing in the direction of isolated brains appearing to behave, at least on a macro level, much like our own.
The most clear cut demonstration of this correspondence compared the activity of a normally developing human brain to that of an artificial brain ‘organoid’ that is made up of artificial neurons derived from human stem cells but has never had any sensory input from the outside world (Trujillo, et al., 2019). The activity patterns of the artificial brain island closely tracked those of the normally developing human brain across time, suggesting many of the same complex neural processes occur. It’s difficult to know whether this complexity on its own really means anything, or if it implies this islands are somehow generating internal experiences. Since we wont be able to go in and ask islands of neural tissue if they are thinking, perhaps a technique that has been used successfully to probe the internal states of patients in comas can shed some light.
Perturbational Complexity Index (PCI) is a technique developed to non-invasively determine if a given brain is capable of consciousness. The motivation for this technique came from a study that used transcranial magnetic stimulation (TMS) to stimulate the brains of awake and asleep participants (Massimini et al., 2005). When the awake brains were ‘zap’ed, there brain waves showed a sharp increase in activity at the site of the ‘zap’ followed by waves of activity throughout the brain. However, when individuals were ‘zap’ed during the deepest phase of sleep without dreaming (known as slow wave or non-REM sleep), the boost in activity did not spread to brain regions beyond the stimulation site. This suggests that awareness might come from the ability to integrate information across diverse brain regions, like how your awareness of a baseball game comes from a combination of the sights, sounds, smells, and emotions generated across the brain.
To quantify the amount of information processing induced by a ‘zap’, activity from across the brain was recorded from electrodes placed on top of the scalp. This information was then ‘zip’ed or compressed like how you compress a file before you email it. When the file size of these compressed files was compared across conditions (the Perturbational Complexity Index mentioned earlier), it was found that conscious states always produced a value >0.4 while unconscious states, either through sleep or under various anesthetics, produced a PCI <0.3 (Casali, et al., 2013). The zap-zip test as it has been called, has been verified in a variety of patient groups including those in a vegetative states (low PCI indicating, no awareness) and those with locked-in syndrome (high PCI, indicating awareness) (Casali et al., 2013; Casarotto et al., 2016).
A technique like the zap-zip test could be utilized on islands of neural tissue to probe there capacity for awareness. It is not entirely clear however, what a positive reading (PCI>.4) would mean or what the proper response would be. Should an aware piece of matter be given rights (see a nice discussion of similar issues here)? Should it be protected to preserve its state of being, or destroyed to prevent any potential suffering? These are questions we may soon have to grapple with as our tools to probe awareness are developed and deployed across islands of potentially intelligent matter.
Bayne, Tim, Anil K. Seth, and Marcello Massimini. “Are there islands of awareness?.” Trends in Neurosciences (2019).
Trujillo, Cleber A., et al. “Complex oscillatory waves emerging from cortical organoids model early human brain network development.” Cell Stem Cell 25.4 (2019): 558-569.
Massimini, Marcello, et al. “Breakdown of cortical effective connectivity during sleep.” Science 309.5744 (2005): 2228-2232.
Casali, Adenauer G., et al. “A theoretically based index of consciousness independent of sensory processing and behavior.” Science translational medicine 5.198 (2013): 198ra105-198ra105.
Casarotto, Silvia, et al. “Stratification of unresponsive patients by an independently validated index of brain complexity.” Annals of neurology 80.5 (2016): 718-729.