Book Review: Hallucinations, by Oliver Sacks

George Wallis

This is a guest post by George Wallis, one of my PhD students.  We recently attended a seminar in which Oliver Sacks discussed his recent book ‘Hallucinations’.  In this post George discusses the ways in which hallucinations provide neuroscientists with clues about the hidden workings of the brain. This article is also cross-posted at Brain Metrics, a Scitable Blog hosted by Nature Education. 

Oliver Sacks is a neurologist and a writer, and close to a household name.  For many readers, he will be a familiar figure.  Since 1970 he has been writing humane accounts of the ways in which different forms of neurological illness or damage affect the lives of his patients – or occasionally Sacks himself.  Amongst his book-length works are The Man Who Mistook His Wife For a Hat, and Awakenings, an account of the almost miraculous effect of the drug l-DOPA on sleeping sickness patients at the Beth Abraham hospital, that has been adapted into a feature film starring Robin Williams.  Mark and I were lucky to be invited to a small discussion session with Dr Sacks at Warwick University where he is a visiting professor.  The topic of discussion was his most recent book, Hallucinations.

Hallucinations is known for its detailed account of Sack’s own hallucinatory experiences during his remarkably excessive drug-taking phase in the 1960s.  Before tight drug laws, and with access to the most potent compounds to be found in a doctor’s medicine cabinet, Sacks experimented with a wide range of compounds – often in huge doses.  He describes the mind-altering experiences he had with classic psychedelics, the disturbingly real-seeming hallucinations experienced whilst on Artane, frightening episodes of psychotic delirium following withdrawal from some lesser known toxic agents, and the time-eating stupor of opiates.  Most fascinating for Sacks fans is his description of the amphetamine fuelled epiphany that crystallized his desire to write about the neurology and the experiences of his patients.

Beyond the spectacle of these autobiographical chapters, Sacks’ book is a catalogue of the many varieties of hallucination.  For students of neuroscience, this makes for engrossing reading.  Hallucinations can tell us a lot about the brain.

What are hallucinations?  Sack’s defines them as ‘percepts arising in the absence of any external reality – seeing things or hearing things that are not there’.  A few hundred years ago hallucinations might have been ascribed to the influence of Gods or ghosts.  Nowadays, neuroscientists and psychologists see hallucinations as the result of abnormal activity in the brain.  Crucially, neuroscientists consider all of the things we experience to result from models the brain builds.  When you look at something in the outside world, your brain doesn’t magically ‘reach out and touch’ the object so you can perceive it (though, some philosophers might disagree with neuroscientists on this point!).  Instead, the brain builds a model of what is probably out there in the world, doing its best to match the model to the sensory input we receive at our sense organs (for example, in the retina of the eye).  The things you perceive reflect the model the brain builds – a model built out of the buzzing activity of billions of neurons in your brain.  It’s basically intelligent guesswork, but mostly our brains do pretty well, and we have the impression of a stable world.  Importantly, we tend to agree with other people about what’s out there - which gives an indication that our brains are getting things right!  However, if the activity of the brain is in some way altered by a neurological disturbance of one form or another (illness, drugs, damage from a stroke or injury), the model can diverge from its normal faithful representation of the outside world, and we can have hallucinatory perceptions.

Depending on the type of neural disturbance, these hallucinations can take many different forms.  These are all interesting to neuroscientists, as they all have the potential to tell us something about the workings of the brain.

For example, there is Charles Bonnet Syndrome, which Sacks describes in his opening chapter.  The brain’s intelligent guesswork about the outside world is normally informed by a stream of activity from the sense organs. What happens if you cut off that stream of incoming information?  In some cases, the brain keeps on ‘making up a story’ – except now, it has no information to go on, so the percepts that are produced bear no relation to reality.  For example, diseases of the eye can deprive someone of the visual input their brain has been used to receiving.  If part of the retina is damaged, this can leave a blind patch called a ‘scotoma’, and people with a scotoma can sometimes have vivid hallucinations in just their blind patch. 

Charles Bonnet type hallucinations can also occur if someone goes completely blind.  These hallucinations can be highly ornate – for example little ‘lilliputian’ people are sometimes seen, often in very colorful and ornate clothing.  Some people describe these hallucinations as being like a movie.  For most people, however, Charles Bonnet syndrome involves simpler hallucinations – shapes, colours and patterns.  The patterns in the scotoma can ‘scintillate’, giving the impression of constant movement.

Scintillating scotoma patterns

Just because the retina is damaged doesn’t imply that the visual parts of the brain are damaged too – this isn’t necessary for hallucination.  Charles Bonnet syndrome reflects the normal activity of a brain forced to guess in the absence of information – and people with Charles Bonnet are often well aware that their hallucinations aren’t real, even if they seem very solid and detailed.  Interestingly, some people with disrupted sensory input experience hallucinations and some do not – it isn’t clear why.

Does this mean that you could hallucinate too if you were deprived of sensory input?  Yes – though as with Charles Bonnet syndrome, it seems to vary from person to person.  There have been various experiments with sensory deprivation.  A recent example was published in the Journal of Neuro-opthalmolagy in 2004, by Lofti Merabet, Alvaro Pascual-Leone, and their collaborators (Merabet et al., 2004).  They simply blindfolded thirteen healthy volunteers for four days – otherwise, their volunteers were able to walk inside and outside, talk to others, and listen to the TV.  10 out of 13 people reported hallucinations.  Just like in Charles Bonnet syndrome, these were sometimes simple (flashing lights, geometric patterns) and sometimes complex (landscapes, people, buildings, sunsets – often seeming extremely vivid; more vivid than normal visual perceptions).

Hallucinations resulting from sensory deprivation are evidence for the neuroscientists’ view of perception – that the brain generates a model and fits it to the world.  Sometimes the brain tissue responsible for generating that model is disturbed in a way that alters the things people perceive.  For example, in epilepsy, the normally controlled activity of the brain briefly goes haywire.  Out of control neuronal firing emerges, and can spread over the brain surface.  Another form of disturbed brain activity is experienced by many people in the form of migraine.  Migraines are sometimes accompanied by a visual hallucination superimposed on the real visual scene – often termed a ‘migraine aura’.

A migraine sufferer’s recreation of a ‘migraine aura’

 In migraine or epilepsy, people sometimes perceive geometric patterns – for example chequer-boards, zig-zag lines, or concentric rings.  These geometric hallucinations are so consistent across people, they were catalogued in the 1920s by the psychologist Heinrich Klüver.  He divided them into four types: tunnels and funnels, spirals, lattices, and cobwebs.

Kluver’s four categories of hallucination pattern.
Bressloff et al., 2002; used with permission.

These patterned hallucinations are interesting because they seem to reflect the structure of the parts of the brain responsible for early visual processing - parts of the brain that are quite organized in their layout.  In the 1970s, mathematicians Jack Cowan and G Ermentrout built models of aberrant activity patterns, given what they knew about the structure of the visual cortex.  These models have been extended by the Oxford mathematician Paul Bressloff (Bressloff, Cowan, Golubitsky, Thomas, & Wiener, 2002).  By modeling unusual activity in the visual cortex, and then also taking account of the way the neurons in our visual cortex map onto visual space, these researchers are able to predict the kind of hallucinatory patterns catalogued by Klüver.

A mathematical simulation of a hallucination pattern

Whilst migraines and epilepsy are certainly not pleasant, the actual hallucinations experienced are rarely frightening.  The same is true for Charles Bonnet Syndrome.  People experiencing these hallucinations are usually able to tell them apart from reality, though sometimes only once they have become used to them and know what to expect!  Of course, this isn’t true of all hallucinations.  Sacks also discusses the more terrifying types of hallucinations, for example, those of psychosis, or of the ‘night terror’ associated with sleep paralysis – in which people awake unable to move, with the feeling that they are trapped beneath a horrible intruder who is trying to suffocate them (the ‘night mare’ or ‘night hag’).

Nicolai Abildgaard’s ‘Nightmare’

What do these more frightening hallucinations - in particular, the hallucinations associated with psychosis (in which people often also experience delusions) - say about the brain?  This is a fascinating but difficult area, as yet poorly understood.  Here it becomes more difficult to draw the line between perceptions and beliefs, and emotional and motivational factors seem to be more involved.  Researchers are currently trying to understand how hallucinations in diseases like schizophrenia are related to the other symptoms of the disorder, and how they may be similar or different to the kind of hallucinations produced by sensory deprivation or epileptic activity patterns in the brain.

Finally, an interesting speculation that may haunt you as you read Sacks’ book is that hallucinatory experiences – which, as Sacks points out, are much more common than one might think – could be responsible for the religious, mystical, and paranormal parts of our culture.  For example, Sacks points out that Joan of Arc’s visions are classic manifestations of epileptic activity in the temporal lobes.  He speculates that these seizure related visions were the reason an uneducated farmer’s daughter became a religious leader who rallied thousands of followers.

Sacks’ book is a engrossing survey of hallucinatory experiences of all types.  In their variety (far more extensive than described in this blog post) hallucinations provide many insights into the way our ordinary perception works.  Reading Sacks’ book is also a good preparation for the possibility – not too slim, as Sacks points out – that you will one day have a hallucinatory experience of one form or another (if you haven’t already!).

References

Bressloff, P. C., Cowan, J. D., Golubitsky, M., Thomas, P. J., & Wiener, M. C. (2002). What Geometric Visual Hallucinations Tell Us about the Visual Cortex. Neural Computation, 14(3), 473–491. doi:10.1007/BF00288786

Merabet, L. B., Maguire, D., Warde, A., Alterescu, K., Stickgold, R., & Pascual-Leone, A. (2004). Visual Hallucinations During Prolonged Blindfolding in Sighted Subjects. Journal of Neuro-Ophthalmology, 24(2), 109.

All images Creative Commons except Kluver patterns, from Bresloff et al., used with permission.