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The pathology of experience

Chris Frith
DOI: http://dx.doi.org/10.1093/brain/awh085 239-242 First published online: 15 January 2004

The fundamental assumption of cognitive neuroscience is that the way we behave and the way we experience the world is determined by the way our brains work. Pathological cases provide the most stringent tests for this assumption. From our knowledge of the way our brains work it should be possible to predict what kind of behaviour or experience will occur as a result of damage to a specific brain region or system. Lichtheim (1885) was the first to describe this approach. In his simple model of how the brain processes speech Lichtheim pointed out that there were seven possible ‘interruption points’ in this system. He then specified the different kinds of aphasia that should result from damage at each of these points. A striking and erroneous early example of the approach concerns cerebral achromatopsia. For many years neurologists refused to accept the existence of this disorder on the basis of the mistaken belief that it was incompatible with the way the brain worked (Zeki, 1990). Today the demonstration of segregation in the visual system predicts the existence of many specific disorders including achromatopsia (impaired colour perception), akinetopsia (impaired visual movement perception) and prosopagnosia (impaired face recognition).

These disorders are all negative in the sense that the patients lack a particular aspect of normal experience. It is not too difficult to understand how damage to the brain could prevent some behaviour or experience. It is much more difficult to understand how damage to the brain can create a positive symptom in which the patient experiences something, such as an hallucination, which most of us don’t experience. A second problem is that there is a long tradition of treating hallucinations not as false, but as veridical perceptions from a spiritual world; telepathy or a voice from beyond the grave. This tradition gave rise to what is probably the most thorough investigation of hallucinations to date, “The Report on the Census of Hallucinations” (Sidgwick et al., 1894). With a sample of 17,000 informants this contrasts very favourably with modern surveys. The motives of the distinguished Cambridge academics who compiled the report were mixed. Some hoped that the data would prove the existence of the spirit world. Others wanted to uncover the psychological and physiological mechanisms underlying hallucinations. Care was taken to ascertain that, at the time of the experience, the informant was sane and was not suffering from any physical disorder such as a fever. About 10% of the sample had experienced hallucinations and the majority of these (8.4%) were visual. The compilers noted that this differs from hallucination in the insane of which the majority are auditory.

There are many examples of apparent spiritual communication. From Mr Eggie: “On October 5th, 1863, I awoke at 5 a.m. ….. I heard distinctly the well‐known and characteristic voice of a dear friend, repeating the words of a well‐known hymn. I have always thought it remarkable that at the very same time, almost to the minute, my friend was seized suddenly with a mortal illness.” Other informants, however, did not trust their experiences. From Mr. W.S.: “I became painfully anxious, and sat down for a minute …. and then I saw, floating, as it were, between me and the mantel‐piece, the upper half of my father’s body. …. I looked steadily at my half‐ghost, and saw how a spot in the mantel‐piece, a knot in the wainscot, &c., &c., had combined to produce the spectral appearance.” The report also includes a discussion of possible physiological mechanisms. “The view that … hallucinations are originated centrally, in the brain and not in the sense organs, is that now generally held by physiologists, as well as by psychologists.” A mechanism for this central origin is attributed to Professor Sully: “The cerebral activity that produces a hallucination may probably diffuse itself downwards to the periferal regions of the nerves so that the sense‐organs may thus become involved secondarily”. But the report concludes that “this hypothesis of the secondary participation of the sense‐organs in hallucinations through a downward sensory impulse from the brain …. is inconsistent with generally accepted physiological theories of the actions of the nervous system.”[There is an interesting discussion in the report about whether hallucinations or dreams or mental images can cause visual after‐images, and, whether this implies top‐down influences on the retina. There is evidence such top‐down effects can occur in some people (Weiskrantz, 1950)]. Today we believe that ‘downward sensory impulses’ (called variously top‐down, feedback or re‐entrant signals) have a major role in brain function (e.g. Lamme et al., 1998). What we perceive depends upon the interaction between these top‐down signals and the information coming from the sense organs. Abnormal dominance of the top‐down signals would lead to false perceptions including illusions and hallucinations.

Visual Hallucinations

Unlike Sidgwick and his collaborators, we know now that activity in the sense organs is not necessary for sensory experience. Direct electrical stimulation of visual cortex produces visual hallucinations (Lee et al., 2000) and the nature of the visual experience, whether it be of colour, form or motion, depends on where exactly the cortex is stimulated. The hallucinations experienced by patients with Charles Bonnet syndrome are associated with activity in extra‐striate cortex and here too the location of the activity determines the form of the experience (ffytche et al., 1998). There is a striking similarity between the visual hallucinations associated with a variety of different causes including peripheral damage (Charles Bonnet syndrome), occipital lobe epilepsy, and mescalin. Patients report flashing and spinning colours, complex repetitive patterns, organic forms and grotesque faces and scenes (ffytche and Howard, 1999). These visual hallucinations come from a restricted set of categories determined by the anatomy of the visual brain (Santhouse et al., 2000).

False beliefs

There has been even greater resistance to fitting psychotic disorders into our neuro‐cognitive framework. The hallucinations and delusions associated with disorders like schizophrenia were for a long time considered to be ‘not understandable’. Karl Jaspers (1963) wrote that ‘the profoundest difference … seems to exist between that type of psychic life which we can intuit and understand, and that type which, in its own way, is not understandable and which is truly distorted and schizophrenic …’. He implies that an understanding of normal cognitive processes will not help us to understand these experiences. In the case of psychosis, there is no clear distinction between hallucinations (false perceptions) and delusions (false beliefs). I shall consider two examples: Capgras syndrome and delusions of control. The patient with Capgras syndrome falsely believes that a close relative or friend has been replaced by a double. The patient with a delusion of control falsely believes that his actions are being directly controlled by alien forces. These two possibilities lie so far from our normal experience that these disorders were typically classified as examples of false beliefs rather than abnormal experiences. Recent formulations suggest that these disorders are better characterised as abnormal experiences that derive their particular form from basic neural functions.

Capgras syndrome

We know that information is processed in many parallel streams in the brain and that each stream is optimised for different functions (e.g. the ‘what’ and ‘where’ streams; Ungerleider and Mishkin, 1982). Another example is the rapid and unconscious processing stream that evaluates objects in terms of whether they should be approached or avoided (the ‘****!’ stream). This stream allows us to respond unconsciously to fearful objects and involves the amygdala (Morris et al., 1999). Explicit identification of objects is achieved much more slowly and via a different neural pathway involving inferior temporal cortex (the ‘what’ stream). As a result we can find ourselves running away from something before we are aware of precisely what it is (LeDoux, 1996). These two streams can be damaged independently. Damage to the stream that explicitly identifies faces leads to prosopagnosia. Patients with this disorder can no longer identify individual faces (including friends and relatives). However, rapid, implicit evaluation of faces remains intact and such patients still show emotional responses to familiar faces (e.g. Blount, 1994). Damage to the evaluation stream leads to a situation in which the patient can recognise a face, but no longer experiences the emotional response associated with evaluation of the face. The face may look like that of the patient’s wife, but the emotional colouring normally associated with that face is no longer present (Ellis and Lewis, 2001). The conclusion that this person, who claims to be his wife, must be an impostor is almost inevitable. [Perhaps this conclusion is not quite inevitable. It is possible that additional frontal damage is needed in order to entertain this rather outlandish hypothesis (Burgess et al., 1996)].

Delusions of control

Our understanding of delusions of control also results from the discovery of multiple representations, but in this case in the system underlying the control and awareness of action rather than the visual system (see Blakemore & Frith, 2003 for a review). In particular there are separate representations of the intended consequences of our movements (based on prediction) and the actual consequences of our movements (based on sensory feedback). Whenever we make a movement this will cause changes in tactile and kinaesthetic sensation, but we are largely unaware of these changes. Most of the time it is representations of the intended consequences of our movements that determine our awareness rather than representations of the actual consequences of our movements. Only if the discrepancy between intended and actual consequences of movement is quite large do representations of the actual state of our motor system enter awareness. Furthermore the physiological activity associated with tactile sensations caused by our own movements is attenuated. This, of course, is why we cannot tickle ourselves. In patients with delusions of control something as yet to be determined goes wrong with the system whereby sensations caused by the patient’s own actions are attenuated. They are abnormally aware of these sensations (Blakemore et al., 2000) and manifest over‐activity in parietal cortex (Spence et al., 1997). For them, active movements feel like passive movements. On this basis it is perfectly understandable that it is indeed as if their movements were being caused by external forces.

Multiple representations of the body

Our understanding of delusions of control was informed by the observation that there are separate representations in the brain for the intended and the actual state of the motor system. However, there are many other representations differentiated in terms of temporal and spatial coordinates. There are representations of past, present and future states of the body. There are also representations of the body in terms of different spatial coordinate systems: my arm in relation to the rest of my body, my arm in relation to the object I am reaching for, my arm in relation to the room in which I am standing. In the normal case we are not aware of all these different representations, but only of an integrated sense of our body in space. However, damage to the motor system can lead to abnormal awareness of un‐integrated representations. For example, McGonigle et al. (2002) describe a patient with a phantom supernumerary left arm. This phantom arm occupies the position previously occupied by the patient’s real left arm about a minute previously and disappears whenever the left arm is moved. In this case the lesion was in the left pre‐Supplementary Motor Area (SMA) and cingulate motor area and the activity associated with presence of the phantom was in SMA proper.

Out‐of‐the‐body experiences

In the case of out‐of‐the‐body experiences it is the whole body rather than just one arm that is replicated. In one form (autoscopy) we see our double. In true out‐of‐the‐body experiences we look down at our own body from above. Such experiences are associated with psychiatric disorders, but are also estimated to have a prevalence of 10% in the general population, a figure close to that reported for hallucinations. Like hallucination these experiences have exerted a particular fascination since they seem to provide access to a spirit world. For example, it was believed that we each have a dopplelgänger who normally remains unseen. If we see our doppelgänger then our death is imminent. Meetings with doppelgangers were a poplar theme in romantic literature of the 19th century (Webber, 1996). Even today many people believe that during an out‐of‐the‐body experience (astral projection) the mind literally leaves the body and thereby can view things that would be invisible from the vantage point of the body. Experimental tests of this possibility continue to be conducted (e.g. Tart, 1968).

Against this background of mysticism the study of Blanke et al. in this issue of Brain stands out with admirable clarity. Blanke and his colleagues provide a very thorough review of earlier literature on out‐of‐the‐body experiences and autoscopy and then report a detailed examination of 6 neurological patients who report such experiences. They find that patients with such experiences also report pathological sensations such as floating and rotating (associated with the vestibular system) and visual body‐part illusions such as shortening or movement of limbs. Furthermore they have been able to localise an area of common brain dysfunction in all these cases to the temporo‐parietal junction. In one patient (case 3) direct electrical stimulation of this region reliably generated out‐of‐the‐body experiences and other abnormal experiences of the body.

We know that the brain contains multiple representations of the body for proprioceptive, tactile and visual information and that some of these representations are in body centred co‐ordinates while others are coded in terms of external space. Normally all these representations are integrated to provide a unitary sense of the body in space. However, as a result of damage (or perhaps during low arousal when on the verge of sleep) this unity can be lost leading to the experience of a divergence between the felt and seen position of our body. I find it particularly interesting that the temporo‐parietal junction has a special role in the experience. Recent brain imaging experiments with normal volunteers have shown that activity in this region is elicited by observing biological motion, actions and perhaps simply by the apparent presence of other people (Saxe et al. 2003). This raises the possibility that an out‐of‐the‐body experience occurs when a strong sense of the presence of another person is coupled with a discrepancy between the felt and the seen position of our own body. In these circumstances a representation of our body can get falsely bound with the representation of another person in external space.