Hallucinations are often associated with psychiatric conditions such as schizophrenia or with LSD and related drugs. Hearing voices is a characteristic symptom which is reported by about 70% of schizophrenic patients, as well as by some 15% of patients with mood disorders such as depression; and those under the influence of LSD often experience extreme spatial distortions and surreal visions.
Most common are auditory and visual hallucinations, but the other senses can also produce mirages. Temporal lobe epilepsy or brain injury can lead to phantosmia, or olfactory hallucinations, during which one detects pleasing or foul smells (e.g. fresh flowers or rotting flesh) that are not actually present. More unusual is a tactile hallucination in which one experiences the sensation of insects crawling under the skin. This can be caused by shingles or cocaine abuse, and is referred to as formication (from the Latin word formica, meaning ‘ant’).
Hallucinations arise spontaneously and are transient in nature, and so the neural activity underlying them is difficult to study. Now though, Dominic Ffytche of the Institute of Psychiatry in London has devised a novel experimental technique with which he has studied the changes that occur in brain activity as an induced visual hallucination is taking place. His findings, which are published in the September issue of the journal Cortex, provide a new theoretical understanding of what happens in the brain during a hallucination.
Theories about how hallucinations occur can be broadly divided into two categories. Topological theories emphasize abnormal activity in specific regions of the brain. For example, visual or auditory hallucinations are associated with increased activity in the visual and auditory regions of the brain, respectively, and can be induced by electrical stimulation, during, for example, presurgical evaluation of epileptic patients.
Hodological theories, on the other hand, emphasize the changes in activity of pathways connecting different regions of the brain. For example, in schizophrenic patients who are prone to hallucinations, neuroimaging shows changes in the activity of pathways connecting the frontal and temporal lobes. Further evidence comes from patients who have undergone frontal lobotomy, which involves severing the white matter tracts which contain the connecting fibres; some lobotomized patients exhibit a reduced or abolished ability hallucinate.
Hallucinations are not restricted to the mentally ill or those under the influence of psychotropic drugs. They are actually rather common, and are often experienced by healthy people under various circumstances. They can also be evoked in various ways. The Czech anatomist Jan Evangeliste Purkinje, one of the founding fathers of modern neuroscience, realized this at an early age:
The lively mind of the child revels in the manifold stimuli of the external world…Who does not remember, if only dimly, such games from that beautiful time? One of them, which could keep us busy at a more serious age, is as follows: I stand in bright sunlight with closed eyes and face the sun. Then I move my outstretched, somewhat separated fingers up and down in front of my eyes, so that they are alternately illuminated and shaded. In addition to the uniform yellow-red that one expects with closed eyes, there appear beautiful regular figures that are initially difficult to define but slowly become clearer. When we continue to move the fingers, the figure becomes more compelx and fills the whole visual field.
Purkinje studied this and other visual phenomena for his doctoral thesis. In the laboratory, he evoked simple hallucinations in his subjects using a bright light and a rotating wheel; immediately afterwards, he would ask them to draw the patterns they experienced. The drawing above, which comes from Purkinje’s thesis, shows one of the visual phenomena, as drawn by one of his subjects.
Ffytche adapted Purkinje’s old method for his study. He induced these so-called Purkinje patterns in 6 subjects using custom-made goggles containing light-emitting diodes to produce stimuli consisting of repetitive flashes of light of a specific frequency. Functional magnetic resonance imaging (fMRI) and electroencephalogram (EEG) were used to observe the changes in brain activity that occur during the transition between the hallucinatory and non-hallucinatory states. As a control, the neural activity evoked by the flashes was compared to the activity that occurs in response to light stimuli of higher or lower frequencies that do not induce hallucinations.
The hallucinations induced in this way began several seconds after the light stimulation and contained not just geometrical patterns but also colour and movement. They were found to be associated with increased activity in a widely distributed network of brain regions, especially in the visual cortex in the occipital lobe, but also in regions of the frontal and temporal lobes. Activity in the white matter tracts (the connections) within the occipital lobes was found to first decrease and then increase, consistent with the subjects’ reports that the hallucinations began several seconds after the stimuli were presented to them.
In the EEG experiments, the activity recorded from two of the electrodes was found to become sychronous whilst the subjects were hallucinating. Paradoxically, the neuroimaging also showed that the hallucinations were associated with a negative relationship between activity in the visual cortex and lateral geniculate nucleus (LGN), which is the first stop for visual information sent from the eye. When a hallicination was taking place, activity in the LGN was seen to decrease, whereas activity in the visual cortex increased at the same time.
Ffytche hypothesizes that the changes in connectivity could be due to changes in the firing mode of the thalamo-cortical connections (the connections between the LGN and visual cortex). He suggests that during a hallucination the LGN switches from “tonic” mode, in which the frequency of signals in the retina are faithfully translated to the cortex, to “burst” mode, in which the two become dissociated from one another. The latter is associated with an increase in the energy requirements of the visual cortex and a decrease in that of the LGN, which is consistent with the apparently paradoxical findings of the neuroimaging.
Overall, Fytche’s findings suggest that hallucination cannot be explained by a topological or hodological explanation alone, but instead by a combination of the two. And according to his hypothesis that the connectivity changes occur because of a switch by LGN neurons from tonic to burst mode, hallucinations (or Purkinje patterns at least) occur because of temporary “blindness”. During burst firing mode, certain aspects of the visual field do not reach the visual brain because of the uncoupling of activity in the LGN and cortex.
Ffytche, D. (2008). The hodology of hallucinations. Cortex 44: 1067-1083. DOI: 10.1016/j.cortex.2008.04.005