Way back in 1769, a Swiss physician named Charles Bonnet noticed how his completely blind grandfather experienced vivid, detailed visions of people, animals and objects. It was later named the “Charles Bonnet syndrome,” but scientists didn’t understand how this was possible.
Now, researchers at the Weizmann Institute of Science in Rehovot have observed slow spontaneous fluctuations in the brain’s visual centers that preceded visual hallucinations in people who have lost their eyesight. It has just been published in the journal Brain under the title “How do the blind ‘see’? The role of spontaneous brain activity in self-generated perception.”
Prof. Rafael Malach and his group members of the institute’s neurobiology department researched the phenomenon of spontaneous “resting-state” fluctuations in the brain. These mysterious slow fluctuations, which occur all over the brain, take place well below the threshold of consciousness. Despite a fair amount of research into these spontaneous fluctuations, their function is still largely unknown.
The research group suggested that these fluctuations underlie spontaneous behaviors. However, it is typically difficult to investigate truly unprompted behaviors in a scientific manner for two reasons. One is that instructing people to behave spontaneously is usually a killer of spontaneity. Secondly, it is difficult to separate the brain’s spontaneous fluctuations from other, task-related brain activity. The question was: How could they isolate a case of a truly spontaneous, unprompted, behavior in which the role of spontaneous brain activity could be tested?
Individuals experiencing Charles Bonnet visual hallucinations presented the group with a rare opportunity to investigate their hypothesis. This is because in the syndrome, the hallucinations appear at random, in a truly unprompted fashion, and the visual centers of the brain do not process outside stimuli (because these individuals are blind). As a result, they are activated spontaneously. In a study led by Dr. Avital Hahamy, a former research student in Malach’s lab who is now a postdoctoral research fellow at University College London, the relation between these hallucinations and the spontaneous brain activity has indeed been revealed.
The researchers first invited to their lab five people who had lost their sight and reported occasionally experiencing clear visual hallucinations. These participants’ brain activity was measured using a functional MRI (fMRI) scanner while they described their hallucinations as these occurred. The scientists then created movies based on the participants’ verbal descriptions and showed these movies to a sighted control group, also inside the fMRI scanner. A second control group consisted of blind people who had lost their sight but did not experience visual hallucinations. These were asked to imagine similar visual images while in the scanner.
Because some participants with the syndrome had some, albeit minimal, residual vision, all of those studied were instructed to close their eyes during the entire scanning procedure. Participants were trained to speak without moving their heads, both outside and inside the scanner. In-scanner verbal reports of hallucinations were recorded, and played back to the participants outside the scanner at the end of each session, asking them to give details of these hallucinatory events. Because the visual acuity of all participants deteriorated at a relatively late stage of life, their description of the hallucinations was based on their prior visual experiences.
The same visual areas in the brain were active in all three groups – those that hallucinated, those that watched the films and those creating imagery in their minds’ eye. But the researchers noted a difference in the timing of the neural activity between these groups. In both the sighted participants and those in the imagery group, the activity was seen to take place in response either to visual input or to the instructions set in the task. But in the group with Charles Bonnet syndrome, the scientists observed a gradually increasing wave of activity, reminiscent of the slow spontaneous fluctuations, that emerged just before the onset of the hallucinations. In other words, the hallucinations were not the result of external stimuli (sensory images or instructions to imagine specific things), but were rather evoked internally by the slow, spontaneous, brain activity fluctuations.
“Our research clearly shows that the same visual system is active when we see the world outside of us, when we imagine it, when we hallucinate and probably also when we dream,” explained Malach. “It also exemplifies the creative power of vision and the contribution of spontaneous brain activity to unprompted and creative behaviors.”
In addition to the scientific value of the work, Hahamy hopes it may raise awareness of Charles Bonnet syndrome, which can be frightening to those who experience it. “These individuals may keep their visual hallucinations a secret – even from doctors and family – and we want them to understand that these visions are a natural product of a healthy brain, in which the visual centers remain intact, even if the eyes have ceased to send them sensory input,” Hahamy concluded.