The cortical origin of visual hallucinations

How does subjective visual experience relate to the neural machinery of the brain? Visual hallucinations provide a clue. Geometric patterns of spirals, honeycombs and checker-boards are common themes in drug-induced hallucinations. The same patterns can also be seen by gently pressing the eyeballs or by gazing into stroboscopic flickering light. These patterns are collectively known as Kluver forms, after the pioneering neurologist Heinrich Kluver who classified them in the 1920s. Kluver forms are much alike from one person to another and are thought to originate from the neural circuitry of the primary visual cortex -- the region of the brain which processes visual shapes. They provide a unique opportunity to deduce the functional properties of the neural circuitry from subjective visual experience.

Geometric visual hallucinations.  A-D: LSD flashbacks painted by Oster (1970).  E-F: Hallucinations by THC intoxication (Siegel & Jarvik, 1975).  G: Hallucinations by occular pressure (Tyler, 1978).  H: Migraine aura (Richards, 1971). Adapted from Billock & Tsou (2012)
Until now, the fleeting nature of hallucinations has made them difficult to study. Our collaborators at the University of New South Wales have recently devised a method for stabilising the visual hallucinations seen in stroboscopic flicker. The technique works by presenting the flicker on an annulus (ring-shaped stimulus) that is centred on the fovea. That particular stimulus maps onto a thin strip of tissue in the primary visual cortex, by virtue of the retinotopic map. It forces the hallucinated pattern into one spatial dimension. Observers report regularly-spaced blobs that appear to race around the annulus in one direction and then the other. Clever techniques from psychophysics can then be used to measure the spatial wavelength and speed of the blobs, as well as switching times in the perceived direction of motion.

Flicker-induced hallucinations adapted from Pearson, Chiou, Rogers, Wicken, Heitmann & Ermentrout (2016). A: Physical stimulus and a depiction of the percept. B: Depiction of the stimulus used to measure the effective contrast. C: Hallucination depiction and nonius lines used to measure the effective rotation propagation times.  D: Effective contrast of the hallucination as a function of flicker frequency. E: Data showing interocular interaction. F: Hallucination motion speed as a function of flicker rate. G: Dependence of propagation times on cortical distance.
As part of this study, we constructed a mathematical model of the visual cortex that reproduces much of the perceptual behaviour of the hallucinations. The neural activity in our model self-organises into patterns of spirals and stripes that bear an uncanny resemblance to the hallucinatory patterns. The patterns only emerge for flicker frequencies near 11 Hz. If the flicker is too slow, or too fast, then the model reproduces the physical stimulus, as is the case in human perception. Interestingly, the same patterns spontaneously alternate with their negative image. These alternations occur at half the frequency of the flicker stimulation. They evoke a sense of apparent motion that resembles the motion of the illusory blobs reported by humans. The illusory motion is most evident when the flicker is constrained to an annulus, as was the case for the psychophysical experiments.

   

The combination of psychophysics and mathematics allowed us to relate the physiological properties of the visual cortex to the shape and movement of visual hallucinations that people typically see. We believe that this approach holds great promise for elucidating further relationships between neural circuitry and subjective visual experience.

Selected Media reports

Journal papers
  • Billock & Tsou (2012) Elementary visual hallucinations and their relationships to neural pattern forming mechanisms, Psychol Bull. 138:4. p744.
  • Ermentrout & Cowan (1979) A mathematical theory of visual hallucination patterns. Biological Cybernetics. 34:137-150.