Neural Correlates of Consciousness - The Neuronal Basis of Perception

The Neuronal Basis of Perception

The possibility of precisely manipulating visual percepts in time and space has made vision a preferred modality in the quest for the NCC. Psychologists have perfected a number of techniques – masking, binocular rivalry, continuous flash suppression, motion induced blindness, change blindness, inattentional blindness – in which the seemingly simple and unambiguous relationship between a physical stimulus in the world and its associated percept in the privacy of the subject's mind is disrupted. In particular a stimulus can be perceptually suppressed for seconds or even minutes at a time: the image is projected into one of the observer's eyes but is invisible, not seen. In this manner the neural mechanisms that respond to the subjective percept rather than the physical stimulus can be isolated, permitting visual consciousness to be tracked in the brain. In a perceptual illusion, the physical stimulus remains fixed while the percept fluctuates. The best known example is the Necker cube whose 12 lines can be perceived in one of two different ways in depth.

A perceptual illusion that can be precisely controlled is binocular rivalry. Here, a small image, e.g., a horizontal grating, is presented to the left eye, and another image, e.g., a vertical grating, is shown to the corresponding location in the right eye. In spite of the constant visual stimulus, observers consciously see the horizontal grating alternate every few seconds with the vertical one. The brain does not allow for the simultaneous perception of both images.

Logothetis and colleagues recorded a variety of visual cortical areas in awake macaque monkeys performing a binocular rivalry task. Macaque monkeys can be trained to report whether they see the left or the right image. The distribution of the switching times and the way in which changing the contrast in one eye affects these leaves little doubt that monkeys and humans experience the same basic phenomenon. In the primary visual cortex (V1) only a small fraction of cells weakly modulated their response as a function of the percept of the monkey while most cells responded to one or the other retinal stimulus with little regard to what the animal perceived at the time. But in a high-level cortical area such as the inferior temporal cortex along the ventral stream almost all neurons responded only to the perceptually dominant stimulus, so that a "face" cell only fired when the animal indicated that it saw the face and not the pattern presented to the other eye. This implies that NCC involve neurons active in the inferior temporal cortex: it is likely that specific reciprocal actions of neurons in the inferior temporal and parts of the prefrontal cortex are necessary.

A number of fMRI experiments that have exploited binocular rivalry and related illusions to identify the hemodynamic activity underlying visual consciousness in humans demonstrate quite conclusively that BOLD activity in the upper stages of the ventral pathway (e.g., the fusiform face area and the parahippocampal place area) as well as in early regions, including V1 and the lateral geniculate nucleus (LGN), follow the percept and not the retinal stimulus. Further, a number of fMRI experiments suggest V1 is necessary but not sufficient for visual consciousness.

In a related perceptual phenomenon, flash suppression, the percept associated with an image projected into one eye is suppressed by flashing another image into the other eye while the original image remains. Its methodological advantage over binocular rivalry is that the timing of the perceptual transition is determined by an external trigger rather than by an internal event. The majority of cells in the inferior temporal cortex and the superior temporal sulcus of monkeys trained to report their percept during flash suppression follow the animal's percept: when the cell's preferred stimulus is perceived, the cell responds. If the picture is still present on the retina but is perceptually suppressed, the cell falls silent, even though primary visual cortex neurons fire. Single-neuron recordings in the medial temporal lobe of epilepsy patients during flash suppression likewise demonstrate abolishment of response when the preferred stimulus is present but perceptually masked.