The brain transforms sensory messages into conscious perceptions almost instantly Chaotic, collective activity involving millions of neurons seems essential for such rapid recognition.
When a person glimpses the face of a famous actor, sniffs a favorite food or hears the voice of a friend, recognition is instant. Within a fraction of a second after the eyes, nose, ears, tongue or skin is stimulated, one knows the object is familiar and whether it is desirable or dangerous. How does such recognition, which psychologists call preattentive perception, happen so accurately and quickly, even when the stimuli are complex and the context in which they arise varies?
Much is known about the way the cerebral cortex, the outer rind of the brain, initially analyzes sensory messages. Yet investigations are only now beginning to suggest how the brain moves beyond the mere extraction of features-how it combines sensory messages with past experience and with expectation to identify both the stimulus and its particular meaning to the individual.
My own group's studies, carried out over more than 30 years at the University of California at Berkeley, suggest that perception cannot be understood solely by examining properties of individual neurons, a microscopic approach that currently dominates neuroscience research. We have found that perception depends on the simultaneous, cooperative activity of millions of neurons spread throughout expanses of the cortex. Such global activity can be identified, measured and explained only if one adopts a macroscopic view alongside the microscopic one.
There is an analogy to this approach in music. To grasp the beauty in a choral piece, it is not enough to listen to the individual singers sequentially. One must hear the performers together, as they modulate their voices and timing in response to one another.
Our studies have led us as well to the discovery in the brain of chaos- complex behavior that seems random but actually has some hidden order. The chaos is evident in the tendency of vast collections of neurons to shift abruptly and simultaneously from one complex activity pattern to another in response to the smallest of inputs.
This changeability is a prime characteristic of many chaotic systems. It is not harmful in the brain. In fact, we propose it is the very property that makes perception possible. We also speculate that chaos underlies the ability of the brain to respond flexibly to the outside world and to generate novel activity patterns, including those that are experienced as fresh ideas.
An understanding of perception must be based on knowledge of the properties of the neurons that enact it. My colleagues and I have concentrated in many of our studies on neurons of the olfactory system.
For years it has been known that when an animal or a person sniffs an odorant, molecules carrying the scent are captured by a few of the immense number of receptor neurons in the nasal passages; the receptors are somewhat specialized in the kinds of odorants to which they respond. Cells that become excited fire action potentials, or pulses, which propagate through projections called axons to a part of the cortex known as the olfactory bulb. The number of activated receptors indicates the intensity of the stimulus, and their location in the nose conveys the nature of the scent. That is, each scent is expressed by a spatial pattern of receptor activity, which in turn is transmitted to the bulb.
The bulb analyzes each input pattern and then synthesizes its own message, which it transmits via axons to another part of the olfactory system, the olfactory cortex. From there, new signals are sent to many parts of the brain-not the least of which is an area called the entorhinal cortex, where the signals are combined with those from other sensory systems. The result is a meaning-laden perception, a gestalt, that is unique to each individual. For a dog, the recognition of the scent of a fox may carry the memory of food and expectation of a meal. For a rabbit, the same scent may arouse memories of chase and fear of attack.
Such knowledge has provided a valuable starting point for more detailed study of olfaction. But it leaves two important issues unresolved. The first is the classic problem of separating foreground from background: How does the brain distinguish one scent from all others that accompany it?
"PHASE PORTRAITS" made from electroencephalograms (EEGs)
generated by a computer model of the brain reflect the overall activity of
the olfactory system at rest (above) and during perception of a familiar
scent (right). Resemblance of the portraits to irregularly shaped, but still
structured, coils of wire reveals that brain activity in both conditions is
chaotic: complex but having some underlying order. The more circular
shape of the right-hand image, together with its greater segregation of
color, indicates that olfactory EEGs are more ordered-more nearly
periodic-during perception than during rest.
Also, how does the brain achieve what is called generalization-over- equivalent receptors? Because of turbulence in nasal air flow, only a few of the many receptors that are sensitive to an odorant are excited during a sniff, and the selection varies unpredictably from one sniff to the next. How does the brain recognize that signals from different collections of receptors all refer to the same stimulus? Our investigations begin to suggest answers to both problems.
Many of our insights were derived from intensive studies of the olfactory bulb. Those experiments show clearly that every neuron in the bulb participates in generating each olfactory perception. In other words, the salient information about the stimulus is carried in some distinctive pattern of bulbwide activity, not in a small subset of feature-detecting neurons that are excited only by, say, foxlike scents.
Moreover, although this collective neural activity reflects the odorant, the activity itself is not determined solely by the stimulus. Bulbar functioning is self-organized, very much controlled by internal factors, including the sensitivity of the neurons to input.
The experiments uncovering the collective activity were conceptually simple. By applying standard reinforcement techniques, we trained animals, often rabbits, to recognize several different odorants and to behave in particular ways when they did-for instance, to lick or chew in expectation of food or water. Before training was started, we attached 60 to 64 electrodes 0.5 millimeter apart in a gridlike array to a large part of the bulbar surface.
During training and thereafter, the array enabled us to collect sets of 60 to 64 simultaneously recorded electroencephalogram (EEG) tracings as the animals breathed in and out, sometimes sniffing familiar scents and sometimes not. Each tracing reflects the mean excitatory state of local pools of neurons lying in a well-defined layer immediately beneath the electrodes. Rises in the wavelike tracings indicate increasing excitement; dips represent diminished excitement caused by inhibition.