Different people would answer this question in different ways. For instance, Adrian (1932) clearly regarded himself as an empiricist, saying:
In all branches of natural science there are two methods of approach, that of the strategist who can devise a series of crucial experiments that will reveal the truth by a sort of Hegelian dialectic, and that of the empiricist who merely looks about to see what he can find.
In his hands, "merely looking about to see what one can find" was astonishingly fruitful, but I confess that I have often aspired to the more theoretical approach that Adrian described first in the above passage. As a research student I was intrigued by information theory and cybernetics, which were then coming to the fore (Shannon and Weaver, 1949; Wiener, 1961), by early work on computer pattern recognition (Grimsdale et al., 1959; Selfridge and Neisser, 1960), and by the ideas of ethologists about fixed action patterns and innate releasing factors that were being popularized by Niko Tinbergen (1953) and Konrad Lorenz (1961) at about that time. But theories can close your eyes as well as open them.
One of the first experimentally satisfactory experiments I did on the frog's retina gave a result that made nonsense of the theory I was testing, but I was so fixated by the theory that I nearly missed an important new fact that was staring me in the face. Having previously mapped the receptive field of a retinal ganglion cell, I measured its sensitivity to circular spots of increasing size. My theory predicted that while it was within the receptive field, sensitivity would rise either in proportion to the area of the stimulus spot or in proportion to its square root, depending on the type of unit. My theory attached great importance to which of these rules it followed, but the results showed that the sensitivity rose at a rate almost exactly halfway between the alternatives expected. I went home late at night in great gloom, thinking the experiment had failed and was not worth repeating. It was only as I was falling asleep that I remembered that the sensitivity had plunged to a nonsensical-seeming near-zero value for the largest spot size when it spread outside the excitatory receptive field. I then realized that this unpre-dicted near-zero result actually provided direct evidence for something more interesting than my previous theorizing: it strongly suggested that the retinal ganglion cell had an inhibitory surround, a new fact that was only later described by Hartline (1949) and Kuffler (1952).
This event might justify ignoring theoretical and philosophical issues altogether, but, of course, the real lesson is to stay awake and be ready with a new theory whenever the facts demand it.
For Steve Kuffler, linking single-unit function to known (or discoverable) anatomical structure was probably the main inspiration, as it was for his most famous followers, David Hubel and Torsten Wiesel. Their school of thought was extraordinarily influential, for it diverted the main efforts of neurophysiologists in the United States away from the study of evoked potentials and massed responses to single units. Single-unit recordings are never going to make much sense unless they are related to the anatomy, but this needs no further emphasis.
Obviously, one important aim of neuroscientists is to explain subjective experience, and the role of single neurons in mediating this process adds much zest to their investigation. However, I think this appeal has been seductive rather than productive. We know so little about the nature of conscious experience that it would not help very much even if we were able to establish tight relations with single-unit activities. Instead, the qualitative parallels are weak and tend to fall apart when closely examined, so I shall not discuss them further, feeling that the quantitative parallels that signal detection theory has established are far more significant. There has, however, been one very simple and direct demonstration of the relation between subjective experience and single impulses in a single unit.
Vallbo and colleagues (see Valbo, 1989) demonstrated that human subjects (actually, the experimenters themselves) can detect the occurrence of a single impulse in a single sensory fiber. They inserted a fine metal microelectrode, insulated up to its tip, into the nerve that runs from the hand to the spinal cord and then connects to the brain. With fortunate placement of the electrode it is possible to record the activity of just one fiber, and in such a case a certain region on the hand or finger may be found that, when touched, causes a succession of brief, equal-sized pulses to appear on the oscilloscope screen and to be heard through the loudspeaker as a volley of brief clicks. These action potentials come from a single sensory fiber, and one can reduce the intensity of the mechanical stimulus until it only causes, on average, a single action potential. Will this minimal response ever be felt? For some types of touch receptors at the fingertip, it can: it is felt as a brief and very light touch. For other types of receptors, and at other positions on the skin, this is not the case, and even where it is, one is not forced to conclude that conscious awareness accompanies a single impulse, for it is quite possible that a single one in the peripheral fiber causes several impulses at later stages. All the same, these facts do seem to show that sensory experience does not necessarily depend on hundreds of impulses in hundreds of fibers: a single impulse in a single fiber sometimes makes a perceptible difference.
For myself, the reason for retaining a keen interest in single neurons is simply that they are the main computing elements of the brain, and I cannot believe that we shall get our models right until we understand them better; the properties of neurons define the work that a network can do, whereas the network connections only permit (or prevent) that work being done.1 So at this point I shall indulge in some guesswork about how our notions of pyramidal cells may evolve over the next decade or so.
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