Why does a constant stimulus feel constant? (I)

What is the relationship between neural activity and perception? That is, how does the quality of experience (qualia) relate with neural activity? For any scientist working in sensory neuroscience, this should be a central question – perhaps THE question. Unfortunately the obsession of the community for the question of “neural coding”, which is about relating neural activity with externally defined properties of sensory stimuli, does not help much in this regard. In fact, very naïve philosophical assumptions about this question seem to pervade the field. A popular one is that the perceived intensity of a stimulus corresponds to the firing rate of the neurons that are sensitive to it, in particular sensory receptor neurons. This was indeed an idea proposed by Lord Adrian in the 1920s, and the basic argument is that the firing rate of sensory neurons generally increases when the strength of the stimulus is increased. Clearly the argument is very weak (only an observed correlation), but I will try to refute it explicitly, because it triggers some interesting remarks. To refute it, I will turn the perspective around: why is it that a constant stimulus feels constant? In fact, what is a constant stimulus? This is a very basic question about qualia, but it turns out that it is a surprisingly deep one.

Let us start by listing a few sensory stimuli that feel constant, in terms of perceptual experience. A pure tone (e.g. the sound produced by a diapason or a phone) feels constant. In particular its intensity and pitch seem to be constant. Another example could be a clear blue sky, or any object that you fixate. In the tactile modality, a constant pressure on a finger. For these stimuli, there is a perceived constancy in their qualities, ie, the color of the sky does not seem to change, the frequency of the tone does not seem to change. Attention to the stimulus might fade, but one does not perceive that the stimulus changes. In contrast, neural activity is not constant at all. For a start, neurons fire spikes, and that means that their membrane potential always changes, but we do not feel this change. Secondly, in sensory receptor neurons but also in most sensory neurons in general, the frequency of those spikes changes in response to a constant stimulus: it tends to decrease (“adapt”). But again, a blue sky still feels the same blue (and not darker) and the pitch and intensity of a pure tone do not decrease. There appears to be no such simple connection between neural activity and the perceived intensity of a stimulus. Why is it that the intensity of a pure tone feels constant when the firing rate of every auditory nerve fiber decreases?

In response to this question, one might be tempted to propose a homunculus-type argument: the brain analyzes the information in the responses of the sensory neurons and “reconstructs” the true stimulus, which is constant. In other words, it feels constant because the brain represents the outside world and so it can observe that the stimulus is constant. As I noted a number of times in this blog, there is a big conceptual problem with this kind of argument (which is vastly used in “neural coding” approaches), and that is circular logic: since the output of the reconstruction process is in the external world (the stimulus), how can the brain know what that output might be, as it is precisely the aim of the reconstruction process to discover it? But in fact in this case, the fallacy of this argument is particularly obvious, for two reasons: 1) whereever the representation is supposed to be in the brain, neural activity is still not constant (in particular, made of spikes); 2) even more importantly, in fact what I called “constant stimulus” is physically not constant at all.

Physically, a pure tone is certainly not constant: air vibrates at a relatively high rate, the acoustic pressure at the ear fluctuates. The firing of auditory nerve fibers actually follows those fluctuations, at least if the frequency is low enough (a phenomenon called phase locking), but it certainly doesn't feel this way. Visual stimuli are also never constant, because of eye movements – even when one fixates an object (these are called fixational eye movements). In fact, if the retinal image is stabilized, visual perception fades away quickly. In summary: the sensory stimulus is not constant, neurons adapt, and generally neural activity is dynamic for any stimulus. So the question one should ask is not: how does the brain know that the stimulus is constant, but rather: what is it that make those dynamic stimuli feel perceptually constant?

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