Detecting Physical Variability in the Environment

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Almost 2500 years ago, in his treatise On the Soul (De Anima), Aristotle wrote, "There is nothing in the intellect that was not first in the senses." He enumerated five senses: sight, hearing, smell, taste, and touch. To Aristotle, the senses were formed of earth, water, air, and fire, as was all matter, and they came together in the "common sense," the heart, which brings us the awareness of sensation, allows us to distinguish between the perceptions of each sense, and yet ultimately combines them into one common experience.

Aristotle was probably the most noteworthy empiricist in the history of Western thought, at least until Bacon and perhaps Descartes in the Enlightenment period. He believed that nothing could be known without first being experienced. He had very broad interests and investigated all subjects with the same intensive datagathering approach. His teacher, Plato, by contrast, was a rationalist. To Plato, knowledge was innate; it preceded and was not dependent upon experience.

We can argue with Aristotle's restricted list of the senses, because he should have realized that we can sense gravity, or balance, or the location of our bodies in space, or other ways in which we (and other organisms) sense our environment. Or we can disdain his primitive idea that the senses are of the four elements, because we know they are really receptors and ligands and proteins, or that the heart is the interpreter of sensation, because we know it is really the brain. We can smile at Plato's rationalism, because we, too, are empiricists in the best scientific tradition. But if we step back from these particulars, we might find that our own view of the senses, even with our extensive knowledge of genes and molecules, is in fact more similar to, or even derived from, the thought of these ancient Greeks than we care to realize. In fact, from an evolutionary perspective we should expect more connectedness, less distinction, more repetition but in other ways less "rationalism" in the traits of life.

Does knowledge precede experience, or is it the other way around? What we know about senses and learning and behavior suggests that it is not one or the other.

Genetics and the Logic of Evolution, by Kenneth M. Weiss and Anne V. Buchanan. ISBN 0-471-23805-8 Copyright © 2004 John Wiley & Sons, Inc.

The gravitational sense, the light-seeking behavior of many organisms, and sucking in newborn mammals are all considered to be instinctive or reflexive behaviors. Animals are born "knowing" these things. Biologists would even argue that it is "coded" in the DNA, which must be as platonic a view of inherent knowledge as there can be.

On the other hand, implicit in our understanding of the senses is that they are used to acquire information—new and unpredictable information—about the world. Knowledge derives from experience, Aristotle said—so our own view of the senses has also undeniably been Aristotelian. Furthermore, many biologists assign darwinian purpose to the senses: hearing is "for" the detection of predators, taste is "for" the detection of toxic or poisonous foodstuffs, smell is "for" detecting pheromones and finding mates, etc. The knowledge we take from our senses, then, is "for" survival and reproduction.

However, in both the Aristotelian and Darwinian views of the world, knowledge—the information our senses provide us with—has two teleological components. First, it does not seem a stretch to say that the current functional purpose of our eyes is to receive light (this is not the same as saying that eyes evolved with that intended objective, which would imply that before there were eyes, an organism dreamt of seeing and strove to create a way to do so). Second, our brains use the information received from our eyes to direct us to objectives that we have in mind— pursuing that deer, searching for our lost keys.We might note that once sight evolved as a distinct function, integrated with the brain to regulate motor and other behavior, it is philosophically reasonable to say that the sense was modified by evolution (e.g., to achieve greater light and color sensitivity or focusing resolution) "for" (at least, in relation to) what today is its function. A pure mechanician might argue that our awareness that we are purposive is itself molecularly programmed, but we can leave that ultimately philosophical issue aside.

As stated earlier, we generally attribute to René Descartes the view of the body as a machine. He wrote in 1664:

First of all, I want the reader to have a general notion of the entire machine which it is my task to describe. So I will say here that the heat in the heart is like the great spring or principle responsible for all the movements occurring in the machine. The veins are pipes which conduct the blood from all the parts of the body towards the heart, where it serves to fuel the heat there. The stomach and the intestines are another much larger pipe. . ..

(Descartes, Treatise on Man, 1664)

Intrinsic to the Western scientific method and tradition is the purposeful dissection of a system into its constituent parts so that we might analyze them in order to understand the whole. Thus we try to understand the senses individually, in a Cartesian way, even though we know that taste without smell is not as rich and that a homing pigeon relies on smell as well as sight to find its way. What does it mean to understand the parts, then? And, even after we reduce the senses to their molecular and cellular pathways in fact this tells us nothing about their "purpose," how the brain interprets sensory signals sent to it, or how information from all the senses at once is integrated, and the like. These kinds of questions cannot be reduced, or answered sense by sense.

In this and succeeding chapters we discuss many of the ways in which organisms perceive and respond to stimuli in their external environments. The stimuli we discuss include sound, touch, movement, chemical gradients, temperature, gravity, light, taste, smell, and the electromagnetic spectrum including infrared and ultraviolet light, electricity, and magnetism. Except for the constant forces of gravity and magnetism, a key fact is that these stimuli are unpredictable and of varying intensities and ranges. This unpredictability is comparable to that of the molecular diversity confronting the immune system. An organism's ability to perceive them must be open-ended in a similar way. Light comes in many colors and levels of intensity, odors can be perceived as good or bad, seductive or noxious, sound is loud or soft, high-pitched or low.

One way or another, most if not all organisms, from bacteria to plants to invertebrates to vertebrates, have evolved receptors to at least a subset of these stimuli and are able to respond to a range of many of them. For each organism's life circumstances, the ability to discriminate among such stimuli has been at least sufficient for its survival—or, to survive, the organisms used what they had. Whether in some way it might be useful to be even more sensitive is moot. Thus whether humans would make use of better night vision or an ability to hear musical instruments producing lower sounds, or the like, these questions are irrelevant because our senses did not evolve with the purpose of seeing well in the dark, or capturing all vibration as sound.

A distinction is often made between the detection of internal and external stimuli, but this distinction, again in the manner of Descartes, may not be as clear-cut as it is often presented. Organisms monitor their internal as well as external state; the distension of the gastrointestinal system, blood pressure, or the levels of hormones such as insulin or glucose, salt and pH at the cellular level, and so forth. Receptors for internal events, interoceptors, share some principles of structure and function with receptors for external stimuli, exteroceptors. In all these systems, signals are received in specialized cells in the sensory organs and the information is transduced and transmitted to the central nervous system for deciphering. In addition, organisms can only respond to changes in pH and temperature and the like if they are monitoring their own internal environment so that they are able to determine when indeed there is a change. In fact, one could argue that the immune response is a form of monitoring and defending against threats from the external world—it just happens to be done internally. Immune detection and response is somewhat different from the usual notion of a "sense" because it happens strictly at the molecular level without being cognized; but there can be organismal response (sleeping in mammals, seeking warmth in cold-blooded species, and the like). However, for the purposes of this chapter, we will ignore these kinds of muddied distinctions and concentrate somewhat arbitrarily on responses to external physical and chemical stimuli.

WHAT ARE SENSES, AND WHY DO THEY EXIST? If Aristotle and the other ancients defined senses in a rather restricted and perhaps anthropocentric way, here we are interested in generalities that we can draw from knowing something about these systems in very different organisms. What is sensation, and why do organisms have it?

As a general statement, we can characterize senses as the means by which organisms are stimulated by their external environment to react in some way. Here, the environment includes macromolecular (touch, sound), energetic (e.g., heat, magnetism, light), and chemical (pH, odors, tastes) characteristics, but signals from these kinds of stimuli may overlap. The nature of perception need not be neural and certainly not conscious, in the usual sense of awareness (but are ants "conscious" of each other when, as noted by Dante, they "touch their muzzles, each to each, perhaps to seek news of their fortunes and their journeyings" (Alighieri 1314)?). Similarly, in discussing response to environmental information we do not restrict ourselves to any particular types of response.

It is more than rhetorical to suggest that the division of sensation into discrete Cartesian categories is artificial. Such division is based on incompleteness but also to a considerable extent on how humans are structured to receive environmental signals (e.g., with distinct eyes, nose, and ears) as well the experiential aspects of how we perceive them, and thus seems "natural." For practical reasons, the treatment below classifies sensation in broad categories, but we will show how this categorization is largely a human creation and, in particular, that the genetic mechanisms involved in different modes of sensation are often very closely related and probably ancestrally identical.

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