Which living things have senses?

Case study: viruses

Image of influenza virus.
Copyright Linda M. Stannard, Department of Medical Microbiology, University of Cape Town, 1995.

Viruses (and all other organisms) exhibit some degree of phenotypic plasticity, which can be defined as the ability of organisms with the same genotype to vary their developmental pattern, phenotype or behaviour in response to varying environmental conditions (Ancel and Fontana, 2002).

A well-known case of phenotypic plasticity in viruses is the lysis-lysogeny decision, whereby parasitic lambda-phage viruses adopt a bet-hedging strategy in order to cope with fluctuations in the availability of their hosts (E. coli bacteria). When a virus invades a host bacterium, it may kill the host immediately by multiplying until the host's cell walls burst (lysis) or it remain quiescent and may confer immunity to infection upon its host (lysogeny). The strategy is described in detail in the Appendix. The important thing is that the actual decision to invade or lie low is a random one, which depends entirely on thermal background noise. As one researcher puts it:

"...Thermal fluctuation at the molecular level makes for diversity in cells that start out under identical conditions," says Arkin. "The phage actually makes use of noise as a survival mechanism: sometimes it pays to multiply and infect as many hosts as possible, sometimes it pays to lie low. Either way, the viral population is prepared to cope with changing conditions" (italics mine).

The above behaviour does not seem to meet the criteria required for the adoption of Dennett's intentional stance. At the very least, viruses need to possess information that enables them to realise their goals. However, viruses, which are little more than living molecules, have no built-in sensors. In this instance, we do not see viruses possessing (i.e. encoding or storing) information about environmental conditions conducive to replication, but simply responding to changing conditions.

Our discussion of phenotypic plasticity in viruses has yielded one important conclusion regarding mental states in organisms:

S.1 An organism must be capable of encoding and storing information about its environment before it can be said to possess mental states.(Corollary of Conclusion I.2.)

Case study: bacteria

Staph bacteria. Picture courtesy of Janice Carr/CDC via BBC.

Bacteria, unlike viruses, certainly possess sensors. According to John S. Parkinson, a professor of biology at the University of Utah, "most organisms - even bacteria - can sense sound, light, pressure, gravity and chemicals" (University of Utah, 2002). E. coli bacteria "can sense and respond to changes in temperature, osmolarity, pH, noxious chemicals, DNA-damaging agents, mineral abundance, energy sources, electron acceptors, metabolites, chemical signals from other bacteria, and parasites" (Meyers and Bull, 2002, p. 555). Bacteria are very sensitive to chemicals - for instance, E. coli bacteria have five different kinds of sensors which they use to detect food. As Di Primio, Muller and Lengeler (2000, pp. 4 - 5) explain, common bacteria like E. coli swim in chemical gradients towards attractants (e.g. glucose) or away from repellents (e.g. benzoate) - a phenomenon known as chemotaxis. Other bacteria display phototaxis and magnetotaxis, or movement in response to light and magnetic fields, respectively (Martin and Gordon, 2001, p. 219). Bacteria possess an elaborate chemosensory signaling pathway, which involves the phosphorylation (combination with phosphorus compounds) of a set of proteins in the cytoplasm of a bacterial cell (Blair, 1995, p. 489).

There are several philosophical questions relating to the sensitive capacities of bacteria. Should we call these capacities bona fide senses? For that matter, what are senses, anyway? Is there a distinction between sensing an object, and being sensitive to (or being affected by) it? And is the possession of senses by an organism a sufficient condition for its having perceptions (which, in common parlance, are mental states), or can an organism have senses without the capacity to have perceptions?

What are senses?

In principle, anything is capable of acting as a sensor: camera film is photosensitive, as are metals which release electrons when exposed to light (the photoelectric effect). The bimetallic strip in a thermostat is a temperature sensor.

Daniel Dennett. Photo courtesy of University of California.

On Dennett's account, any sensor can be described using the intentional stance: it is a "micro-agent, ... an utterly minimal intentional system whose life project is to ask a single question, over and over - 'Is my message coming in NOW?' ... - and spring into limited but appropriate action whenever the answer is YES" (1997, p. 108). It is intentionality at this level, Dennett argues, that makes perception possible, and allows an animal to process information about its surroundings.

Dennett believes that there is no difference between the sensitivity displayed by phototactic bacteria and the photosensitivity of light meters in cameras. I would argue that he is profoundly mistaken here: it was argued in the previous chapter that there is a fundamental distinction between living individuals (such as bacteria), which possess a formal cause (i.e. a master program that regulates their internal structure and the interactions between their components), as well as a final cause (arising from the intrinsic relations between their parts, which are organised in a nested hierarchy of functionality), and the merely extrinsic finality found in current man-made devices, which are assemblages rather than individuals, and which possess neither a master program nor a nested hierarchy of organisation.

Aristotle.

Should we, then, say that an individual has bona fide senses if and only if it is alive? Aristotle thought not: he maintained that senses are not found in all living things. Aisthesis - which in his writings "is capable of bearing the meanings both of sensation and of perception" (Lawson-Tancred, 1986, p. 78; see also Sorabji, 1993, pp. 8, 15) - is found in animals, and only animals (De Anima 2.2, 413b1ff; 3.12, 434a30; 3.13, 435b1). Aristotle stresses that senses exist for a practical, teleological reason: they are discriminative capacities (De Anima 3.9, 432a16), which enable animals to survive. Without these capacities, animals cannot avoid danger or acquire what they need (De Anima 3.12, 434b - 1ff). This is particularly true of animals that move around: "If any body that travels did not have perception, it would be destroyed and so not achieve nature's function by reaching its purpose" (De Anima 3.12, 434a33-34). Since bacteria also travel, we require a philosophical justification for any distinction that may be drawn between the sensory capacities of animals and the sensitivity exhibited by bacteria. Does Aristotle's definition of sensation offer such a justification?

Aristotle argued that there is more to sensing an object than merely being affected by it:

For perception is being affected in a certain way. Thus the active thing [the sense object - V.T.] makes that [the sense organ - V.T.] which is potentially like it, like it in actuality...[T]he sense is the recipient of the perceived forms without their matter, as the wax takes the sign from the ring without the iron and gold... And it is also clear why it is that plants do not perceive, though they have a psychic part and are in some way affected by the touch-objects. After all, they become cold and hot. The reason, then, is that they do not have a mean, nor such a principle as can receive the forms of the sense-objects, but are affected by the matter as well (De Anima 2.11, 424a1; 2.12, 424a17-19, 424a34-424b3, italics mine).

What Aristotle seems to be arguing is that although a living thing which senses an object (with one of its sense organs) is altered by that object, it is not altered by taking that object into itself, but rather by taking on the object's form, without its matter. Using contemporary jargon (which is etymologically rooted in the form-matter distinction), we might describe this process as a reception of information. For Aristotle, to be able to sense or perceive an object means, roughly, to be a living thing with a sensory organ that can encode information about that object.

There remains the question of what Aristotle meant by saying that aisthesis is "a kind of mean of the opposition in the sense-objects, and thus a judge of them" (De Anima 2.11, 424a1ff). Later, he argues that to perceive A and B (e.g. white and black) the sense-organ must be neither in actuality but both in potentiality. How does this notion of a mean tie in with the requirement that sensory organs be capable of receiving forms without matter? I would suggest that the key lies in Aristotle's remark that "it is the mean that judges" (De Anima 2.11, 424a6). Since aisthesis is a discriminatory capacity, the sense organ needs to not only be able to encode information about its object, but also be separable from the information that it encodes about its object - i.e. it is not always actualised in the same way, and may even be capable of existing in an inactive state. Our eyes can be said to sense colour, only because they do not always see any given colour: at night, they see nothing at all. (Aristotle's remarks on vision are unfortunate; he regards white and black as "two ends of the scale" (De Anima 2.11, 424a7-8), whereas black is, in reality, the absence of light - precisely the kind of mean he is looking for.) A sensory deprivation tank is one way of illustrating the notion of a mean: here, we have a perfect separation of sense organs from the sensory information they encode, as none of the sense organs is being activated.

On Aristotle's account, there are thus two ways in which sensitivity in an organism can fail to qualify as a bona fide sensory capacity: either the actual state of the object sensed may not be encoded as information, or the sensor may be unable to represent different actualisations of its object (e.g. different temperatures). Certainly, the distinctions drawn by Aristotle are not trivial ones. The question is: does the sensitivity exhibited by bacteria measure up to Aristotle's criteria for sensory capacities?

Bacteria possess specialised "receptors" or information-encoding devices, which are sensitive to light, chemicals, magnetic fields and so on. These receptors may or may not be activated, depending on the local environment. A bacterium has two kinds of motion: directed movement (a "run", which occurs when a bacterium's rotary motors or flagella, rotate in a counter-clockwise direction) and random tumbling (which occurs when a bacterium's flagella suddenly change direction and rotate clockwise). When the external section of a bacterial receptor recognizes and binds its target, a signal passes through the rest of the receptor and causes sequential changes in two proteins inside the bacterium. (This two-protein sensing system is found in all bacteria and in many other life-forms, but not in animals.) The first protein is called a kinase and sits next to the receptor. Normally, when there is no signal, this protein activates a second protein, the regulator, which interacts with the gear shift of a bacterium's flagella, causing them to turn clockwise and the bacterium to tumble randomly, about once every second. However, when there is a signal from the receptor, the kinase cannot activate the regulator protein. Thus, the flagella continue to turn counterclockwise, and the bacterium, instead of tumbling, swims smoothly towards the target (Aegerter, 1997). What is more, these receptors can even store information about their objects over a short period of time - in other words, they possess a kind of "memory" (to be discussed later). On Aristotle's account, there appears to be no good reason for denying sensory perception to bacteria, as their receptors can encode information about their objects (attractants and repellents), at different actualisations (i.e. concentrations of attractants), spanning five orders of magnitude (Illingworth, 1999).

This may be a surprising conclusion, given Aristotle's denial that plants can perceive (De Anima 2.3, 414a31, 3.13, 435b1). However, knowing what we now do about organisms, it is reasonable to infer that he would revise his conclusions. A modern commentator, Charles Kahn, has argued that Aristotle "would have been obliged to" grant one-celled animals "a share in perception proper... since the possession of a sense faculty is included in the definition of an animal" (1979, p. 25). Moreover, Aristotle would have probably classified bacteria as animals, since they are capable of locomotion, which he regarded as a capacity possessed only by some animals (De Anima 3.9, 432b19) In fact, Aristotle explicitly declared: "No non-stationary body has a soul without perception...If, then, any body that travels did not have perception, it would be destroyed... After all how is it to be nourished?" (De Anima 3.12, 434b2-3, 434a33, 434b1). It should also be pointed out that van Leeuwenhoek, the first person to observe bacteria through his microscope, called them "little animals" or "animalcules" (Waggoner, 1996).

An objection from Cotterill

Rodney Cotterill. Picture courtesy of Danish Technical University

Recently, Cotterill (2001) has denied the existence of proper senses in bacteria, because the order of stimulus and response is reversed: instead of environmental changes acting as the stimulus which causes a motor response in a bacterium, the bacterium initiates its own random tumbling movements and thereby gains information about its surroundings, using a short-term memory that informs it as to whether the concentrations of certain molecules in its environment have changed in the last few seconds. As Cotterill puts it:

The stimulus in this case is thus the motor movement, while the response is that of the impinging substances. This is just the opposite of a reflex... There are no senses, of the type found in more advanced species, and the internal state of the creature is embodied in the concentrations of various molecules. These concentrations dictate the creature's movements (2001, pp. 3-4).

In a creature with reflexes, by contrast, the motor response is "independent of the creature's internal state" (2001, p. 5), and the reaction of a specialised receptor cell in the creature's body to "an unprovoked stimulus" (2001, p. 5, italics mine) leads to a rapid, automatic motor response.

Cotterill's main argument can be recast in an Aristotelian form. He acknowledges that bacteria can store information relating to the concentrations of substances in their surroundings (2001, p. 6), but insists that sensing an object means something more than that. In Aristotle's account, sensing an object meant being affected by it in a certain way, and an animal's desire of the sensed object produces locomotion towards it (De Anima 3.10, 433a16). In bacteria, according to Cotterrill, "sensing" an object means acting upon it, and it is the perpetual movement (locomotion) of bacteria that enables them to "sense" chemicals. That is, locomotion is prior to "sensation".

We can express Cotterill's objection another way, by saying that sensations are a form of "feedback", whereas bacteria seem to use "feed-forward" instead to navigate around their environment. Certainly, bacteria are much more active in probing their environment than other sensitive organisms, because of their size: since they are too small to gauge spatial variations in the concentrations of molecules in their environment (e.g. differences between concentrations at their anterior and posterior extremities), they have to actively "sample" their surroundings, relying on a form of short-term chemical memory to alert them to changes.

One must, however, distinguish two kinds of bacterial motion: (a) the random tumbling movements which bacteria initiate in order to probe their surroundings, and (b) the directed "runs" which they make along chemical gradients towards attractants. I would agree with Cotterill's characterisation of movement of the former kind as a stimulus and its feedback about its environment as a response. But it is only movement of the latter kind which Aristotle would characterise as locomotion, or "movement started by the object of desire" (De Anima 3.10, 433a16). This kind of motion is subsequent to, not prior to, the act of sensing the attractant. Moreover, the change in a bacterium's pattern of movement (from random tumbling to directed swimming) is (ultimately) produced by events occurring outside its body: variations in the concentrations of attractant or repellent molecules. This does not sound so different from the Aristotelian of perception as "being affected in a certain way" (De Anima 2.11, 424a1).

Cotterill also points out that bacterial "sensing" differs from animal senses, in that bacteria employ chemical signaling, which is much slower than the electrochemical signaling used by animals and other organisms (Illingworth, 1999; Cotterill, 2001, pp. 4-5). However, this appears to be a difference of degree rather than kind.

Which living things have senses?

To sum up: although there are significant differences between the ways in which bacteria and other organisms sample their environment to detect changes in it, there does not appear to be any good reason to deny them sensory capacities. We can now formulate a conclusion about the scope of sensory capacities in organisms:

S.2 All cellular organisms possess sensory capacities, insofar as they all have sensors that are capable of encoding different states of information about their surroundings.

The term "cellular organisms" includes prokaryotes and eukaryotes, but excludes viruses.

There are, however, important differences between bacteria and animals regarding the causes of their movements, which may be relevant to the question of whether bacteria can be properly said to have appetitive states such as desire. This will be addressed in chapter 3.