Fixing Content and Function in Neurobiological Systems:

Keywords: adaptationism, Daniel C. Dennett, electric fish, electroreception, evolution, evolutionary function, indeterminism, mental content, neuroethology, sensory modality, underdetermination

Introduction

In his 1987 book, The Intentional Stance, Daniel Dennett defends a position concerning attributions of function (in biology) and content (in psychology) according to which neither is determinate. Content and function attributions are the result of a process of “retrospective radical interpretation” (283). In psychology, we begin our explanations of behavior, according to Dennett, by assuming the rationality of the agent and then attributing content (i.e., intentional states such as beliefs, desires, intentions) to the agent according to a strategy he calls the “intentional stance”. Similarly, in biology, we begin our explanations for the existence of behaviors and structures by assuming the optimality of natural selection and then attributing functions these structures and behaviors in the process commonly known as “adaptationism”. Dennett writes, “The problems of interpretation in psychology [determining content] and the problems of interpretation in biology [determining evolutionary function] are the same problems, engendering the same prospects–and false hopes–of solution, the same confusions, the same criticisms and arguments” (1987: 277, emphasis in original).1

Dennett argues that, in biology, “We take on optimality assumptions not because we naively think that evolution has made this the best of all possible worlds, but because we must be interpreters, if we are to make any progress at all, and interpretation requires the invocation of optimality” (278-279). Dennett offers a similar analysis of the rationality assumption in psychology. He writes,

We cannot begin to make sense of functional attributions until we abandon the idea that there has to be one, determinate, right answer to the question: What is it for? And if there is no deeper fact that could settle that question, there can be no deeper fact to settle its twin: What does it mean?

(319)

Dennett nicely sums up his own position: “It is not just that I can't tell, and they can't tell; there is nothing to tell” (312). Content and function are indeterminate because there simply is no “fact of the matter” in either case. For Dennett then, attributions of content and function are intimately related, and for both he draws the same indeterminist conclusion.

In this paper, I begin by accepting Dennett's claim for the close relationship between content and function attributions. Instead, I challenge his characterization of these attributions as indeterminate and unfixable. I will argue that, contrary to his analysis, attributions of content and function are determinate, at least insofar as it is relevant to scientific attributions of both. There are facts of the matter, I claim, and we do make such determinations. To support my argument, I will consider the case of the twentieth century discovery of electroreception. Electroreception is relevant because this non-human sensory modality–the ability to perceive the environment via electricity–was only discovered this century, and yet the existence of this modality commands a strong consensus among present-day scientists. That is to say, there is today a strong scientific consensus that certain organisms possess anatomical structures which have the function to process electrical information about the organisms' environments. (It is notable that other proposed non-human modalities, such as vertebrate magnetoreception, lack a similarly strong consensus.)

Electroreception is a sensory modality and thus provides an added advantage, vis-a-vis Dennett's claimed relationship between content and function, in that it cuts across the distinction between content and function. Attributing electroreception to particular animals simultaneously involves hypotheses about both content and function. More specifically, it proposes that these animals possess structures, undergo processes, and exhibit behavior that have the function of bringing about a particular kind of contentful connection between the world and the organism. A claimed discovery of a new modality in certain fish and other organisms is a claim about the evolutionary function of particular structures those animals possess. It is the function of these structures to act as sensory organs to process electrical information, just as it is the evolutionary function of hearts to circulate blood and the function of birds' wings to allow flying.

The electroreceptive hypothesis is also a claim about the kinds of sensory content that such organisms possess. Sensory systems are, by their very nature, perceptual content production and manipulation systems. To claim that sharks, say, are genuinely electroreceptive is to claim that these organisms are capable of representing a particular kind of environmental information, i.e., electrical information.2 Nonetheless, given Dennett's arguments for a connection between content and function attributions, then if I can undermine either the argument for content indeterminacy or the argument for function indeterminacy, the remaining claim will as a consequence meet the same fate. That is to say, since Dennett argues that attributions of function and content are indeterminate for the same reasons, then (by his lights) undermining one set of arguments should simultaneously undermine the other.

In their own attempts to undermine Dennett's arguments, some (Kitcher and Kitcher 1988; Amundson 1988) have pointed out a curious mismatch between his conclusions and day-to-day scientific practice. Far from being mired in a morass of indeterminism, biologists seem to fix the evolutionary function (or functions) of biological structures, processes, and behavior all the time. Biologists take as their ken, such questions as: Why do male guppies have spots? Why do fish and birds flock? What does this structure do in this organism? In answering these questions, biologists often make reference to the concept of evolutionary function; guppies have spots, say, because male guppies with spots (of a particular type) have historically had a reproductive advantage over those which did not.3 The actual story is no doubt a great deal more complicated than this simple statement, but as shorthand for the long-winded, causal-historical description, we say that male guppies have spots in order to attract females; the function of the spots is to attract females.

Dennett offers three counter-arguments to such claims. First, function and content determinists generally fail to tell stories in enough detail to refute the thesis of indeterminacy. Dennett (1988b) points out that, “The guppy example is supposed to exhibit a case in which careful biological research yields determinate (but complex) attributions of function. Why then do [functional determinists] refrain from concluding their tale by telling us exactly what the function (or functions) of those guppy spots is and is not?” (540). Dennett is here setting a high standard. Philosophical “toy examples” will not do; neither will hand-waving. I accept Dennett's challenge and, in Section II, I provide a highly detailed account of the scientific history of the discovery of electroreception. This discovery was the result of an interdisciplinary investigation–an endeavor best characterized under the rubric “neuroethology”, the biological study of the neural basis of animal behavior.

Second, Dennett (1988b) notes that it is no argument against indeterminacy arguments that some attributions are, “obviously wrong, and it is no argument in favor of functional determinacy that some functional attributions are obviously right (the eagle's wing is obviously for flying, and the eye for seeing)” (540, emphasis in original). Setting aside worries about this claim's cogency (see Note 5, below), let me stress that the possession of electroreception is far from obvious. Indeed, it is so non-obvious that even though humans have been aware of the existence of electric fish for at least three thousand years, it is only during the last century that the possibility of electroreception has been imagined.

Third, Dennett (1988b) gives reason to believe that a longer and more detailed story–even one packed with causal details–would still fail to answer his philosophical objections: “There is causation to be taken into account at all times by the psychologist, and by the biologist. Neither, however, has succeeded in telling a watertight causal story that licenses functional, or referential, interpretations” (541, my emphasis). According to Dennett, no matter how much causal detail is amassed, there will always be room for multiple interpretations. To address this worry, a careful analysis of the components of the neuroethological case for electroreception will be developed in Section III. This will demonstrate how various kinds of evidence are necessary for such attributions, but also how each, on its own, is insufficient. The point of this analysis is to show how specific kinds of scientific detail both constrain the space of possible explanations and offer support for specific interpretations. Then, in Section IV, I argue that such a story is as “watertight” as it needs to be in order to fix content and function.

The metaphysics and epistemology of content and function

What are content and function, such that they are either determinate or not? In this paper, I endorse the standard etiological accounts of content and function. The primary contemporary proponent of the etiological account of both content and function is Ruth Millikan. In two influential books, Millikan (1984, 1993) has argued for a causal-historical approach to psychology and biology–an approach she calls the theory of “Proper Function”. For Millikan (1993), content and function are best understood in terms of evolutionary history: “A proper function of ..... an organ or behavior is, roughly, a function that its ancestors have performed that has helped account for its own existence” (14). To use one of her favorite examples, what makes it the function of a heart to circulate blood is that it is in virtue of its blood-pumping properties (and not, say, its weight or color) that organisms which have possessed hearts have differentially successfully reproduced in competition with organisms whose hearts did not possess the same blood pumping properties. According to Millikan, function is a matter of an organism's evolutionary history and is not due to current properties or propensities.4_

A similar story can be told about content. Dretske (1981, 1988, 1995) and others have defended a causal-historical account of content. On this account, a particular physical or neural state has a particular content if that state has the appropriate causal connection to the appropriate state or states of the world. In many respects, this account of content parallels the etiological account of function. On the causal account of content, a state has the content it has because of its place within a particular causal history. According to Dretske, content is a matter of an organism's causal history and is not due to current properties or propensities.

On both of these accounts, what it is to have a particular function or content is to have a particular causal history. This account is fine as far as it goes. It is limited, however, to the theoretical or metaphysical nature of content and function. Such characterizations tell us what it is to be (or to have) a function or content. The central issue here has a distinctly more epistemic flavor. My central question is: Whatever content and function are, can we ever know them? Can we ever discover, in Dennett's phrase, “some fully determinate truth about what things mean, or what their functions really, truly are” (1988b: 540)? Borrowing a phrase from Peirce, how do we fix content and function (if content and function are the sorts of things that can be fixed)?

To date, the philosophical work on content and function has mainly focussed on the metaphysical issue, and less attention has been given to the epistemic standards of evidence required to make content and function claims, supposing that some version of the etiological theory is correct. Notice that Dennett's claim about indeterminacy involves both the metaphysics and epistemology of content and function. He claims that content and function are epistemically unfixable (“we can't tell”). However, the reason for this epistemic situation is his claim that content and function are metaphysically indeterminate (“there is nothing to tell”). For Dennett, the metaphysics and epistemology go hand-in-hand. It is the nature of content and function that they are unfixable.5

My strategy is to argue backwards through this relationship. Regardless of the ultimate metaphysical nature of content and function, the case of the discovery of electroreception demonstrates that they are indeed fixable. As the Kitchers, Amundson, and others have pointed out, biologists fix function and psychologists fix content all the time. That content and function are fixable does not tell us everything about the metaphysical or theoretical nature of content and function, but it does take out much of the epistemic sting said to derive from their (alleged) indeterminacy.

Nonetheless, there is still the question of how content and function are fixed. I argue that content and function are fixed by collecting a variety of cross-constraining and mutually supporting evidence. To make an attribution of content or function, one needs concurring evidence from behavioral analysis, anatomical analysis, physiology, ethology, evolutionary biology and adaptationist reasoning. By itself, not one of these sources of evidence is sufficient to explain the strong consensus on behalf of electroreception, although each provides a necessary piece of the evidentiary story. This collective, neuroethological approach to content and function fixation for which I argue will, with luck and diligence, license the appropriate attributions.

In Section II, I review the history of the discovery of electroreception, tracing the history of the science that led to the discovery of this non-human sensory modality. In Section III, I analyze the evidentiary contributions and limitations of the scientific components that make up neuroethology. The point of this section is to show how these components complement one another; allowing the collection to license content and function claims not licensed by any single component. This then allows me to return, in Section IV, to Dennett's arguments on behalf of indeterminacy using an example that meets his three desiderata: (1) I present a thorough and detailed story of the attribution of electroreception, (2) the attribution of electroreception is not an “obvious” attribution, and (3) such neuroethological claims are sufficiently “watertight”.

Humans have long been familiar with the phenomenon of animal electricity.6 The electric catfish of the Nile (Malapterurus electricus) is featured in Egyptian murals and statuary. Hippocrates, Plato, and Aristotle were familiar with the stunning charge of Torpedo ocellata, a Mediterranean species of ray from which the modern words “torpor” and “torpid” derive their meanings.7 Even prior to the development of the modern theory of electricity in the eighteenth century, it was recognized that there was something unusual about certain kinds of catfish, rays, and eels. Soon after the discovery of ways to detect and measure electricity, the true nature of these bioelectric animals was revealed.

The electric ray, the electric catfish, and the South American electric eel (Electrophorus electricus) possess “electric organs” that allow them to produce powerful electrical discharges capable of paralyzing prey or discouraging would-be predators. This discovery led to new mysteries, particularly the discovery of what were called “pseudo-electric” fish. These fresh-water fish from both Africa and the New World were so-called because their anatomy includes structures of highly regular morphology; a morphology strikingly similar to that of the electric organs of the electric eel and the electric ray. However, pre-nineteenth century technology could detect no electrical discharge from these “pseudoelectric organs”. That these organs do indeed generate a genuine, albeit weak, electrical discharge was discovered by Robin in 1865, and Babuchin in 1877. (See Moller and Fritzsch 1993.) Notwithstanding, their discharge was clearly too weak to subserve the kind of offensive and defensive function possessed by electric rays, eels, and catfish (see Textbox 1).

{Textbox 1 about here. Textboxes unavailable for web version.}

The possible function of such a weak electric organ was utterly mysterious and this, in turn, presented a problem to Charles Darwin. In the fourth and subsequent editions of his Origin of Species, Darwin notes that the existence of pseudoelectric fish pose an important challenge to his theory of evolution by natural selection. Darwin (1897) writes,

Although we must be extremely cautious in concluding that any organ could not have been produced by successive, small, transitional gradations, yet undoubtedly serious cases of difficulty occur.

[…]

The electric organs of fishes offer [a] case of special difficulty; for it is impossible to conceive by what steps these wondrous organs have been produced. But this is not surprising, for we do not even know of what use they are. In the Gymnotus [sic8] and Torpedo they no doubt serve as powerful means of defence, and perhaps for securing prey; yet in the Ray [Raja clavata], as observed by Matteucci, an analogous organ in the tail manifests but little electricity, even when the animal is greatly irritated; so little, that it can hardly be of any use for the above purposes. (234)

The existence of pseudoelectric organs posed a significant problem for the nineteenth century evolutionary biologist. The first step in giving an evolutionary account of a trait is to form a hypothesis as to its possible adaptive function. Nineteenth century biologists–as Darwin attests–could not begin to imagine the function of pseudoelectric organs. I will refer to this as “Darwin's Problem”. Darwin's own solution was to bide his time until more evidence could be collected and an answer found:

[We cannot currently go far] in the way of explanation; but as we know so little about the uses of these organs, and as we know nothing about the habits and structure of the progenitors of the existing electric fishes, it would be extremely bold to maintain that no serviceable transitions are possible by which these organs might have been gradually developed.

(235)

According to one line of reasoning, pseudoelectric fish organs no longer have a function. That is to say, these structures are vestigial (Du Bois-Reymond 1884; Rosenberg 1928; Dalhgren 1910). (See Moller 1995: 26.) On this account, the pseudoelectric organs are best thought of as atrophied versions of the powerful electric organs of electric eel or electric ray (which have a more obvious, offensive or defensive function). Of course, the gradualist problem about the evolution of strong electric organs in the first place would still remain.

By the turn of the century, some began to suspect that, in addition to the ability to generate electricity, some animals could detect the presence of electricity in their environment. In 1891, Fritsch “observed that mormyrids [the African family of pseudoelectric fish], when `surprised' by a pair of recording electrodes, avoided the metal with great agility.....” (Moller and Fritzsch 1993). The electrosensory hypothesis gained credibility in 1917 when Parker and van Heusen discovered that the non-bioelectrogenic catfish, Ictalurus (Amiurus) nebulosus, could detect galvanic and direct currents. They did so through a series of experiments in which they presented blindfolded catfish with glass, wooden, and metal rods. The fish were able to detect the presence of metallic rods at a distance, but only reacted to the glass and wooden rods when they touched the surface of the fish. They went on to show that the type of behavior (to flee from or to approach and “nibble” at the rod) elicited by the presentation of rods could be modulated by changing the length of rod exposed to the water. Parker and van Heusen correlated the amount of exposed metal with the amount of galvanic current produced by the rods, and then reproduced the behavioral results using direct electrical currents presented via electrodes placed in the aquaria with the catfish.

To what do Parker and van Heusen attribute this observation (that their catfish behave differently depending on the amount of electrical stimulation in their environment)? Notably, they do not posit an electroreceptive modality. Rather they propose that electric detection is mediated by the gustatory system, more specifically, by the taste buds. Their reasoning was that, (1) electrical stimulation elicits feeding responses and these behaviors are typically mediated by the gustatory system, (2) the head of the catfish is the most sensitive to stimulation, and most taste buds are found on the head,9 and (3) “This assumption is completely in line with what has long been known of human taste organs for these are easily stimulated by direct currents of very low energy value” (419). (Think of the distinctive sensation elicited by touching a 9-volt battery to the tongue, and 9 volts is far above the human threshold of sensitivity.) However, they admit that such evidence is inconclusive, for “[a]side from these general indications, however, we have no grounds for any determination as to the exact sense organ concerned” (418). They conclude, in the terminology of sensory physiology, that these catfish have only the capacity to electrodetect and do not possess a true electroreceptive modality (see Textbox 2).

{Textbox 2 about here}

A consensus on the ability of certain animals to electrorecept did not come until after the publication of several landmark papers by Hans W. Lissmann and his colleagues in the 1950s. The first, Lissmann's 1951 Science paper, confirmed that the so-called pseudoelectric fish were genuinely, albeit weakly, bioelectric. He measured weak, but highly regular fields generated by these fish and showed that such signals were very similar within species, but differed between species. Lissmann's discovery contributed to the renaming of pseudoelectric fish, which have since been known as “weakly electric” fish.

However, Darwin's Problem remained: Exactly what is the function of these weakly electric organs? Lissmann (1958) acknowledges Darwin's Problem: “The inadequacy of functional and evolutionary theories of electric organs in fish has been apparent for a long time” (156). He explicitly addresses this inadequacy: “In the absence of any existing, coherent theories about the evolution of electric organs, and about the function of weak electric organs, the speculative picture presented here may fill a gap” (186). Lissmann proposed his answer in two papers published in 1958. The first paper, entitled “On the function and evolution of electric organs in fish”, is a detailed exposition of an idea first suggested in 1947 by C. W. Coates of the New York Aquarium. Coates had speculated that the discharges of weakly electric fish are used to locate objects in their environment. That is to say, the electric organs of weakly electric fish subserve an electrosensory function.

Lissmann rejects the vestigial account. This account claims that strong electric organs evolved first and that they later degenerated into weak, pseudo-electric organs. Instead, he concludes that, “the easiest explanation for the evolution of strong electric organs would appear to start from ..... muscular action potentials, and proceed via weak electric organs used for orientation, to the powerful offensive and defensive organs [of electric eels, say]” (188). He supports this conclusion by presenting a series of discharges recorded from a variety of weakly electric species. Across every species investigated, these electric organs produced precise, stereotyped discharges. Lissmann reports on comparative ethological (in the field) and behavioral (in the laboratory) studies of representative species of seven genera of the African family, Mormyridae, and on behavioral studies of several members of the South American gymnotids.

Lissmann's conclusion from his work is that, contrary to the vestigial account, “the weak electric fish discussed here represent already very advanced, highly specialized forms” (186). According to Lissmann, far from being vestigial and without function, these electric organs play an important role in the lives of these animals: weakly electric fish use the discharges of their organs to actively locate objects in and navigate through their often dark and murky environments. He demonstrates the role of their electrosensory abilities with a series of experiments. Here is a description of a characteristic set of observations:

..... some preliminary experiments were carried out in Africa. A cloth partition was fixed in an aquarium dividing it into two equal halves. This partition consisted of a wooden frame over which the cloth was stretched on both sides, so that the two layers of cloth were about 2 cm apart. This frame was fitted into the aquarium by means of plasticine, and could be expected to be transparent to electrical but not visual stimuli. One Gnathonemus senegalensis [an African species of weakly electric fish] was introduced into one compartment of this tank and allowed to settle down for 2 days. After this period a second fish of the same species was carefully introduced into the second compartment. Both fish were resting motionless on the bottom. Recording electrodes introduced into the tank showed that both fish were discharging at a fairly low and regular rate. Whenever one of the two specimens was gently touched with a glass rod its discharge rate went up abruptly and the fish in the other compartment usually followed suit. When one fish was removed, a similar movement of the glass rod in the empty compartment remained without effect. These two specimens were left in the tank overnight. After darkness the light of a dim torch showed them both swimming up and down on opposite sides of the partition, obviously taking note of each other's presence and discharging with higher frequencies. Bursts of discharges from both fish coincided when they came close together, but no correlation in the timing of the individual pulses was noted. This observation, though not conclusive, does suggest that the electrical discharges may play a social role in the life of the Mormyridae. (169-170)

Lissmann does not pursue that final speculation on the social role of electrical discharge in these papers. (Although see Lissmann 1961.) However, later work has shown him to be largely correct. Lissmann instead focuses on the possible role of electrical discharges in perceptual and orientating behavior. He does this by:

(1) describing the nature of the electrical field generated around the fish, particularly focussing on the changes (at the surface of the fish) to that field as a result of objects of differing conductances being brought near the fish;

(2) noting the existence of pores distributed across the skin of these fish, and that “these pores lead through canals filled with a jelly-like substance to a variety of sense organs termed `glandular sense organs' or `mormyromasts'“ (181). These mormyromasts seem appropriately distributed across the body to participate in electroreception and are innervated by lateral line ganglia (which typically innervate sensory systems);

(3) noting the ecological conditions under which the fish live (often dark and turbid waters);

(4) noting natural behaviors (in some electric fish) such as being nocturnal and exhibiting a marked and unusual tendency to swim backwards and to explore novel environments tail-first; and finally,

(5) pointing out the unique swimming behavior of certain species of electric fish, who move primarily by undulating a highly specialized anal (or, in some species, dorsal) fin that runs most of the length of the body. This would tend to affect the generated electrical field less than swimming by undulating the whole body or by the use of large lateral fins as most bony fishes do. That so many species of electric fish in both major groups (one from Africa, the other from South and Central America) show a similar fin morphology is evidence of convergent evolution, according to Lissmann (Figure 1).

{Figure 1 about here. Figures unavailable for web version.}

Lissmann does more than offer a merely plausible account of the evolution of electric organs and the adaptive significance of an electric modality. The linchpin of Lissmann's account is his detailed proposal about how electric fish perceive electricity: that, “it can be imagined that such a fish, living in a private, electric world of its own, receives a variety of information through sense organs distributed over the surface of its body which may be likened to an `electro-receptive retina'“ (186).

Having presented an account of its possible adaptive significance, what Lissmann next presents is a hypothesis concerning the mechanism of electroreception. He does this in his second paper of 1958, written with K. E. Machin, entitled “The mechanism of object location in Gymnarchus niloticus and similar fish”. They first demonstrate a distinction between the presumably large number of fish which can electrodetect (or which can passively electrorecept) from those that exhibit genuine, active electroreception. They note that the galvanic currents used by Parker and van Heusen in their catfish experiments are several orders of magnitude larger than the sensitivity threshold of Gymnarchus: “It is clear that the sensitivity of Gymnarchus is of an entirely different order of magnitude to that of the other fish [previously investigated. These include minnow, carp, goldfish, catfish, and stickleback.]” (452). This is crucial because Lissmann and Machin's proposed mechanism of electrolocation requires detecting very small electrical changes; changes much smaller than the comparatively large changes detected by Parker and van Heusen's catfish (see Textbox 3).

{Textbox 3 about here.}

They next go back over the ground originally trod by Parker and van Heusen and demonstrate that their fish are actually detecting electrical changes in the environment, and are not making discriminations based on some other environmental properties. I have not the space here to rehearse these elegant experiments. I will only note the authors' conclusion: “..... [I]t has been shown that Gymnarchus can distinguish between geometrically identical objects if they have different electrical conductivities, and cannot distinguish between objects which, although geometrically identical and with similar electrical effects, have different internal arrangements” (454).

Having shown that Gymnarchus can perceive objects on the basis of their electrical properties alone, Lissmann and Machin then ask what kind of mechanism might carry out such a perceptual feat? They begin by assuming that the mormyromast-type structures found in the skin of Gymnarchus are electroreceptors (455). They next ask how sensitive these “electrical receptors” would have to be in order to carry out the process of electroreception they observed in their behavioral studies? Their answer is based on both physical and mathematical models of an electric fish. The physical model involved an artificially produced electric field mimicking that produced by weakly electric fish. They placed recording electrodes in the water at points corresponding to the surface of a fish, and then recorded changes to electrical properties as objects were passed through the artificial field. This physical model of the kinds of perturbations demonstrably detectable by the fish was supplemented by a mathematical model of the effect of a cylindrical object, of known conductivity, on a dipole electric field in water of known conductivity. They conclude from their models that, depending on the electrical properties of the receptors (specifically, the resistivity of the jelly-filled canals of the mormyromasts), the fish are probably performing both temporal and spatial integration of the potential or its second derivative (see Figure 2). It is important to note here that Lissmann and Machin not only suggest that electric fish are capable of electrolocating, they also outline with a good degree of precision, how that perceptual ability might be carried out in physical, neurophysiological, and computational terms.

To see how Lissmann's predictions about the physiology of electroreception were born out, we need to turn our attention to a second stream of research. While work on pseudoelectric fish and catfish can be characterized as a function in search of an organ, work on the ampulla of Lorenzini was an organ in search of a function. Found in the skin of sharks and rays, the ampulla of Lorenzini has a striking structure. It consists of a long canal leading to swelling (or ampulla), all filled with jelly (Figure 3). Until this century, it was generally accepted that the ampulla was responsible for some form of mechanoreception.

Physiological studies (Sand 1938; Hensel 1955) demonstrated that ampullae are extremely sensitive to changes in temperature, a finding which suggests that perhaps the ampullae are thermoreceptors. However, this hypothesis leaves some unanswered questions. For example, what is the purpose of the long canals? Murray (1960) and Loewenstein (1960) showed that, in vitro at least, these cells exhibit a response to large mechanical distortions. However, this evidence offered only dubious support to a mechanoreceptive hypothesis because the degree of mechanical distortion required to elicit ampullary responses is much greater than that typically experienced by sharks and rays.

In 1962, both Murray and Loewenstein and Ishiko published results indicating that the ampullae of Lorenzini are highly sensitive to chemical changes, specifically small changes in salinity, thereby suggesting a possible chemoreceptive function. However, strong conclusions could not be drawn from such physiological research unless it could also be shown that such changes in salinity actually played a role in the lives of the organisms and that the organisms indeed made behavioral distinctions on the basis of such stimuli. Except for a few species that wander in and out of river mouths, such ethological evidence was not forthcoming any more than it was for the mechanoreceptive hypothesis.

{Figure 2 about here}

These two streams of research–a function in search of an organ and an organ in search of a function–came together in the 1960s. T. H. Bullock and colleagues (Bullock, Hagiwara, Kusano, and Negishi 1961), recording from the lateral line nerve of the electric fishes Gymnotus and Hypopomus, measured differential neurophysiological activity when the fish were stimulated by passing a conductive or insulating object nearby. Significant neural activity was not observed when the fish were stimulated by ethologically-plausible levels of mechanosensory stimulation (brushing the skin with a brush or with weak water currents). They conclude that they have demonstrated the existence of “true electroreceptors” (1427). Part of the basis of this claim is the work that had already been done by Lissmann, Machin and their predecessors–work that demonstrated the ethological, behavioral, and historical cogency of the sensation and discrimination of small changes in the naturally available electric organ discharge current path. As the history of this entire episode plays out, Bullock's physiological work was one of the last pieces of an intricate puzzle, whose solution resulted in a scientific consensus that a new sensory modality, electroreception, had been discovered; there exist organisms that possess anatomical structures (mormyromasts in weakly electric fish, ampullae of Lorenzini in sharks, skates, and rays) with the function of mediating electrical information about their world.10

In following years, electroreception has become a mainstay of neuroethological research. The number of species for which electroreception has been claimed has grown to include salamanders, sharks, skates, rays (Kalmijn 1982, 1987), catfish, sturgeons, paddlefish, lungfish, lampreys, and even the platypus (Scheich, et al 1986). In 1986, scientists at the Smithsonian Institution claimed to have discovered that electroreception even occurs in a species of placental mammal, the Star-nosed mole (Gould, et al 1993), but this claim has recently been called into question (Schlegel and Richard 1992; Catania 1994).11

{Figure 3 about here.}

Research on weakly electric fish has continued. Much of the neural circuitry underlying electroreception and electrically-mediated behavior–from receptor cells to central nervous system nuclei to motor cells–has been uncovered (Heiligenberg 1991). In terms of known circuitry, the electric fish electrosensory/electromotor system is one of the best understood vertebrate systems in contemporary neurobiology. Beyond its use in electrolocation, bioelectricity has been shown to subserve important communication functions, allowing electric fish to easily identify and communicate with conspecifics, even in dark and turbid environs (Hopkins 1977). Fish use their electrical signals as part of complex electrical “mating dances” in much the same way that courting birds “dance” (Hagedorn and Heiligenberg 1985). The ability to send and receive electrical signals provides these animals with an essentially private channel of communication in their crowded, tropical environs.

III

The final stages of the history described above indicate the strength of the consensus in favor of electroreception. Scientific effort has shifted away from trying to show whether electroreception exists to trying to discover exactly which species do and do not possess it and to elucidating further the neurobiological mechanisms that subserve this modality. All this, with a function whose possibility was not even imagined a century ago. What has led to this strong consensus? I claim that it is due to the depth and breadth of evidence brought in its favor. Electroreception has been fixed through a process in which behavioral, ethological, physiological, computational, and evolutionary evidence have all been marshalled in a mutually supporting fashion. The result of this interdisciplinary endeavor is a hypothesis that unifies findings from all of these areas. Lissmann is given primary credit for having discovered electroreception because he had a hand in more areas than any other single researcher. Each area contributes answers to different aspects of the issue, and together they tell the strongest story we can practically expect to have.

The name given to this combination of mutually constraining areas of research is “neuroethology”–a name that traditionally captures a wide variety of research priorities in biology, from neurobiology and ethology (as the name suggests) to computation and evolutionary biology.12 These different areas make a nicely complementary suite of priorities. We need the kind of evidence encompassed by neuroethology to license claims about content and function. The strong consensus on behalf of electroreception is not due to some singular piece of evidence that is both necessary and sufficient. For example, it might be claimed that it is the evolutionary reasoning alone which licenses the claim for electroreception and all the rest (physiology, anatomy, ethology, etc.) is just icing on the cake. To show that this is not the case and that no one area alone is sufficient, let us look at these areas in more detail and determine what they can and cannot do for hypothetical content and function attributions.

Anatomical and Behavioral Analysis

Anatomy and behavior are almost always good places to start, because more often than not they provide that which requires explanation. Having identified a biological trait, organ, capacity, etc., we can begin an investigation by asking two basic questions: (1) Of what is it composed (anatomy)? (2) What does it do (behavior)? The answers to these questions set the initial limits on function/content hypotheses. But research in the other areas may send us back to take another look at anatomy and behavior to see if we overlooked something.

This situation is well illustrated in the case of electroreception. Prior to the birth of modern science, it was well known that certain fish (the strongly electric fish) do something unusual: they induce a numbing feeling in those who would harass them. Anatomical investigation revealed that these organisms have in common an elaborate and intricate organ. Additional research revealed that other animals (the pseudoelectric fish) also share this anatomy, but do not share the striking behavioral anomaly. This discrepancy between anatomy and behavior set the basis for Darwin's Problem. What is the function of pseudoelectric organs, if not to produce the type of behavior associated with strongly electric fish?

Behavioral analysis provided the next piece of the puzzle, when Parker and van Heusen demonstrated that their catfish exhibited an unexpected behavioral capacity for distinguishing objects differing only in their electrical properties. However, lacking firm evidence as to the anatomical basis of this perceptual skill, they cautiously concluded that their catfish were capable of electrodetection. That is to say, the analysis of behavior alone is insufficient to support the stronger claim of electroreception. Looking at behavior alone, it is impossible to distinguish between detection via a previously identified modality and reception via some new modality. Lissmann replicated their work in his weakly electric fish as the first piece of evidence for the hypothesis that such organisms possess an electroreceptive function.

Physiology

Anatomy and behavior go hand-in-hand with physiology. In a sense, physiology is a science situated between these other two areas. Where the behavioral analysis described above primarily focussed on the overt behavior of the organism as a whole, physiology explores the behavior of its components as identified by the anatomist–behavior that ultimately underlies the overt behavior exhibited at the organismic level.

The work of Bullock and colleagues is an excellent example of the role of physiological evidence. They discovered cells in the peripheral nervous system whose physiological responses tracked electrical properties in the environment. In essence, Bullock and colleagues replicated the experiments of Parker and van Heusen, but recorded the neural activity directly instead of simply observing overt behavior.

Physiology offers powerful tools for determining what activity in sensory cells represents. It might seem initially plausible to say that a true sensory cell is one which responds best to some particular type of sensory stimulus. For example, a true electroreceptor would be one which responds best to electrical stimuli. We would have to say “responds best” on this account, because nerve cells will typically respond to many different kinds of stimuli. Press the outside of your eyeball with your thumb and you will elicit a visual percept. However, we do not normally think of the eye as a pressure receptor. A battery touched to the tongue causes a quite distinctive flavor sensation. However, it seems absurd to say that humans are electroreceptive. To avoid such absurdities, someone wishing to wield physiological evidence alone to determine content must be able to show that a given type of stimulus is best at eliciting a physiological response from the nerve cells of the structure in question.

However, this will not work. First, as Bullock (1974) has noted, there is no metric for comparing intensity of stimuli across modalities. Say a given cell responds to intensity x of auditory stimulation. However, it responds equally well to intensity y of chemical stimulation. Based on intensities in qualitatively distinct domains alone, one cannot decide to which stimuli the cell responds best. The problem here is that we lack a cross-modal metric. Based on physiological data alone, we simply have no way of evaluating the intensity of stimuli of different modalities, because we have no way of comparing different quantities of different qualities. For this reason, physiology alone is helpless to distinguish between the various functional hypotheses attributed to the ampulla of Lorenzini: mechanoreception, thermoreception, chemoreception, or electroreception.

A second limitation of physiological evidence is that one of the best stimuli for eliciting responses in sensory cells (actually, to be accurate, in all neurons) is a properly inserted stimulating electrode. Neuronal response covaries very nicely indeed with the amount of current injected into a neuron by an electrode. Chances are, this covariation is much stronger than that recorded with any other stimuli. But it seems absurd to call every neuron known to humanity a “stimulating electrode detector!”

However, these problems are insurmountable only if we consider physiology and nothing else. These problems indicate only that physiological evidence needs to be buttressed by other kinds of evidence. For example, one might respond to the stimulating electrode problem by noting that “electrode detecting” is an unlikely candidate for neuronal function (and “stimulating electrode” is an unlikely candidate for neural representational content) because animals do not typically encounter stimulating electrodes in the natural environments in which they have evolved. Since the etiological/causal theory of content and function defines them in terms of the selection history of the organism, a consideration of normal or natural environments is called for. Such a consideration is the purview of ethology, to which we now turn.

Ethology

Behavioral analysis is typically carried out within the well-controlled confines of the laboratory. However, that which makes the lab attractive (greater control over the stimulus environment of the organism) is also a potential weakness. This is because we are generally more interested in what organisms do naturally in the wild than what they can be coaxed to do in the lab. Physiological investigation also has related problems, as just noted. Because of these problems, ethology offers an important constraint on content/function theorizing. Ethology is the study of animal behavior within natural settings. Ethologists study naturally behaving organisms and attempts to discover to what sorts of stimuli they are normally exposed, as well as to what sorts of stimuli they naturally respond. Where physiology and behavioral analysis tell us what organisms are capable of doing, ethology tells us what they actually do.

The story of electroreception is shot through with ethological considerations. Lissmann collected data in the field, observing the behavior of wild electric fish. Also, in proposing that electric fish were active electrolocators he proposed that weakly electric fish are perceiving electrical signals in their environment that they themselves produce. That is, he simultaneously proposed a sensory function and the ethological plausibility of the signals detected by that sensory system. Electrical fields are indeed in the fishes natural environments because they themselves naturally generate these stimuli. This ethological evidence in favor of electroreception stood in stark contrast to the poverty of ethological evidence in favor of the mechano-, chemo-, and thermoreception hypotheses.

Ethology can be helpful in conjunction with other approaches, but it is not without its limitations. First, the fact that the natural environments of organisms are simply packed with potential stimuli is problematic. In any given situation, there is a virtually infinite set of possible stimuli to which an organism might be attending. The natural world is full of electromagnetic radiation, vibrations, chemicals, etc., and most organisms generally pay attention to all and only those stimuli which it can profitably exploit. Determining what stimulus or set of stimuli is responsible for eliciting a given behavior requires controlled experiments with known stimuli.

As if the plurality of stimuli were not bad enough, the ethologist is also faced with the same problem on the other side of the coin: not only are natural environments just packed with potential stimuli, but naturally behaving organisms do lots of things. Animals rarely perform only a single behavior at a time. A variety of interpretations can be placed on a given behavior. Distinguishing between intentional and accidental actions can also be difficult. Did that fish rise six inches by the action of its swim-bladder or was it moved by an upwelling current? Careful experimentation can help narrow the hypotheses down, but in doing so one encounters the Ethologist's Dilemma: the more control an experimenter exercises over the stimuli and behavior of an organism, the less natural and biologically normal such stimulation and behavior becomes. Thus, the experimental ethologist must be careful not to undermine the very naturalness that motivates this approach in the first place.

Again, one should not conclude from such ambiguities and difficulties that ethology is pointless or irrelevant. As with physiology, ethology cannot by expected to answer content a

Abstract