Visible and Invisible Worlds

Recent writing about perception by neuroscientists and philosophers has tended toward a disconcerting message: we have nothing like the simple, direct contact with the world around us that we might suppose. Instead, we are told, our brains actively synthesize a picture of the world, continually guessing, extrapolating, and projecting. Stronger versions of this view hold that what we perceive is a kind of simulation or model—not one imposed on us by some malevolent being but one we fashion ourselves. The simulation is constrained by physical stimuli from the environment—from something outside us, anyway—but the constraint can be tenuous, and ordinary perception may be akin to a “controlled hallucination,” as the neuroscientist Anil Seth has argued.

Against this background, it’s interesting to read two recent books by science writers—Sentient by Jackie Higgins and An Immense World by Ed Yong—that describe, among other things, the sometimes astounding detail with which our senses mediate our contact with the world. The senses of many animals, including ourselves, could hardly be more finely tuned to what goes on around us.

Decades ago scientists found that, in some circumstances, human eyes can detect a mere handful of photons, the basic units of light. More recent work seems to show that in laboratory settings we can respond to just a single photon, though there is some controversy over this finding. It’s not that each photon is seen as a tiny flash, but we can make judgments at a better-than-chance level about when a photon has reached our eye. Our visual system is operating around the absolute limit that physics allows.

Other species are similarly sensitive according to their lifestyles and needs. Higgins, noting that some birds respond to magnetic fields when they navigate, writes that although the Earth’s own magnetic field is quite weak, a bird’s compass “can respond to forces that are one fifty-thousandth of the natural magnetic field.” One researcher told her, “The levels are substantially below anything previously thought to be biophysically plausible.” Male silk moths can track pheromones in the air at a level of one or two parts per quadrillion.

Yong discusses how crickets and spiders both detect air currents, and hence movement, with tiny hairs. These are so sensitive that they can be deflected by a fraction of the amount of energy in a single photon. This doesn’t mean that the hairs are used to see, as it’s wind that makes them move, but that they are more sensitive than any system that could be used to see. “Put another way,” Yong writes, “it would be almost impossible to make these hairs more sensitive without breaking the laws of physics.” And onward: sharks can sense electric fields, and one species of hammerhead can detect a field with a strength of a billionth of a volt across a centimeter of water.

On the one hand, perception is said to be controlled hallucination; on the other, we find astounding sensitivity in animals to what is around them. There is not an outright contradiction between the two views. The people who think we are perceiving a model or simulation do say that these simulations are constrained by stimuli from outside. They might now add that the models we experience are constrained in very precise ways by these influences. (One can imagine their also saying that perception in more complex animals like us differs from perception in insects, spiders, and sharks, but this is not the usual path taken; whether the machinery is simpler or more complex, sensing animals of different kinds are seen as doing roughly the same sort of thing.)

But there does seem to be at least some incongruity here. Perhaps a better overall picture will recognize the active, constructive nature of perception without cutting us off from the objects around us. While our brains do not simply mirror the world, animals—nonhuman and human—are exquisitely embedded, suspended, in nature’s energies.

Both Higgins’s and Yong’s books are organized around a wide range of nonhuman species and their extraordinary senses. In each, we spend a good deal of time with the mantis shrimp, which has exceptionally complex eyes, and the star-nosed mole, which has a flower-like appendage on its face that is prodigiously sensitive to touch. The material overlaps, with Yong’s book more encyclopedic, crammed with fact after fact, and Higgins’s more lyrical. Higgins is also mindful of some underappreciated senses (balance, direction), while Yong’s focus is more on vision, hearing, and other major interfaces with the external world, along with what he calls “the unwanted sense,” pain.

Humans are more accomplished in sensing than might be expected. Primates have excellent vision; only birds of prey have more acute eyes. Many Western philosophers have disparaged our sense of smell: Plato claimed that “the varieties of smell have no name, and they have not many, or definite and simple kinds,” and Kant said not only that this sense is the most dispensable but that “it does not pay to cultivate it or to refine it at all.” Perhaps it is true that smell is more dispensable, at least in comparison to vision, hearing, and touch, but as Covid-19 showed, losing our sense of smell leaves us profoundly unmoored from the world.¹ And the idea that humans are deficient in this sense is not true. A chemical known as TCA is the main cause of “cork taint” in wines—a musty, baggy smell. Some people have the ability to detect TCA at levels of ten parts per trillion—less than one drop in an Olympic-size swimming pool. Lest we become too impressed with our prowess, this is still about 10,000 times less acute than the pheromone-tracking silk moths.

Higgins and Yong, immersed in the details of animal life, are not greatly concerned with abstract questions about the mind’s contact with the world—with the significant exception of Yong’s enthusiasm for the Umwelt, a concept introduced by the Baltic-German biologist Jakob von Uexküll in the early twentieth century. Uexküll did a fairly wide range of biological work with a strongly philosophical orientation. His most famous book, published in 1934, is A Foray into the Worlds of Animals and Humans.² This is another animal-senses book, a precursor in some ways to the books of Higgins and Yong.

Umwelt can be translated as “around-world” but might be better rendered as “self-surrounding world” or “self-world.” It does not refer to an animal’s physical surroundings, for which Uexküll used another word (Umgebung). An animal’s Umwelt is the world it senses and acts on, the world it encounters and deals with. Nothing else exists in that animal’s Umwelt. In Foray, Uexküll described an Umwelt as a sealed unit and pictured the animals around us as “enclosed within soap bubbles.”

Uexküll’s concept has influenced a wide range of philosophers and biologists. It was commended by Martin Heidegger and Maurice Merleau-Ponty, and it is not rare to encounter invocations of the Umwelt in zoological articles today. This influence has not so far been affected too much by the political side of Uexküll’s life. A conservative German nationalist, he did not join the Nazi Party, as Heidegger did, but he supported Hitler’s rise and had ties to the racial and antisemitic theoretician Houston Chamberlain. A recent book, Uexküll’s Surroundings: Umwelt Theory and Right-Wing Thought by Gottfried Schnödl and Florian Sprenger,³ has argued that his engagements with right-wing movements and the Nazis were quite a bit more extensive than had been supposed. Schnödl and Sprenger aim to correct the impression of Uexküll as an “upstanding and unsuspecting conservative aristocrat,” an impression encouraged by the posthumous biography his widow, Gudrun von Uexküll, wrote.

Uexküll was strongly influenced by Kant and wanted to extend the philosopher’s insights into biology. Kant recognized both a “phenomenal world” that we can encounter and know but that is partly a product of our own concepts and faculties, and—more elusively—a “noumenal world” of things in themselves, a sort of unknowable beyond. Kant’s was not a simple form of idealism, but Uexküll’s own version ended up in a stark and simple form: “All reality is subjective appearance. This must constitute the great, fundamental admission even of biology.”

Uexküll’s biological application of idealism did take things in novel directions. Ordinary action—doing things that affect one’s environment—has often been sidelined in Western philosophical thought about the mind and knowledge. But from a biological point of view, especially if one is interested in animals, the importance of action can’t be overlooked. Uexküll, crucially, recognized the reciprocal or two-way relationship between sensing and action. What you sense affects how you act, and what you do in turn affects what you sense. Uexküll saw that a theory of sense perception needs more than just stimuli coming in from who knows where; a picture of that kind does not fit with the continual ways in which action affects what is sensed—from acts as trivial as a turn of the head to those as consequential as building a nest. These cycles connecting sense and action form the soap bubbles, or invisible worlds, of Uexküll’s Foray.

The details of the Umwelt do raise puzzles. Is an animal’s Umwelt made up only of things the animal can both perceive and act on, or does it contain all that can be perceived plus all that can be acted on, collected together? A distant star can be seen but not acted on; a tiny speck of dust can be acted on but not seen. In mathematical terms, is it the intersection or the union of the two sets? It seems generally to be the two collected together, the union, that Uexküll has in mind. But both options have problems.

If action is its own source of objects in the Umwelt, then the bubble must extend beyond anything that might be sensed by that organism: our actions have effects, especially indirect ones, that we don’t and can’t perceive. If the bubble is defined by what we can both act on and perceive, then it gets the nature of sensing wrong. Sensing can be fed by one’s own actions, but it’s also open to other things going on. Some of what we sense really does come from “out of the blue.”

Uexküll’s picture is designed to make sense of the perspectives of individual animals. It runs into difficulties when we start to think about many animals interacting at once, as we do in evolutionary biology or ecology. Uexküll was an opponent of Darwinism, which he saw as a mechanistic view that failed to recognize the plans and purposes that govern nature. But even if we set aside Darwinian evolution, the understanding of the world given in ecology is also one in which animal worlds are not at all sealed off from one another. Here Uexküll tried to have things both ways: he noted that the lives of different animals intersect and also insisted that each animal still lives within its own circle, its own world, “in complete isolation.”

But what does isolation mean here? Each animal will perceive things differently, detecting and reacting only to a small sliver of what is going on around it, but it does this within a single system, a single scene. Uexküll thought Kantian philosophy had undermined the idea of a single world common to us all, a world that we each perceive in our own particular way but all then act on, in concert. He was trying to give us a biology that did not locate life within such a shared world. But especially when we think about life ecologically—and, in fact, even before we do that—such a world forces itself back upon us.

Yong introduces Uexküll and the Umwelt immediately and uses the idea all through his book; as we learn what each animal responds to, we learn about its Umwelt. (Higgins invokes the Umwelt, too, but only in her final pages.) I do not suggest that Uexküll’s political views infiltrate Yong’s argument. I’ve never seen a strong connection between the Umwelt concept and Uexküll’s politics, though the book by Schnödl and Sprenger does make intriguing links, finding in his biology “an identitarian logic in which everything should stay in its place and nothing should mix.” My problem with the Umwelt is with how it portrays the lives of animals.

Yong does not endorse the idealist flavor of Uexküll’s thinking. His title, An Immense World, even pushes in the other direction—a single immense world is what Uexküll wanted to lead us away from. But what then is left of the Umwelt? Yong says he sees the idea as expanding our view rather than locking us in: “It tells us that all is not as it seems and that everything we experience is but a filtered version of everything that we could experience.” This idea of a world largely beyond our ken that we act on along with the other animals around us is in a way the opposite of Uexküll’s vision; it is an anti-Umwelt. It is not, as in Uexküll, a biological version of a perennially alluring, solipsistic picture. Leaving the Umwelt behind, something Yong seems reluctant to do, is progress.

The books by Higgins and Yong are both about our contact with the here and now, with what’s happening in front of us and how we register it. This contrasts with another side of our mental life, the realm of memory, dreams, and imagination—these are sometimes now described together as “offline” cognition.

With the exception of the more practical aspects of memory, this side of the mind has often seemed a bit of an extravagance. It is part of what makes human experience rich and valuable, but appears far removed from the main business of guiding action with the aid of the senses. It does not seem at all essential to getting by as an animal. Yet many recent findings in biology and neuroscience suggest, somewhat surprisingly, that nonhuman animals have a lot of this sort of thing going on.

David Peña-Guzmán’s When Animals Dream is about what might seem to be the most exotic form of offline cognition. He argues that dreaming is a part of the inner lives of at least some animals, and perhaps a wide range of them. As he says, if this is true then it bears directly on debates about animal consciousness (as dreaming is a kind of conscious state) and hence on ethical issues around animal rights and welfare.

In an early chapter Peña-Guzmán gives a forthright exposition of the scientific evidence for dreamlike phenomena in birds, chimps, cats, cuttlefish, and others. The data here are striking; what goes on in these animals is remarkable even if you are not convinced that the episodes are felt as dreams.

What does the evidence look like, and how could we learn about something as elusive as an animal dream? Some say animal dreams will always remain a matter of mere speculation because of the impossibility of a verbal report. But a lot of research into dreaming in humans does not rely on report, drawing instead on brain activity along with dream-enacting behaviors. When we sleep, especially during the REM (rapid eye movement) phase that is most associated with dreaming, many of our muscles enter a state of paralysis or “atonia,” ensuring that we don’t physically act in response to our dreams. But various disorders of sleep, mild or serious, include a breakdown of this paralysis, resulting sometimes in violent behaviors during sleep.

Many of us have seen what look like dream-enacting behaviors in cats and dogs, when they make semisuppressed running motions and the like. The French neuroscientist Michel Jouvet used surgery to interfere with sleep paralysis in some domestic cats in experiments in the 1950s and 1960s. The result was the unleashing of a range of elaborate behaviors while the cats slept: “Some of them stared intently into empty space as if stalking prey, ready to pounce, while others ran around their enclosures energetically fighting imaginary enemies like little furry Don Quixotes.”

Peña-Guzmán’s book opens with an observation that is similar, in some ways, but involves a more exotic animal. An Octopus cyanea living with the biologist David Scheel, filmed during the Nature episode “Octopus: Making Contact,” was observed going through a mesmerizing series of color and body-pattern changes while asleep. The color-changing mechanisms in an octopus are controlled by the animal’s brain; in cephalopods, the animal’s whole skin is a window to the soul—or at least to the activity of the brain.

Many of the interpretations that people offered of this octopus’s sleep episode were quite narratively coherent: they suggested that the octopus dreamed it was engaged in a successful hunt or a similar activity. But as with human dreams, the dream of an octopus might be more chaotic than that. Scheel and his coauthors have suggested in a recent paper that octopuses and cuttlefish, despite their evolutionary distance from us, may provide valuable information about dreamlike states. In animals like us, muscle atonia during dream sleep keeps us from wild behavior. Damage to this function, as in the Jouvet experiments, reveals what is usually suppressed. In octopuses, color changes do not need to be suppressed as bodily motions do. This window into the dreaming brain of an octopus remains more open than it is in other animals.

Another body of research is based on measurement of brain activity itself and has been used to show the occurrence, especially in rats, of “replay” of various behaviors during sleep. This work relies on the existence of maplike arrays of neurons in the rat’s brain; particular cells fire when the animal takes itself to be in a certain place within an environment. Such maplike structures can be identified while a rat is moving around when awake, and rats have then been found to replay movement along particular paths, especially ones that lead to rewards, when they are asleep.

For Peña-Guzmán one of the things we need to understand is why people—including some of those responsible for the experimental results he discusses—do not just accept that animals dream. Researchers sometimes describe apparent dreamlike phenomena in animals, including the replay and rehearsal of behaviors during sleep, and then seem to search for language that enables them to avoid concluding that the animal is dreaming, talking of “algorithmic implementations” instead of experiences.

Peña-Guzmán is occasionally more impatient about this than I think is fair. Many writers surely just want to be cautious and are not sure we know what all this brain activity might connote. After describing one study that found that rats “generated an internal simulation that ‘re-activated’ or ‘re-constructed’ a waking behavior,” Peña-Guzmán writes, “Of course, to reconstruct a waking behavior during sleep simply is to dream about that behavior, so this amounts to saying that the rats were dreaming.” But that conclusion is not so definite if dreaming is taken to imply a kind of felt experience. We don’t know that all reconstructions of behaviors in sleep are associated with experiences of that kind.

Peña-Guzmán gives a general analysis of these situations. In cases where research seems to indicate dreaming but people resist that conclusion, this is because of a philosophical rather than a scientific disagreement:

At stake…is the question of the kinds of beings that rats are. Are they furry little computers that implement algorithms? Or are they conscious subjects with an inner phenomenology, subjects who perceive, feel, and think? This is not a question that can be answered on purely empirical grounds, which is why these researchers can agree about the facts yet disagree about what these facts ultimately mean. The crux of their disagreement is reflected in the terms they use to describe what they see: “algorithmic implementation” versus “internal simulation.” The first places replay [of behaviors in sleep] squarely within the ambit of computationalist theories of mind, whereas the second portrays it less as a program that the rat brain runs unconsciously and more as an experience that rats live through while asleep with the full thrust of their being.

Peña-Guzmán thinks that philosophical pictures drive the interpretation of scientific results, and he wants to establish a different picture than the one that most scientists have. Accordingly the book is a mix of careful argument and description of recent science, along with passages that have a deliberately arresting and sometimes poetic character—the “full thrust of their being” above is an example.

I found myself appreciating the push of Peña-Guzmán’s language toward his alternative vision, but I don’t agree that we are at a point where ordinary research has done all it can be asked to do and we just have to make a leap. To think that is to give up too quickly on the prospects for further scientific progress. I think we will probably work out what subjective experience is, in our brains and those of other animals, and dreams will fall into place.

The bet I’d make about how things will look then is along the same lines as Peña-Guzmán’s: a lot of animals dream. In fact, the list may grow beyond the cases he argues for. Peña-Guzmán does not discuss invertebrate animals, other than octopuses and cuttlefish. Bees, given their complex although miniature brains, are a natural case to consider next, and some hints of a “replay” of events during sleep, analogous to what is seen in rats and birds, have been found in bees, too.

Who, then, dreamed the first dream? When did evolution give rise to this unusual characteristic of animal life? If dreaming is widespread among animals, present in invertebrates as well as us, then there are two main possibilities. One is that dreaming has independently arisen several times in the history of animals; another is that it evolved just once, before the distant branching in the evolutionary “tree” that separates us from octopuses and bees.

The many-origins hypothesis seems more likely. The common ancestor of humans and octopuses (also of humans and bees) was probably a small worm-like creature living in the sea. It most likely had no eyes and a very simple nervous system, and was capable only of limited motion. What use could dreaming have for such a creature? On the other hand, an alternation between waking and sleeping is turning out to be extremely common in animals; something like it has even been observed in a jellyfish. Many animals, including bees, also have distinct phases in sleep, often with one phase that is “quiet” and one that is “active,” featuring brain activity that is akin in some ways to a wakeful state. In humans this is the distinction between “slow wave” and REM sleep. Bees have three phases of sleep; octopuses have two. Whenever an animal is in an active sleep phase, like REM sleep in us, it’s reasonable to wonder about dreaming.

These three books about the lives and minds of animals fall into a genre (along with Uexküll’s as an early member of the line, and some of my own). They not only chart the lives of nonhuman animals but try, at least cautiously, to get inside their point of view, to work out how things seem to them. Increasingly, books of this kind also expose a difficult relationship between our findings and our methods. The picture we’re getting is one of likely experiential richness in many animals; the means by which we get it include a lot of invasive neuroscientific work requiring surgery, implants, and dissection. The experiments done by Jouvet on dream-enacting behaviors in cats are a disturbing example, and Peña-Guzmán is very mindful of these issues.

When deciding what kinds of animal research should continue, we face the problem that we can’t neatly separate work likely to lead to practical benefits from work driven purely by curiosity. Scientific findings that are practically beneficial often appear unexpectedly and also build upon slowly accumulating masses of basic research. How should we move forward?

A reasonable response is to seek, at the least, to greatly scale down the use of invasive work on neurally complex animals such as rats, primates, octopuses, and others. Difficult as it is, we should try to achieve the next steps in research through methods that do not compromise the lives of the animals nearly as much, methods that rely on noninvasive scanning and observations of animals in naturalistic conditions who have not been subjected to surgical procedures, along with computer modeling and the like. Miniaturization of internal recording devices might one day give us more benign ways of tracking the details of brain activity. We need to work toward a resolution of the tensions between what we’ve been learning and how we’ve been learning it.