Complex Worlds from Simpler Nervous Systems. Frederick R. Prete, ed. MIT Press, Cambridge, MA, 2004. 436 pp., illus. $40.00 (ISBN 0262661748 paper).
Not many years ago I gave a talk to an audience, consisting largely of engineers, on what the field of neuroethology had to offer to their efforts to design “biologically inspired” computer chips. I introduced them to what is arguably the best-understood part of any nervous system on this planet, the crustacean stomatogastric ganglion (STG). I told them we had a complete wiring diagram for its 30-odd neurons, could record simultaneously from up to eight of these cells to describe their circuit interactions, knew all of the neurotransmitters and most of the neuromodulators they used, had constructed detailed biophysical models of the individual neurons, and were only now beginning to figure out how this circuit actually worked. But the jaw-dropping moment came when I told them that this level of knowledge had required an investment of something on the order of 1000 person-years, and that the behavior the STG produces is movement of the animal's stomach. Even the simplest neural systems have turned out to be dauntingly complex.
Against this sobering background comes Complex Worlds from Simpler Nervous Systems. In this volume, Frederick Prete (of Visuo Technologies) has assembled a collection of papers that look at how “simpler” organisms (grant-speak for “not a bird or mammal”) construct their Umwelt—their self-world. We owe the word to Jakob von Uexküll, who emphasized that organisms construct their Umwelt through the interaction between their physical environment and their own behavior, sensory capabilities, and internal states. Prete's self-stated goal is to move away from the misconception that animals such as spiders, insects, and molluscs are simple reflex machines, and to appreciate the complex perceptual models they construct of their environments. While this is not a view that will surprise those who study the neural bases of behavior in these simpler systems, it is a case worth making. In particular, in an era of funding agencies focusing ever more tightly on a small number of model systems, it is good to be reminded of the advantages of diversity, and of curiosity-driven research.
After a typically delightful foreword by Mike Land, the book is organized into three sections: “Creating Visual Worlds: Using Abstract Representations and Algorithms” (four chapters), “Enhancing the Visual Basics: Using Color and Polarization” (five chapters), and “Out of Sight: Creating Extravisual Worlds”(two chapters). The reader will immediately note that this is very much a book about vision. This is not surprising, given Prete's research background in vision in mantises. However, it is unfortunate that there are no chapters on olfaction, particularly given the large number of active laboratories investigating problems in olfaction in nontraditional model systems, and the fact that so many animal behaviors are guided by olfaction rather than by vision.
Nonetheless, this is a highly readable and worthwhile book. Several chapters stand out both for the wonderful behaviors described and for their careful attention to detail. I was particularly impressed by Harland and Jackson's chapter on spider-hunting spiders of the genus Portia. These authors actually succeed in drawing the reader into the spider's Umwelt. Opening with descriptions of sophisticated and flexible hunting behavior that would be surprising enough coming from a primate, let alone an arthropod, they move on to a thorough description of the known sensory capabilities of these marvelous animals. They conclude with a laudable attempt at understanding how an organism integrates disparate sensory modalities into its own view of the world. This chapter alone is worth the price of the book, but I warn principal investigators that graduate students who read it will want to change their projects!
Equally impressive from the standpoint of cognitive abilities is visual pattern recognition and maze learning in honeybees, reviewed by Zhang and Srinivasan. These authors thoroughly review the excellent work that has come out of their own laboratory, but I was a little disappointed to find, in a chapter on cognition in bees, so little mention of olfactory learning, particularly when this is an area in which researchers are beginning to understand the cellular mechanisms involved.
Perhaps the most ambitious chapter in the book is Comer and Leung's attempt to understand the integration of multimodal inputs in the escape systems of insects. In large part because of the wealth of information on escape circuitry in crickets and cockroaches, this chapter offered the most complete description of how an animal uses its Umwelt to direct its behavior.
The chapters on vision in bees (Chittka and Wells), butterflies (Arikawa and colleagues), and mantis shrimps (Cronin and Marshall) are all excellent critical reviews of the current state of knowledge, and would be a superb introduction for workers new to these fields, or for those looking to catch up on recent findings. I was also gratified to learn about an animal communication system I had never encountered before: auditory signaling in bladder grasshoppers (van Staaden and colleagues). Each of these chapters contains numerous suggestions for important work that needs to be done (i.e., good thesis topics).
Unfortunately, I found the remaining chapters rather uneven. While Ewert's chapter on the visual world of frogs and toads was thorough and authoritative, it also seemed somewhat aimless at times. I suspect this is simply a case of trying to stuff too much of the several decades of beautiful work that has come from his lab into one small review. There was also an unfortunate lack of scholarship in Kral and Prete's chapter on vision in the praying mantis: it's difficult to understand how the authors could review mantis vision without discussing Samuel Rossel's work on binocular stereopsis. Although this appears to be a case of tit for tat (authors ignoring each other's work), it is a behavior that does not help the field.
While reading this book, I was frequently reminded of Ken Roeder's Nerve Cells and Insect Behavior (Cambridge, MA: Harvard University Press, 1963). This is high praise, as Roeder's book is the first I put into the hands of any student interested in neurobiology and behavior. Roeder emphasized that it is important to understand neurobiology from the perspective of the organism, and that important general principles are often first learned from relatively obscure organisms. Prete's book continues this tradition, and will be of interest to engineers looking for biological inspirations, to biologists looking into new fields, and to anyone who is interested in how amazing the behavior of even “simpler” animals can be.