Roots of the NS&B course at Woods Hole*

by Alan Gelperin

*This article was originally published in the November 2006 newsletter of the International Society for Neuroethology

“Perhaps these insects are little machines in a deep sleep, but looking at their rigidly armored bodies, their staring eyes, and their mute performances, one cannot help at times wondering if there is anyone inside.”

Charles Otis Whitman on Oct. 10, 1908, in his pigeon cage feeding a hand-reared flicker taken by Whitman from a nest on a previous field trip.

Charles Otis Whitman on Oct. 10, 1908, in his pigeon cage feeding a hand-reared flicker taken by Whitman from a nest on a previous field trip.

This sentence concludes a remarkable paper published in 1964 by Vincent Dethier, in which he considers the evidence that the cognitive abilities of insects are equivalent to those of mammals (Dethier, 1964). Since that time, the comparative study of cognition has expanded considerably, particularly in the area of linguistics,tool use and social organization. For example,arousal and cognition are now studied in flies and bees.The neurochemistry of aggression has been dissected in crayfish and Drosophila. These recent advances were presaged by Dethier who took seriously the evolutionary prediction that elements of complex mammalian behaviors were to be found in other branches of the tree of life.It was within this framework, while a student in Dethier’s laboratory at the University of Pennsylvania, that I developed my own views of the heuristic value of a comparative approach to cognition, which would later find expression during the creation of the Neural Systems and Behavior (NS&B) course at the Marine BiologicalLaboratory (MBL) in Woods Hole, USA.
The birth of the NS&B course at the MBL is bound up with the evolution of other courses at the MBL and the evolution of the field of neuroethology in the 1960s and 1970s. It is also bound up with my own evolutionary trajectory as a combination of these general and personal intellectual antecedents led me to propose creation of the NS&B course in 1977. I therefore beg your indulgence for a short biographical journey.
As the Dean of the University of Kansas medical school welcomed me back to his office after a day of interviews at his medical school, he told me in quite cheery tones “I am going to admit you to make your own mistake”.When pressed for some amplification of this pithy statement,he added that he did not think me unfit for medical school but rather thought it a mistake to forsake my senior year of college to enter medical school after my junior year. With this comment he effectively saved me from a career choice that would have pleased my father but probably led to a life as a street person. Since I had gone to college with no high school diploma, leaving college with no college diploma and then finding medical school did not suit me, I would have been on the street with no credentials of any kind. Happily I took the Dean’s statement cum advice quite seriously and declined the offer of admission to the University of Kansas medical school. By the end of the ensuing summer, my second spent in full-time research in the laboratory of my college Biology professor, I knew quite firmly that research,not medicine, was the life for me.
Two encounters with eminent neuroethologists during my college years had a vital impact on my research trajectory.Vincent Dethier give a talk at Carleton and introduced me and the assembled students to the wonders of chemosensory science and its linkage to studies of feeding behavior in the blowfly Phormia regina. During my second summer of research at Carleton, our ecology professor led a cavalcade of students to the summer meeting of the Animal Behavior Society at Purdue University,where I was mesmerized by Kenneth Roeder and his lecture relating nerve cell activity to insect behavior,particularly during courtship and mating in the praying mantis. Who could escape being captivated by movies of a headless male mantis completing its mating behavior and insemination of a female mantis who had just dined on its head, thereby removing cephalic inhibition of the male mating motor program? The encounter with Vince Dethier led me to apply to the University of Pennsylvania for graduate study under the joint auspices of the Department of Biology and the Institute of Neurological Sciences. Upon completion of my doctoral work I became a postdoctoral fellow with Kenneth Roeder.
The Institute of Neurological Sciences at the University of Pennsylvania was one of the first neuroscience training programs that was truly interdisciplinary and interdepartmental,bringing together a group of legendary intellects united by a shared interest in brain science, mutual respect for the intellectual prowess of their colleagues and a social network of personal relationships which allowed cohesion to survive heated disagreements on matters of scientific interpretation. I internalized this model of how to think about problems from multiple perspectives and integrate analytical approaches at many levels, behavioral, cellular and biophysical, in attacking a particular phenomenon. This approach would also find expression in the construction of the NS&B.
My training at the University of Pennsylvania occurred in the early 1960s, during the flowering of data from multiple invertebrate model systems showing how bits of behavior could be understood in cellular terms, whether in crayfish swimming, mollusk feeding, leech swimming,cricket singing, fly vision, locust flying, honeybee communication,and many other situations in which the activity of single nerve cells could be tightly linked to behavioral acts or perceptual decisions. Even the cellular analysis of learning, my passion since college days, was beginning to yield some of its secrets in both mammalian hippocampus and molluscan ganglia. These events led to the emergence of the field of neuroethology, characterized by a focus on how cellular interactions in the nervous system account for species-typical behavior relevant to adaptation of an animal to its Umwelt or characteristic sensory world. These were heady days where in our hubris we wrote about “simple systems,”thinking that functional dissection of a nervous system containing a few thousand neurons would be “simple”compared with analysis of the mammalian brain. At this point it is not clear that even “simpler systems” is an accurate characterization, as we learn of the multiple functions carried out by different parts of a single neuron.We can confidently talk about “compact” nervous systems but we are wise enough now to avoid naïve term like “simple”.
My own first encounter with the idea that insects had many of the classes of behavior ordinarily thought of as strictly mammalian was during the weekly “feeding seminars” under the auspices of the Institute of Neurological Sciences at the University of Pennsylvania. A collection of local luminaries, such as Eliot Stellar, John Brobeck, Jim Sprague, Vince Dethier and Alan Epstein,would gather with graduate and postdoctoral students to share data and ideas on the control of feeding behavior.Vince and Alan Epstein had a particularly interesting set of exchanges over the course of many weeks during which Alan Epstein championed the view that what separated mammals from insects was the operation of a higher-order behavioral mechanism called motivation.Motivation was in some ways like pornography. It was hard to define but you knew it when you saw it. Alan Epstein would construct a definition of motivation designed to make clear the separation of insects and mammals. Vince Dethier would take this as a challenge to design experiments probing the feeding behavior of the blowfly Phormia to see whether evidence of motivated behavior could be found, and in due course return to the feeding seminar to present data showing that the latest version of the definition of motivation applied equally well to rats and Phormia (Dethier, 1966). This exchange went through several cycles, resulting in a series of insect studies on higher-order aspects of fly feeding behavior, such as central excitatory states set up by brief intense taste stimuli. As you can readily imagine,this set of interactions was extremely educational toa young graduate student still constructing the intellectual framework within which to understand how to optimally proceed with cellular analysis of higher-order categories of behavior (Gelperin et al., 2006).
Another strand in the tapestry that would become NS&B was the hubris of the “simple systems” approach to the cellular analysis of behavior, which flowered during the 1960s and 1970s. The demonstration that many invertebrates possessed sensory, motor and interneurons that could be repeatedly identified from animal to animal,coupled with the notion that having thousands of neurons rather than millions would make the complete analysis of behavioral control circuits practical, produced great enthusiasm for the enterprise of cellular circuit analysis. It seemed that if we could mobilize a sufficiently clever and determined army of neuroethologists armed with sharp microelectrodes and fluorescent dyes for intracellular injection, we would soon have complete cellular and circuit understanding of crayfish swimming,locust flight, leech swimming, lobster stomatogastric ganglion, slug feeding, honeybee navigation, fly vision,and sundry other circuit bytes and behavioral bits.Feeding this euphoria was the demonstration that certain interneurons, called command neurons in their early incarnation,seemed to be the sites of decision making as to whether a piece of behavior (e.g., crayfish tail movement,sea slug defensive swim, goldfish swim initiation)would be elicited by an epoch of relevant sensory input.Although modified by later analysis, the concept of the command neuron encouraged the view that intensive cellular analysis of selected behavioral control circuits could reveal general rules of circuit function of wide generality,including relevance to mammalian behavioral control systems.
The MBL in Woods Hole has a long tradition of work in evolutionary studies, animal behavior and cellular neurophysiology.The first director of the MBL, Charles Otis Whitman (1842-1910) had been a student of Louis Agassiz, whose admonition to “Study animals, not books” is prominently displayed at the MBL to this day.Whitman enjoyed natural history fieldwork, and had an uncanny ability to successfully rear a variety of delicate bird species, such as ring doves and passenger pigeons.
He is shown in Fig. 1 with a flicker he had hand reared in order to study its color pattern. In the last half of the20th century neurophysiological work at the MBL onelectrogenesis in the squid axon, basic aspects ofchemical synaptic transmission at the squid giant synapse,discovered by Ted Bullock and Susumu Hagiwaraat the MBL, among many other aspects of neuronal biophysics,made the summer neuroscience community atthe MBL extraordinarily stimulating and attractive to both students and established researchers in the field. StephenKuffler established a legendary Neurobiology course at the MBL that focused on cellular neuroscience,and provided a model for how to organize an intensive lecture and laboratory summer course that would attract both first-class faculty and students from around the world.
It was my great good fortune to start a relationship with the MBL in 1966, as a Grass Fellow in Neurophysiology.This summer as a Grass Fellow was tucked neatly between the completion of my postdoctoral study with Kenneth Roeder at Tufts University and the start of my academic career at Princeton University. This summer fellowship provided the intellectual equivalent of drinking from a fire hose. I learned much from my fellow Grass Fellows, particularly Bill Kristan, from attending lectures in the MBL summer courses, the Monday evening lecture series in neuronal biophysics (also known as the Monday night fights) and the fabled Friday evening lecture series. This was combined with access to a world class open-stack biomedical library, situated adjacent to Eel Pond, which allowed thorough and efficient exploration of the biomedical literature while listening to the gulls call and watching the sailboats swinging at anchor.This was literature consumption before the World Wide Web was invented and internet access to the biomedical literature became the norm. The combination of world-class science and the sea was intoxicating and addictive.
Imagine my surprise to be invited to teach the following summer in a new incarnation of the first course to be offered at the MBL in 1888, originally called Experimental Zoology. The course traditionally surveyed the structure and function of marine invertebrates representing the full range of invertebrate phyla. The laboratory component of the course revolved around the fruits of weekly field trips to diverse ecological domains to collect living creatures of every type and size and bring them to the laboratory for identification. The new version of this venerable course, to be called Experimental Invertebrate Zoology, would condense the phylogenetic survey into two weeks and use the other ten weeks for lectures and laboratory exercises in comparative physiology.Jim Case was the course director, and fellow faculty such as Michael Greenberg and Bob Josephson helped guide my initial forays into this new terrain. I was assigned the Echinoderms for my lecture contribution to the phylogenetic survey, which gave me new appreciation for the amazing bioengineering incorporated into these armored creatures. My experience in this course and its next iteration directed by Bob Josephson furthered my understanding of the potential for creative pedagogy offered by the summer course format at the MBL.
Michael Greenberg followed Bob Josephson as Directorof the Experimental Invertebrate Zoology course. As Greenberg’s tenure as course Director came to a close in 1977, I anticipated being considered as a candidatefor the next Director. Stimulated by this possibility I designed a new course that I thought would fit logically as a summer course offering, to complement the cellular Neurobiology course and bridge the gap between cellular neurobiology and behavior. The outline for the NS&B course was thus in my mind when the Director of the MBL, Paul Gross, called me to his office. As I anticipated,he offered me the Directorship of the Experimental Invertebrate Zoology course. I countered with my proposal for a new course, NS&B, with an explanation as to why the new course would fit naturally with the existing Neurobiology course, my initial suggestions forcourse faculty, and the nature of the laboratory exercisesthe suggested faculty would implement. With remarkableprescience and alacrity, Paul Gross agreed to my proposal and marshaled the needed resources to beginrecruiting faculty for the new course. Then a miraclehappened. Each and every one of the potential faculty Icalled agreed to join me in this new venture. The siren call of the neurobiology community at the MBL and theprospect of teaching a group of extraordinarily talented students selected from an international pool of candidatesproved irresistible. It was also an auspicious timein the evolution of work in cellular and systems neurobiology– the field was growing, the future looked bright,grant funds were available and enthusiasm was high. If Ihad not invented NS&B, someone else would have, as itwas a logical next step in the development of the disciplineof neuroethology.
The first year of NS&B was a heady and hectic affair.Course lectures were given by James Gould, AdKalmijn, Ron Hoy, David Prior, John Nicholls, Bill Kristan,Alan Gelperin, Randolf Menzel, Tom Eisner andFernando Nottebohm. It is left as an exercise for thereader to find these individuals here [link to http://www.mbl.edu/nsb/about/class-pictures/]. In addition tothese regular course lectures at 8:00 AM, NS&B sponsoreda Wednesday evening lecture series, which featured lectures by George Gerstein, Robert Capranica, William Quinn, Eric Kandel, Tom Eisner and Larry Cohen during our first iteration of NS&B. Further intellectual seasoning was provided by Special Lectures from Michael Bennett, Donald Griffin, Eduardo Macagno, John Arnold, who demonstrated an orgy of squid mating,and Gunther Stent. We had a closet full of canaries and boxes and hives full of invertebrate brain donors matching the many and varied interests and expertise of our course faculty. Our 8:00 AM lecture series also nucleated one neurobiological union whose F1 attended Carleton College, thus bringing the story full circle.
Two fields with significant overlap with neuroethology, namely comparative cognition and computational neuroethology, are now growing apace and cross-fertilizing neuroethology. There is a Comparative Cognition Society that will have its 14th annual international conference in Melbourne, Australia, on March 14-17, 2007. More generally, cognitive science as a field bridging psychology, linguistics, neuroscience and computer science is rapidly growing, aided and abetted by the application of functional magnetic resonance imaging techniques to the domain of brain computations occurring during cognitive tasks.
Computational neuroscience is another area of rapid growth, currently represented by a summer course at the MBL called Methods in Computational Neuroscience, in which I have enjoyed giving lectures on computational olfaction for the last several years. A subdivision of this area, computational neuroethology, seeks to meld cellular studies of neural interactions controlling behavior with mathematical models of the neural interactions to both understand the computation carried out by known circuit elements and clarify deficiencies in current understanding,particularly the roles of hierarchy and multiple feedback loops in behavioral control systems. An essential contribution of the neuroethological perspective is the constant focus on the natural stimuli the neural system is built to process and the need to analyze natural units of behavior with some understanding of the ecological niche to which the animal containing the circuit of interest is adapted. The use of recording methods in awake behaving animals while they perform computations involving the circuit being monitored is an increasingly common way to insure that the recorded cellular interactions are relevant to the normal operation of the circuit. This is not a new idea but recent work has involved many channels of simultaneous neural recording and new algorithmic approaches to interpreting multiunit activity.
I had completed planning for the second summer of the NS&B course when family circumstances in the spring of 1979 led me to relinquish the Directorship of the course and turn to my friend and course colleague Ron Hoy to take over the Directorship position. Ron wiselydecided to share the Directorship with EduardoMacagno. They jointly improved the course and put it on a firm foundation for growth and evolution into the future. It is with some satisfaction, perhaps even a bit of nachis, that I have observed the NS&B course mature and become one of the most highly regarded summer courses at the MBL, as judged by both student ratings of their experiences and ratings by the NIH panels that evaluate the periodic applications for student support. Will a summer course at the MBL in cognitive neuroscience be next?