A Hole in the Head
Page 20
ALTMAN’S REFLECTIONS
As this book was going to press at the end of 2008 I received a lengthy “in press” typescript from Joseph Altman entitled “The discovery of adult mammalian neurogenesis.”51 Altman wrote:
. . . my recollection is that [my early publications] were not ignored at all but created considerable publicity . . . with the generous financial support that we were receiving . . . we were able to pursue our research goals and disseminate the data. . . . But then things started to change in the late 1960s, although it took me several more years to realize that something was amiss. The first wake-up call came when I was supposed to be granted tenure at MIT and my promotion was denied. . . . I now know that there was a concerted attempt by some influential members of the neuroscientific community to marginalize us, but at the time I did not pay much attention to it. . . . This neglect of our work continued during the 1980s. . . .
I am not aware of any public criticism or rebuttal of the data we have presented. . . . Instead of open criticism, there appears to have been a clandestine effort by a group of influential neuroscientists to suppress the evidence we have presented and, later on, to silence us altogether by closing down our laboratory. I make this accusation for the following reasons: (a) by the early 1980s we were starting to have difficulties in getting our grant applications approved; (b) by the mid-1980s we lost all our grant support; and (c) by the early 1990s we had several of our submitted papers outright rejected. . . . In fact, we have never since been able to get our grant applications approved, not even when the topic of our research shifted from adult neurogenesis to the comprehensive embryological study of CNS development in rats and, later, in humans.52
Under these conditions how did Altman’s “laboratory survive, indeed prosper, without research grants and . . . remain productive while facing peer indifference and outright hostility?” One explanation Altman gives was that he had accumulated a “large collection of processed brains . . . [and could] analyze . . . [them] . . . and, instead of submitting papers to mainstream journals (a costly and painful enterprise) . . . started to summarize . . . results in books that also yielded some royalty.” He continues:
But there was also a psychological factor: namely, that I was well prepared by my earlier life experiences not to be discouraged by public indifference and hostility. When I committed myself to the study of brain-behavior relationships as a teenager . . . I was barred from finishing my formal education in quasi-fascist Hungary because I belonged to a disenfranchised religious/ethnic minority. When the Wehrmacht occupied Hungary, I was incarcerated in a forced-labor camp and worked on a railroad gang. After some time there, I escaped and lived clandestinely in Budapest, which very soon came under siege. My survival was aided, I tend to believe, by a syndrome that I developed, what I call “aparanoia.” Blissfully neglecting the fact that they were after my kind, I did not hide but walked with head erect through the streets, past bayoneted soldiers and gendarmes looking for Jews and deserters. I convinced myself that I was going to survive no matter what the Nazis’ intentions were. When the Red Army liberated us in 1945, I resumed my formal education. However, I could not tolerate the rising Communist dictatorship and fled the country in 1946. I became a stateless, displaced person in West Germany, waiting there for many years before I could secure the requisite documents to migrate to Australia. . . . I was able to attend lectures and seminars at a prominent German university and spent endless hours in its library. I continued informally with my education in Australia, where I worked through the first half of the 1950s as a college librarian.
Altman then came to the United States in 1955 and, after pre-and postdoctoral training in New York City, went to MIT.
NOTES
Some of the material in this chapter was published previously, in Nature Reviews Neuroscience (1: 67–73 [2000], “Neurogenesis in the adult brain: Death of a dogma”) and in Experimental Brain Research (192: 321–334 [2009], “Three before their time”). The postscript has been added for this volume.
1. Ramón y Cajal, 1928; Rakic, 1985a; Jacobson, 1970.
2. Koelliker, 1896; His, 1904; Ramón y Cajal, 1999; Gross, 2000a.
3. Ramón y Cajal, 1928, 1999.
4. Ramón y Cajal, 1928.
5. Gross, 2000a.
6. Ramón y Cajal, 1928.
7. Sidman et al., 1959.
8. Altman, 1962, 1963, 1967, 1969; Altman and Das, 1965, 1966a, 1966b.
9. Altman, 1963.
10. Altman, 1967.
11. Jacobson, 1970.
12. E.g., Altman and Bayer, 1995, 1996; Bayer and Altman, 2007.
13. Kaplan and Hinds, 1977; Kaplan, 1984.
14. Kaplan, 1981; Altman, 1963; Altman and Das, 1966b.
15. Kaplan, 1983, 1985.
16. Kaplan, 2001.
17. Rakic, 1985a, 1985b.
18. Rakic, 1985a, 1985b.
19. Eckenhoff and Rakic, 1988.
20. Boss et al., 1985; Kuhn et al., 1996.
21. Eckenhoff and Rakic, 1988.
22. Rakic, 1985a.
23. Gross, 1993a, 1993b.
24. Nottebohm, 1985, 1989.
25. Goldman and Nottebohm, 1983.
26. Burd and Nottebohm, 1985.
27. Paton and Nottebohm, 1984.
28. Nottebohm, 1996; Barnea and Nottebohm, 1994, 1996; Kirn and Nottebohm, 1993.
29. Stanfield and Trice, 1988.
30. Nowakowski et al., 1989.
31. Scholzen and Gerdes, 2000.
32. Mullen et al., 1992; Deloulme et al., 1996; Sensenbrenner, Lucas, and Deloulme, 1997.
33. Perera, Park, and Nemirovskaya, 2008.
34. Perera, Park, and Nemirovskaya, 2008; Cameron et al., 1993; Seki and Arai, 1999; Abrous, Koehl, and Le Moal, 2005; Eriksson et al., 1998; Gould et al., 1998, 1999a.
35. Cameron and Mackay, 2001.
36. Gould, 2006.
37. Altman, 1967.
38. Abrous, Koehl, and Le Moal, 2005; Leuner, Gould, and Shors, 2006.
39. Lois and Alvarez-Buylla, 1994; Corotto et al., 1994.
40. Curtis et al., 2007.
41. So et al., 2008; Mandairon et al., 2006.
42. Gould, 2007; Cameron and Dayer, 2008.
43. Gross, 1998a, chapter 3.
44. The positive ones include Gould et al., 1999b, 2001; Dayer et al., 2005; Bernier et al., 2002; Runyan et al., 2006; and the negative ones include Kornack and Rakic, 1999, and Bhardwaj et al., 2006. These and other positive and negative results are examined in Gould, 2007; and Cameron and Dayer, 2008.
45. Gould, 2007; Cameron and Dayer, 2008.
46. Other technical reasons why some studies have been unable to find new cortical neurons are discussed in Gould, 2007. For a discussion of the effect of different methods in assessing cortical neurogenesis, see www.princeton.edu/~goulde/protocols (accessed September 17, 2008).
47. E.g., Brecht et al., 2004; Shadlen et al., 1996.
48. Gould, 2007.
49. Altman, 1967.
50. E.g., Bruel-Jungerman et al., 2007; Anderson et al., 2007; and Shors, 2008.
51. This has now been published (Altman, 2009)
52. E.g., Altman and Bayer, 1995, 1996; Bayer and Altman, 2007.
11
DONALD R. GRIFFIN: ECHOLOCATION AND ANIMAL CONSCIOUSNESS
Most scientists seek—but never attain—two goals. The first is to discover something so new as to have been previously inconceivable. The second is to radically change the way the natural world is viewed. Don Griffin did both. He discovered (with Robert Galambos) a new and unique sensory world, echolocation, in which bats can perceive their surroundings by listening to echoes of ultrasonic sounds that they produce. In addition he brought the study of animal consciousness back from the limbo of forbidden topics to make it a central subject in the contemporary study of brain and behavior.
EARLY YEARS
Donald Redfield Griffin (1915–2003) was born in Southampton, New York, but spent his early childhood in an eighteenth-c
entury farmhouse in a rural area near Scarsdale, New York. His father, Henry Farrand Griffin, was a serious amateur historian and novelist who worked as a reporter and in advertising before retiring early to pursue his literary interests. His mother, Mary Whitney Redfield, read to him so much that his father feared for his ability to learn to read. His favorite books were Ernest Thompson Seton’s animal stories and the National Geographic’s Mammals of North America. An important scientific influence on the young Griffin was his uncle Alfred C. Redfield, a Harvard professor of biology who was also a birdwatcher, hunter, and one of the founders of the Woods Hole Oceanographic Institution.
Young Griffin’s boyhood hobbies were to become the central core of his professional interests and achievements. By the age of 12 Griffin was trapping and skinning small local mammals. Because of his poor teeth, his parents regularly took him to a Boston dentist. These trips were rewarded with visits to the Boston Museum of Natural History, where its librarian introduced him to scientific journals, and its curators to turning his trapped animals into study skins. At 15, with his uncle’s encouragement, he subscribed to the Journal of Mammalogy where he was to publish five papers before graduating from college. In his autobiographical writings, Griffin described his schooling as “extraordinarily irregular.” After he spent a few years at local private schools his “long-suffering” parents decided on home schooling. His father taught him English, history, Latin, and French. A former high school teacher handled the German and math. After a few years of trapping, skinning, sailing, and a couple of hours of daily lessons, his parents sent him to Phillips Andover, where he started but never finished the tenth and eleventh grades. The next year was spent at home again, collecting and sailing, and with tutoring adequate that he was admitted to Harvard College in the fall of 1934.
During these high school years Griffin seemed to be more of a nascent serious scientist than, say, Darwin, who had spent his undergraduate days hunting and collecting beetles rather than studying. For example, young Griffin thought he would be able to describe a new subspecies of California mice but then realized his hopes were based on errors in the literature, his first realization of the fragility of scientific fact. He tried to estimate the population of various hunted species by obtaining the number of animals killed from the state game authorities. He spent several weeks learning about bird-banding at a major banding station and was then authorized to set up a banding substation of his own near his home.
Soon he combined his interests in trapping small mammals and banding birds by banding bats. Recruiting friends, he banded tens of thousands of little brown bats, Myotis lucifugus (figure 11.1). (For the rest of his life he readily found research volunteers to help in such things as lugging heavy electronic equipment into the field, climbing into unexplored caverns, following birds in an airplane, building huts on remote sand spits, and navigating Amazon rivers in dugout canoes full of recording devices.) This bat-banding project resulted in finding that bats migrated between caves in Vermont and nurseries as far away as Cape Cod. Eventually it produced evidence of homing after displacement of more than 50 miles and of unsuspected longevity of these animals. It also yielded his first scientific publication, as a Harvard freshman, in 1934.1
Griffin’s sailing interests led to his second paper. While sailing in the summer before entering college, he had encountered several seal carcasses left by hunters who only wanted their noses for the bounty provided by the state. Little was known about what these animals ate, so he collected the contents of their stomachs and, with the help of several curators at Harvard’s Museum of Comparative Zoology, identified their contents. In one of his characteristically dry and self-effacing memoirs Griffin tells of how, many years later when he was chair of the Harvard biology department, some young discontented molecular biologist in the department sent him reprint requests for this paper in the names of several well-known molecular biologists. Griffin actually sent out the faded reprints until he realized it was a hoax.
UNDERGRADUATE YEARS
As an undergraduate biology major, Griffin took his first science courses but reported mediocre grades in everything but the courses on mammals or birds. At this time John Welsh was studying circadian rhythms in invertebrates and encouraged Griffin to do so in bats. This was an interesting problem because the bats hibernated for long periods under constant conditions in dark caves. Griffin brought some of his bats into the lab, and, using the standard physiological instrument of the time, the smoked-drum kymograph, he showed that indeed they had endogenous rhythms under constant conditions, yielding another paper in the Journal of Mammalogy.
Figure 11.1
Myotis lucifugus, the little brown bat, photographed in flight by H. E. Edgerton, from the frontispiece of Griffin’s Listening in the Dark (1958). Note the open mouth, presumably emitting high-frequency sounds.
Griffin knew Lazzaro Spallanzani’s (1729–1799) work on bat orientation. In a brilliant series of experiments with all the requisite controls, Spallanzani had demonstrated that bats do not require their eyes but do need their ears, to navigate. He speculated that, perhaps, the sound of the bats’ wings or body might be reflected from objects.2 Griffin also was familiar with the English physiologist Hartridge’s suggestion that bats might use sounds of high frequency to orientate. At this time a Harvard physics professor, G. W. Pierce, had just developed devices (the first of their kind) that could detect and produce high-frequency sounds above the human hearing range. Two fellow students, James Fisk (later president of Bell Labs) and Talbot Waterman (later a Yale zoology professor), suggested to Griffin that he take his bats to Pierce to find out whether they produced high-frequency sounds.
Pierce was quite enthusiastic about the idea. In fact he had been studying the ultrasonic sounds of insects (with the help of Vince Dethier, later the doyen of U.S. experimental entomologists). When they put the bat in front of Pierce’s parabolic ultrasonic detector, they observed that the bats were producing sounds that the humans could not hear, but when the animals were flying around the room no such sounds were detected. Nor did the production of high-frequency sound seem to have any effect on the flying bats’ ability to orient. When they published their observations, they suggested that the function of the supersonic sounds might be in social communication rather than orientation. (Later, Griffin realized that the detector had not been suffciently directional to pick up the bat signals in flight. Even later, the social communication role for certain bat ultrasonic cries was confirmed.)
When Griffin was a senior, he was in a quandary about applying to Harvard’s graduate school in biology because its faculty had little regard for Griffin’s current interest in bird navigation. “Wiser heads emphasized that if I really wanted to be a serious scientist I should put aside such childish interests and turn to some important subject like physiology.” The problem was solved with the announcement of the joint appointment of Karl Lashley to the Harvard psychology and biology departments. Lashley’s appointment had been the result of the command of Harvard’s president, James B. Conant, to hire “the best psychologist in the world.” Karl Lashley was the leading “physiological psychologist” of his time and the teacher of many subsequently famous students of brain function and behavior.3 His particular interest to Griffin was that he had written a long and authoritative historical and experimental paper on bird homing (with J. B. Watson, later the founder of behaviorism)4 and had carried out his own experiments on orientation in terns. Lashley took him on as a graduate student but encouraged him to take several courses in experimental psychology, which he did.
GRADUATE SCHOOL
In graduate school Griffin met another student, Robert Galambos (b. 1914), who was recording cochlear microphonics from guinea pigs under Hallowell Davis, a leading auditory physiologist at Harvard Medical School, and suggested Galambos look for bat cochlear microphonics in response to high-frequency sounds. They borrowed Pierce’s instruments, and Galambos was soon able to demonstrate responses of the bat ear to ultras
onic sounds. In a series of experiments Griffin and Galambos then showed that bats do indeed avoid obstacles by hearing the echoes of their cries. Here is a recent recollection by Galambos of these experiments:
Don divided a sound treated experimental room into equal parts by hanging a row of wires from the ceiling. We aimed the microphone of the Pierce device at this wire array, and began to count the number of times a bat flying through the wires will hit them when normal, or deaf or mute. . . . The impairments we produced [by plugging the ears or tying the mouth shut] were all reversible. . . . We also recorded the output of the Pierce device and correlated the bat’s vocal output as it approached the barrier with whether it hit or missed the wires. . . . Everything we predicted did happen. Nothing ever went wrong. We never disagreed. . . . We suspected our claims might be controversial and decided a movie demonstration might help silence the skeptics.5
(In recent years, the original movie has been increasingly shown on nature and science TV programs in many different countries around the world.)
Needless to say, the scientific community was very skeptical at first but the film and visits to their laboratory were soon convincing. As Griffin put it later, “Radar and sonar were still highly classified developments in military technology, and the notion that bats might do anything even remotely analogous to the latest triumphs of electronic engineering struck most people as not only implausible but emotionally repugnant.”