Travels with Charlie
2014; The MIT Press; Volume: 26; Issue: 6 Linguagem: Inglês
10.1162/jocn_a_00627
ISSN1530-8898
Autores Tópico(s)Neuroscience, Education and Cognitive Function
ResumoCharlie Gross is a maverick of modern neuroscience. Never content to tread the straight and worn path, never bridled by accepted views and traditional approaches, Charlie has often veered off the tracks, mapped much new terrain, and repeatedly opened our eyes to new ways of thinking. His scientific contributions are prodigious, transformative, and sometimes—as in his discovery of “face cells” in the cerebral cortex—the stuff of legend.Charlie is also deeply loved by the generations of students and colleagues with whom he has worked. We love Charlie for his wit and wisdom; for the passionate joie de vivre that fills his personal and professional spheres; for the devotion he extends to his students, their work, and their lives; for a certain (often bizarre) unaffected goofiness and unpredictability; and for those seemingly stray provocative comments that tilt the frame of your world.On May 25 and 26, 2013, a great many of Charlie's former and current students, colleagues, and friends assembled in Princeton to honor him, to celebrate his contributions to science and society, and to express our gratitude to a man who has profoundly influenced our careers, our lives, and the way we think. “Charlie Fest” was both scientific symposium and party: We began Saturday with a series of scientific lectures in old Green Hall. This special volume of the Journal of Cognitive Neuroscience is largely a compendium of those presentations. Saturday evening consisted of a banquet at which Charlie was both praised and gently ridiculed by his students and colleagues. Sunday was appropriately marked by a celebration with traditional pig roast (more about that later) at Charlie's home.Much has been written about the age in which Charlie worked—five remarkable decades in which the field of neuroscience not only blossomed but resonated with a public eager to understand why we do the things we do—and about his life and contributions. Charlie's autobiography (“Being Charlie Gross”) appears in the Society for Neuroscience-sponsored collection known as The History of Neuroscience ( The engaging story of his Brooklyn youth, his family, and the unique factors that influenced his development as child of Jewish intellectual Communist Party members is told in “Wait: A Memoir of a Red Diaper Baby” (Boulevard, 2009). Charlie's historical impact on the field of neuroscience is also covered in his “Genealogy of the Grandmother Cell” (The Neuroscientist, 2002), “Single neuron studies of the inferior temporal cortex” (Neuropsychologia, 2007), and “Processing the Facial Image: A Brief History” (American Psychologist, 2005). The scientific articles in this special issue of the Journal of Cognitive Neuroscience reveal just a hint of the scientific world that Charlie has spawned.After a brief summary of my connection to Charlie and a sketch of major episodes in his career, to help set the stage, what I aim to do here is convey a sense of the man—that scruffy, shuffling, frenetic, boisterous, seriously intellectual, mischievous, inspired, ardent, radical, bon vivant provocateur. To convey a sense of what he has meant to us through the years and how he has helped make us who we are—not just as neuroscientists but also as people and members of society. At the same time, I can't help but note that these character manifestations of Charlie are precisely the reasons he has deeply impacted the field of neuroscience. Charlie is testament that we do what we are.I confess at the outset that this is a highly personal account. I have been student, colleague, and friend to Charlie for 35 years. He and I worked and played together intensely during my tenure in Princeton, and the stories that follow are largely derived from that era (the Golden Years, of course). It is naturally impossible for me to convey details of lab dynamics and personalities from the time after my departure. Nonetheless, because I have since remained close to Charlie and have witnessed the constancy of his unique personality, I am certain that those who came after could impart similar sentiments, insights, and stories.I joined Charlie's lab in 1979 as a graduate student in Princeton's “interdepartmental neuroscience program.” The lab when I arrived was largely male (that would quickly change) and best characterized visually as shaggy hirsute (defying the odds, even for the 1970s; see Figure 2), including, in addition to Charlie, Bob Desimone (having just received a Princeton PhD for his work with Charlie on the inferior temporal [IT] cortex, and very full of himself), Charlie Bruce (a gentle unassuming postdoc from North Carolina), and Ricardo Gattass (an earnest MD postdoc from the Federal University of Rio de Janeiro; a sweetheart and a true teddy bear of a man).Following four years that changed my life and worldview, four years in which I made lifelong friends (Figure 3), many from cultures different from my own narrow upbringing and with captivating stories to tell, four years in which I fell in love and married my first wife, Rina (and fell in love with her native India), four years in which I learned how the brain works and how to do science well, I received in 1983 a Princeton PhD in Psychology and Neuroscience and published a handful of papers describing work from Charlie's lab.Inertia and complacency are powerful forces, and I banked much energy by staying put to do a postdoctoral project in Charlie's lab. This is not advisable generally and even less so in today's highly competitive science marketplace, but in my case, it was a career bonanza: I was given a unique opportunity to retool Charlie's lab for studies in behaving animals and to carry out a research project (several, actually) of my own design, all with seemingly unlimited financial support, resources, and encouragement provided by Charlie. And so I embarked on another highly productive four years, during which I made many more new friends, traveled the world, ended my marriage, obtained my first grant, and found a job (not unrelated events, I think). In my memory, it seems that I saw little of Charlie during this time, as he had begun to explore China. I embraced the autonomy he bestowed on me, and he enjoyed the freedom. We nonetheless stayed connected, and I regularly updated him on the odd things I was cooking up in the lab.I often housesat for Charlie during his travels, dwelling with an elusive cat named Mishka, or sometimes with his kids Rowena or Derek, in the modest split-level house on quiet Woodside Lane. Somewhere in this era, Charlie decided to paint the interior of his house, which was a mess, to be frank, and he had the idea that painting it would distract me from my estranged wife. I had painted houses before and knew well the therapeutic power of a new coat of paint, so the idea (and the honorarium Charlie would provide) appealed to me. Charlie and I wandered off to the paint department at Sears in that 1970s New Jersey suburban marketplace monstrosity known as Quakerbridge Mall. We selected a neutral whitish color for most of the walls. I honestly can't recall why today—perhaps it was a relic from his hippie days in California or from his travels in India and China—but Charlie wanted the interior doors painted “kumquat” (that was really the name of the Sears paint color), which was a brash orange with brownish tint that is generally unsuitable for anything in large quantity. If Charlie had taught me anything, he taught me to think outside the box, so I went along with the plan. To add to the problem, however, the existing paint on the interior doors of Charlie's house was high-gloss black. Dark as night; go figure. It took at least three heavy coats of kumquat on both sides of each door to neutralize all that, and I can still picture today the kumquat circus-highlights one encountered at the entrance to Charlie's demure professorial study.At some point, I began to tire of Princeton. The town is famously small and provincial. Most importantly, although I believe that he would have supported me indefinitely, I needed to be something other than Charlie's student. In the fall of 1986, I obtained a job offer (one I could scarcely refuse) from The Salk Institute for Biological Studies, so I severed the cord and moved west. I have continued to collaborate with Charlie, we remain close, and through the years I have spent many hours exploring the world with him, both literally and figuratively.After graduation from Harvard, Charlie began his journey in neuroscience as a Fulbright scholar at Cambridge, where he engaged in neuropsychological studies of frontal lobe function under the supervision of Larry Weiskrantz, working in the tradition of Karl Lashley and Karl Pribram. As a postdoc in the 1960s, Charlie trained with Hans-Lukas Teuber in that cradle of modern cognitive neuroscience, the MIT Department of Psychology. After a brief turn as an assistant professor at his beloved Harvard (the nonelective departure from which would haunt Charlie for years), Charlie moved to Princeton, where he remains today. Throughout this period, he made game-changing contributions to our understanding of the neurobiological bases of memory, visual perception and cognition, motor control, and the functional organization of the cerebral cortex, in addition to shedding light on historical events that gave rise to our modern field of neuroscience.Charlie is perhaps known best for his work on the cellular basis of object recognition, which was inspired early by his introduction to Jerzy Konorski and the concept of the “gnostic unit.” While at MIT, Charlie adopted the powerful neurophysiological techniques developed and promoted by Barlow, Kuffler, Hubel, Wiesel, Mountcastle, and others. Rather than moving up the hierarchy from the sensory periphery, as his contemporaries had done, Charlie inserted his electrodes into the highest stage of visual processing, the IT cortex. One might have thought this as professional suicide, based on the reductionist argument that each processing stage can be understood only in the context of its inputs. But unlike other neurophysiologists of the day, most of whom were classically trained in medicine or physiology, Charlie had a holistic perspective informed by his roots in neuropsychology, from which he understood that one of the most important aspects of perceptual and cognitive experience is object recognition, and recognition is mediated by the temporal neocortex. Charlie's first neurophysiological experiments, which were carried out with some of his earliest colleagues—a fellow MIT postdoc named Peter Schiller, Harvard student Dave Bender, and a visiting scholar from Rio de Janeiro named Carlos Eduardo Rocha-Miranda (opening Charlie's lifelong door to Brazilian neuroscience and culture)—led to the monumental discovery of “face cells,” cells that appear to represent the most behaviorally meaningful class of visual stimuli.The world was apparently not fully prepared for face cells, for Charlie's discovery was derided—simply dismissed as impossible or a flawed conclusion derived from unsound methods—by many for much of the next decade. At the same time, however, a number of other groups became intrigued by the profound implications of Charlie's discovery and began to replicate the findings. One of my earliest adventures as a graduate student in Charlie's lab was an effort to precisely quantify (using new technologies for stimulus presentation and data acquisition), once and for all, the selectivity of IT neurons for complex objects, including faces. This effort was led by Bob Desimone, with whom I overlapped at Princeton in the late 1970s and early 1980s.I was still wet behind the ears, impressionable, and easily thrilled, but through this project, I experienced one of the most astonishing things I have seen in my neuroscience career: the robust, highly selective and readily reproducible responses of a visual cortical neuron to a face. And not just to one view of a face, but rather to a collection of specific face stimuli—different positions, orientations, angles of view—that a viewer would treat as perceptually or categorically identical. Naysayers, of course, maintain that one cannot know whether such responses reflect the true selectivity of a cell without presenting all possible stimuli (such as all of the component parts of a face). But for me, witnessing the phenomenon was a little like confronting a talking pig: It may defy belief and one might argue that it is merely a lucky coincidence of grunts that have no real meaning to the pig, but in the end there are no explanations that fit the data as well as language.After completing this quantitative analysis of the visual response properties of IT neurons, we (Charlie, Bob, Charlie Bruce, and I) submitted a manuscript describing the results to the newly established Journal of Neuroscience, for which Max Cowan then served as editor. The manuscript received favorable reviews, as I recall, but Max's ironic response—“Didn't we already know this about neurons in IT cortex?”—revealed how far the neuroscience community had come since Charlie's initial discovery. The paper (“Stimulus selective properties of inferior temporal neurons in the macaque”) was published in 1984 and remains one of the most highly cited works in Charlie's oeuvre.The second major epoch of Charlie's career addressed the functional organization of visual cortex. In part stemming from Charlie's successes and those of Hubel and Wiesel, coming from opposite ends of the cortical visual hierarchy, much work in the 1970s and 1980s focused on the “visual association” cortices that lay between those extremes. There was a small number of physiology labs doing this at the outset: Semir Zeki working in the Old World macaque and John Allman and Jon Kaas working in the New World owl monkey. In the late 1970s, Charlie entered the field, as did David Van Essen's group at Caltech. A series of studies appeared rapid-fire in the early 1980s, demonstrating multiple distinct visual areas—using criteria that included visual field topography, stimulus selectivities, and patterns of anatomical connections—in what had previously been known as Areas 18 and 19.At the 1981 meeting of the Society for Neuroscience, which was held in Los Angeles, Charlie's camp (Charlie, Bob Desimone, Ricardo Gattass, Leslie Ungerleider [then a research scientist in the NIMH Laboratory of Neuropsychology], and me) was invited to a pow-wow with David Van Essen's group (David, John Maunsell, and Bill Newsome) and John Allman's group (John and Steve Petersen) at the Athenaeum in Pasadena. (In my memory, Charlie and David could easily have passed for the odd couple transported to the elite halls of academia—Charlie was Oscar, naturally—and I learned that John Allman lived in a house full of monkeys.) During dinner, we compared notes cautiously and literally carved up the turf. Maunsell and I were doing twin PhD theses on the response properties of neurons in the middle temporal area (area MT), and it was reassuring to see that we had gotten similar results. In the end, mine was distinguished from his mainly by a focus on the columnar organization of directional selectivity, which I first reported publically at that same SfN meeting.For the next several years, the main areas of interest in Charlie's lab were physiological, anatomical, and lesion studies of the multiplicity of cortical visual areas and their functional contributions to perception. I continued to study area MT (it is now surely the second most well-studied piece of the primate cerebral cortex; the first being V1), later in collaboration with Hillary Rodman (an enigmatic graduate student who had arrived from Yale). Ricardo Gattass, Aglai de Sousa (another happy visitor from Rio), and Ellen Covey (a postdoc from Duke who had previously studied taste cortex with Robert Erickson) were mapping RFs in the far hinterlands of occipital-parietal cortex and tracing connectivity in collaboration with Carol Colby (a postdoc who had just completed her PhD in Peter Schiller's lab at MIT), Sue Fenstemaker (a graduate student coming from Middlebury), Leslie Ungerleider, and Carl Olson (a first-rate neuroanatomist newly recruited to the Princeton faculty). Later in this era, we were joined by two new graduate students, Earl Miller and Jim Skelly, who continued to probe the functions of IT cortex.The third phase of Charlie's career began after I left Princeton in 1987, with the arrival of Michael Graziano. Michael had conducted an undergraduate thesis in Charlie's lab before joining the graduate program at MIT. He returned to Princeton to complete his PhD (remaining as a postdoc), whereupon he and Charlie, along with students Tirin Moore and Dylan Cooke, carried out a series of groundbreaking experiments that revealed the contributions of motor cortex to complex directed actions in personal space.As a backdrop to the last 20 years or so of operating his lab, and since then to the present, Charlie seriously pursued a longstanding interest in the history of neuroscience. He has now written numerous scholarly articles and two books that feature the players and transformative (some frankly bizarre) episodes in our evolving understanding of the brain. During my tenure at Princeton, I took the seminar course Charlie had developed on the history of neuroscience. Fleshed and animated vividly by Charlie, the towering and quirky figures of the field populated my mind and left me with a rich appreciation—one I have carried through the years—not simply of the historical facts, but also of telling patterns and trends, which are all too often lost in the dust spun by a fast growing field.Charlie's two history books—Brain, Vision, Memory: Tales in the History of Neuroscience (1999) and A Hole in the Head: More Tales in the History of Neuroscience (2009)—are collections of compelling and deeply researched essays that are a matter of great pride for Charlie. Both books are also accessible and engaging enough to be suitable for the popular press. But Charlie went with MIT Press, which satisfied his intellectual's desire to be represented by the gold standard in academic publishing. MIT Press naturally expects books from intellectuals of Charlie's caliber to sell on their scholarly merit alone, without any marketing or entreaty to a popular audience. Most sell a few hundred copies, at best, regardless of their merits.Shortly after publication of the second book, Charlie was invited by my wife, Lisa Stefanacci (also a neuroscientist), to speak and sign books at the lovely atmospheric book shop she owned (The Book Works) in Del Mar, California. Charlie happily agreed (I'm not sure he'd ever done a book signing before), but the deck was steeply stacked against him, for the arrangement also included an appearance and book signing by Joyce the day before. Joyce naturally packed the house. She was eloquent, brilliant, and funny, and the signing line snaked outside and down the path long after her presentation. When Charlie took the stage a day later, the room was sparsely filled with a nonetheless eager audience (a few local physicians and clinical psychologists, a handful of UCSD faculty, coffee-house regulars, and some New Agers from the local beach community [this was, after all, Southern California]). I know Charlie to be a practical realist with a good sense of irony, but I have rarely seen him as dejected as he appeared when the short line ended and a tall stack of unsigned books remained on the table by his side. Science can seldom compete with a good novel on the open market, but Charlie's next book, we hope, will be delivered to a more inclusive publisher.Brain research often attracts outsiders with unusual perspectives. I think, by force of his own personality, Charlie has long been a magnet for quirky characters. During my tenure in Charlie's lab, we received occasional visits from a once esteemed senior neuroscientist, who by this time was wont to appear in robes and beads and spoke breathlessly of holograms in the brain. On more than one occasion, we were approached by otherwise decorous individuals who proposed experiments to explore the responses of IT neurons to pornography (a provocative but not entirely silly idea). For some time, Charlie and I worked closely with a student—someone for whom we both came to have great respect—who had the priceless habit of showing up for a gritty 36-hr experiment as though she had prepared for a fashion shoot. Charlie is fond of telling this latter story, I think, in part, because he was enthralled by her curious behavior, but also as commentary on my reaction to it. The truth is I think the experience held a mirror to my own slovenly appearance—ripped dirty misfitting jeans, faded t-shirt, unkempt hair, and several days of beard growth (Ted Adelson, who worked those years at RCA Sarnoff Labs in Princeton, once accused me of sporting the “Yasser Arafat look”; this long before extended stubble became fashionable)—and I was arguably better (cleaner, at least) for the self insight it gave me.One of the most interesting of eccentric characters in Charlie's circle was Eric Schwartz. Eric was a former Columbia particle physicist, who had been adopted by (equally eccentric) neurophysiologist E. Roy John at NYU. Eric came to us with a theory (they all come to us with a theory…) about the coding of visual patterns by IT neurons. There was something distinctly compelling about Eric's idea, and Eric himself was a trip, so we (Charlie, Eric, Bob, and I) began a collaboration in which Eric (coming down from New York) and Bob (returning from his new position as a research scientist in the NIMH Laboratory of Neuropsychology) would converge on Princeton every couple of weeks for a two-day recording experiment. Eric was loquacious and funny and thought about things differently from most people. He and Charlie clicked, whereas Bob and I actually did the experiment. The results were fabulous: The pattern of neuronal responses provided tentative support for Eric's hypothesis but, more broadly, they stood as the clearest evidence to date for position, size, and contrast-polarity invariance in cortical neurons. The whole experience was distinctly positive—the success of the study combined with the quirky intellectual banter and good food that we all shared.We considered follow-up studies but with the lack of proximity this never happened. I did eventually collaborate with Eric on some related experiments in his lab at old Bellevue Hospital on 1st Avenue in Manhattan. The lab was in an abandoned surgical ward that was only accessible by taking the elevator to the 8th floor and then climbing a creepy stair well to what appeared to be the 8th and ½ floor, where one confronted a small battered steel door with 14 locked deadbolts. On the other side was a magnificent 19th century art nouveau surgical suite that Eric shared as lab space with the aging Roy John. Somehow the fact that Eric worked (lurked) here was perfectly in character. I'm not sure that the hospital or the university (old Bellevue was by then operated by NYU Medical Center) even knew he was there or that the space existed.That Charlie not only attracted but also embraced these many odd and interesting characters speaks volumes about him. For Charlie himself is an outsider, albeit a highly credible one, and the creative path he has taken owes much to the different points of view he's been willing to consider through the years.Many adventures with Charlie have featured food, oftentimes as a central character in the plot, but nearly always part of the story in one way or another. I'm not sure that I thought much about it during my years in Charlie's lab—sharing food has long been to Charlie, I believe, a natural element of human social behavior and attachment, so I may have eventually taken it for granted. But a review of photographs from those years reinforces a (frequently comedic) view in which food was the ever-present thread that knit together the social fabric of Charlie's lab.The profound importance of food bonding for science and for life was initially made clear to me when I first met Charlie, in the winter of 1979. I had just been accepted to the graduate program at Princeton and I had driven from my home in Maryland—in a raging blizzard, no less—for an interview with Charlie. I arrived in time to eat and experienced the lunchtime ritual that was to become a rich part of my life for the next several years and which I later incorporated in my own lab.The ritual began, as it did in those days, with calls down the hall for “lunch!” and the Portuguese “vamos almoçar!” (“let's eat lunch!”). After a designee returned with sandwiches and such from Davidson's Market (just across Nassau Street), all gathered in a circle in Charlie's spacious office, or in warmer months at picnic tables in a small grove of trees behind Green Hall. The conversation was bright and lively and ranged from politics to a critique of the latest art film, to the merits of a new Indian restaurant that had opened up on Route 27, to gossipy discussions of graduate student sex or the lazy know nothing faculty member down the hall. Laughter was frequent and unrestrained, Charlie was boisterous and satirical—occasionally waxing intellectual on subjects like Palestine, AIDS, and scientific misconduct—Bob affectionately mocking, often regaling us with bits from last night's Johnny Carson monologue, and Ricardo patiently listening with the amused sensibility of a Brazilian aristocrat (while at the same time peeling a grapefruit with astonishing finesse). Aglai, who could talk faster than all of us combined (even in English), offered sarcastic commentary on everything, often illustrated with off-color anecdotes. The air was communal and open. Absent were the hierarchies of traditional academia; everyone was a player.I had never experienced anything like this before. I came from a rather provincial background and traditional bland public education (we were taught to listen rather than to speak). Although I had worked for some time in a lab while an undergraduate at the University of Maryland, I generally ate lunch alone at my desk. Even under the strain of my Princeton interview and frazzled by a long drive in the snow, I was captivated by this collective lunch, with its patent esprit de corps, and therapeutic laughter. It would be years before I would have the opportunity to implement communal lunch in my own lab, but I knew immediately that this egalitarian social eating with colleagues and coworkers, as practiced so well by Charlie and his clan, was hugely important for building the mutual trust, confidence, and respect needed to collaborate on hard work.Another interesting thing about lab lunch was the opportunity to see what other people ate. I had grown up in a uniformly white Protestant suburb of Washington with very limited exposure to different varieties of food. My mother prepared traditional southern cooking—she was quite good at it—but that was pretty much all she knew (and thus all I ate). By the time I made it to Princeton, I barely knew what a bagel was and Chinese food came out of a can (“Chun King Chicken Chow Mein”). At Charlie's lab lunch, it was commonplace for lab members to interrogate your meal—all in good spirit and with honest curiosity, but I was initially intimidated by the questions I faced from Charlie and Bob about my chicken salad sandwich. At the same time, of course, it was an opportunity to learn. I learned early on about yogurt, which I had never eaten before Princeton. Charlie, who seemed different from me along virtually every dimension I could think of and for whom I had naturally developed an obsessed fascination, ate yogurt for lunch nearly every day, commonly in large-tub quantities. (Charlie had no qualms about eating meat [or anything else, for that matter], but I rarely saw him do so at lunch, except for his pointed consumption of roast beef after surgery.) At some point I also began to eat yogurt. Initially not in the big tubs, like Charlie, but rather in those tiny Dannon containers where yogurt came smothered with sticky sweet jam. With time I made tentative efforts to eat it as Charlie did, plain or complemented with fresh berries and chopped fruit. Soon enough my lunch consisted of nothing but yogurt and fruit, often in massive quantities, and I have maintained this habit for over 30 years (Figure 4), as has Charlie. I like to think that I developed this pattern because it was rational, because it was healthy and inexpensive, but the truth is I was always modeling Charlie and, in doing so, trying to impress my lunch companions.Dinners in those early days were also often consumed in the lab during long experiments. A staple for Princeton students and postdocs was Hoagie Haven (“Hoagie Heaven”), a few blocks north on Nassau Street. It seemed that Bob, Charlie Bruce, and I lived on 12-in. “cheese steak” and “meatball” hoagies for weeks at a time during 1979–1981. Dinner in the lab became more interesting (or challenging) when Charlie joined us, as he often did when we were working with out-of-town collaborators like Leslie or Eric Schwartz. Those dinners acquired a bizarre quality, in that Charlie was always angling for spicier food (generally Indian or Chinese) and we became extremely competitive about our ability to tolerate the spice. Charlie the omnivore had traveled in India just before my joining the lab and was enchanted by Indian cuisine. I, on the other hand, was courting a real Indian girl, which gave me a leg up on Charlie the capsaicin dilettante. I was planning an extended trip to India with my future bride to visit her family and wasn't sure what food I would face, only that it would be very hot and I would be compelled to eat everything. So I went into training, in which I regularly ate “mircha” (Punjabi for intensely
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