REMEMBRANCE

AND

COMMENTARY

Oscar Marin and the Creation of a Cognitive Neuropsychology Laboratory Michael I. Posner, PhD

Abstract: During the 1980s, the Cognitive Neuropsychology Laboratory at Good Samaritan Hospital, Portland, Oregon, made important strides in the study of brain injury. Created and headed by Oscar Marin and the author, in affiliation with the University of Oregon, the lab brought together students, fellows, and visiting experts in neurology, psychology, psychiatry, neuropsychology, neurobiology, neurophysiology, and computation. Their patient-focused collaborations produced groundbreaking research in language and its disorders, bradyphrenia, neglect, cerebellar function and impairment, and the psychology of music. The lab hosted the meeting that they documented in the influential 1985 book Attention and Performance XI: Mechanisms of Attention. The lab’s members have gone on to lead distinguished careers and continue making major contributions to cognitive neuroscience. Key Words: Oscar Marin, cognitive neuroscience, neuropsychology, language, attention (Cogn Behav Neurol 2015;28:129–133)

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he accent was Chilean, the physiognomy larger than life, and the enthusiasm for the topic infectious. It was 1979 at the Cornell Medical College in New York. The lecturer was Oscar Marin, MD, the topic the neurobiology of language. Here was a man of force, passion, and understanding. I was a Professor of Psychology at the University of Oregon, Eugene, Oregon. I was spending 6 months in New York at the invitation of Michael Gazzaniga, PhD, then Director of the Division of Cognitive Neuroscience at Cornell University Medical College, to explore links between neuroscience and cognition. Up until my New York stay, my work on attention had used mainly

Michael I. Posner is Professor Emeritus of Psychology at the University of Oregon, Eugene, Oregon, and Adjunct Professor at the Sackler Institute for Developmental Psychobiology, Weill Medical College of Cornell University, New York, New York. Received for publication August 19, 2015; accepted August 19, 2015. From the Department of Psychology, University of Oregon, Eugene, Oregon. The author declares no conflicts of interest. Reprints: Michael I. Posner, PhD, Department of Psychology, 1227 University of Oregon, Eugene, Oregon 97403 (e-mail: mposner@ uoregon.edu). Copyright r 2015 Wolters Kluwer Health, Inc. All rights reserved.

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measures of reaction time with undergraduates. With the help of my brother Jerry [Jerome B. Posner], a leading neurologist at Memorial Sloan Kettering Cancer Center, I had started to collect data from patients with the hope of connecting brain areas to the mental operations defined by cognitive studies, particularly those involved in attention. At the end of Dr Marin’s presentation, I approached him with the idea of discussing possible collaboration. Even before I could get to this topic, I was stunned and delighted when he said he would be moving to Portland, Oregon to head the Department of Neurology at Good Samaritan Hospital, and we should consider setting up a laboratory there. It was beyond my wildest dream. With the aid of many others, in 1980 we developed the Laboratory of Cognitive Neuropsychology for the study of brain injury at Good Samaritan. Oscar was the focal point for all of the clinical activity with patients. The research staff had tremendous freedom to pursue their work. I was director of the lab, but was usually around for only 1 day each week. There was little to do in the way of administrative duties, and John Walker handled these when I was unavailable. Portland is 112 miles up the Interstate 5 freeway from Eugene, a dreary ride through the relatively flat heart of the Willamette Valley. For 7 years, I made that commute nearly every week. Usually a 2-hour drive, it could become 5 hours in a winter ice storm. But the trip was always worthwhile because Oscar Marin understood the brain and its disorders more completely than anyone I had known. Oscar’s years as a pathologist meant that he really grasped how the anatomy of the brain constrained its function. His love of behavioral neurology allowed him to use his knowledge of anatomy to understand the patient’s problem at a deep level. During its 7 years, the lab attracted many of the world leaders in neuropsychology, including sabbatical visitors Alan Wing, PhD, Sandy [Alexander] Pollatsek, PhD, Jon [Jonathan] Vaughan, PhD, Avishai Henik, PhD, Neil Carlson, PhD, and Tony [Anthony] Marcel, PhD, as well as a stream of visiting postdoctoral fellows such as Eric Sie´roff, MD, PhD, Fran [Frances] Friedrich, PhD, and Albrecht Inhoff, PhD [see his article in this issue]. Local trainees included postdoctoral fellows John Walker and Christine Glenn, and Richard Ivry and David Margolin received their PhDs for work done in the lab. The snapshot shows lab members from those early years. When I left Oregon in 1985 to work on neuroimaging at Washington University in St Louis, a new www.cogbehavneurol.com |

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Members of the Cognitive Neuropsychology Laboratory at Good Samaritan Hospital, Portland, Oregon, around 1981. Front row, seated, left to right: Christine Glenn, David Margolin, Alan Wing. Middle row, standing, left to right: Ann Barnard (secretary to Robert Rafal), Frances Friedrich, Avishai Henik, Oscar Marin, John Walker. Back row, standing, left to right: Robert Rafal, Benson Schaffer, Michael Posner, Jonathan Vaughan, Neil Carlson, Steven Keele. Photograph courtesy of Michael Posner.

collaboration on the cerebellum between Richard Ivry and Steven Keele, PhD, became one of the lab’s major projects, while Oscar remained heavily involved in his studies of language and music. Following Oscar’s retirement in the late 1980s, the Good Samaritan Neurological Sciences Institute, which had housed our lab when we started it, became a part of Oregon Health and Sciences University, and Good Samaritan Hospital itself became part of Legacy Health. Sadly, the lab ended with this reorganization. Although never a large operation, the lab produced many important findings. I describe some representative examples below. Then follows a bibliography of representative papers written by lab members during and after the lab years. Some of these papers have become woven into the fabric of cognitive neuroscience. They form another of the many legacies of Oscar Marin and his remarkable career.

IMPORTANT FINDINGS FROM THE LAB Language and Music Oscar’s research program focused primarily on language and music. During his time in Portland, he explored these issues with researchers in the lab and patients on the ward. For a special issue of the International Journal of Psychology devoted to neuropsychology, Oscar wrote a major review that anticipated the promise of cognitive

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neuroscience (Marin, Glenn, and Walker, 1982). In this paper he introduced the use of epileptic automatisms as an approach to understanding motor programs and even speech. He reported a patient with a rare movement disorder, and used the case to argue strongly for a centrally patterned motor program, often triggered by an external influence. In his patient, this pattern ran over a fixed interval of 21 seconds, even when the physician constrained the patient’s movements. Years before the era of modern imaging, Oscar argued effectively for the integration of biological and cognitive approaches to neuropsychology. The central role that language plays in neurological diagnosis was brought home to me when I was observing rounds at Good Samaritan. Rounds with Oscar were great lessons for me, and his discussions of the detailed anatomy of a disorder were always a revelation. One day, Oscar was delayed and the residents stepped in to lead the discussion. They were trying to diagnose a man who seemed both confused and demented. He could barely answer the questions and often failed to comply with simple instructions. Oscar arrived, fresh from the airport. After a few moments, he began to address the patient in Spanish. The masked face and confused responses were replaced by a smile, pleasure, and clearly responsive actions. Linguistic differences had masqueraded as dementia. It was a lesson for us all. Oscar attracted many interesting people to his department and lab. One of them was Eric Sie´roff, a neuropsychologist then from Lyon, France. During his time in the Copyright

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lab, and later with me at Washington University in St Louis, Eric conducted many valuable clinical studies of language. One paper in particular (Sie´roff and Posner, 1988) described a task in which a cue was presented to participants to the left or right of a briefly presented letter string. When the string was random letters and attention was drawn to the right by a cue to that side, healthy participants nearly always neglected the first few letters on the left, just as people who suffer from neglect do. However, when the string formed a word, both healthy participants and those with neglect almost always reported it correctly, no matter where they were cued. This finding fit with the idea that neglect is a disorder of attention. As for Oscar’s work in music: In a 1982 book chapter (Marin, 1982), he showed the clear separation between language and music based on case studies of patients with amusia or aphasia. However, he believed that music and language could be tied together based partly on their common sequential nature and also through the study of grammar. He and John Walker made this point in a review of a book by Lerdahl and Jackendoff (Marin and Walker, 1988). While critical of the book’s overemphasis on hierarchical structures, Oscar stressed the importance of studying the similarities and differences in the grammars of music and language.

Bradyphrenia Robert Rafal is a neurologist who currently practices neurology and carries on an active research program at the University of Bangor, North Wales [see Dr Rafal’s articles in this issue]. At the time that our lab was created, he had a private practice in Portland. He had published articles on progressive supranuclear palsy and was very interested in impairments in vision and cognition in patients with this palsy as well as other disorders. He was also a close friend, former pupil, and colleague of Oscar Marin. Bob told me that patients with Parkinson disease who showed motor retardation and other motor signs also might be slow in their thinking, a phenomenon that he called bradyphrenia. I told Bob that I knew nothing about Parkinson disease or the basal ganglia, but I did know how to measure the speed of thought. Under Oscar’s benevolent direction, in space provided by the Neuroscience Institute, we studied Bob’s hypothesis. Our goal was to separate the disease’s effect on the basal ganglia from the frontal dementia that affects many patients later in the disease. To do this, we tested patients who showed motor signs when off their medication, but not when medicated. This feature of Parkinson disease, together with strong cognitive measurements, showed that patients who were not demented showed differences in motor behavior when off their medication, but showed no slowing in their speed of cognition. Our paper, published in Brain (Rafal, Posner, Walker, and Friedrich, 1984), was an early product of the new lab and to date has been cited over 200 times. This was only one of many studies in which Bob participated at the lab (see the Neglect section below), on Copyright

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his way to becoming a leading figure in cognitive neuroscience.

Neglect To check attentional function, neurologists ask the patient to fixate on their nose. Then they wiggle a finger on the left hand, right hand, or both hands. When a finger is wiggled on each hand, patients with right parietal lesions often miss the finger opposite the lesion. This deficit, called extinction, often clears several weeks after the stroke. I had often observed Oscar Marin and Bob Rafal carry out this test during rounds. The anatomy of neglect from stroke was complex, but a central localization was the right inferior parietal lobe. Oscar, Bob, and I studied 13 patients who showed neglect from right parietal stroke. We reviewed the computed tomography scans, which were the best structural pictures available at the time. We tested the patients using a spatial orienting task that I had given to many students at the University of Oregon and that I believed measured the ability to disengage attention and switch it to a cued location. From our previous work, we assumed that extinction resulting from the lesion was causing an inability to attend to the side of space opposite the lesion in some, but not necessarily all, circumstances. Indeed, our study showed that the problem seemed to be in disengaging attention from a location when a target or cue was in the contralesional direction. The findings were published in the Journal of Neuroscience (Posner, Walker, Friedrich, and Rafal, 1984) and have been cited >1300 times. Because computed tomography was still primitive in the early 1980s, some of the anatomy was corrected by subsequent imaging studies (Friedrich, Egly, Rafal, and Beck, 1998), but much of the work that took place in the 1990s and beyond has supported our general view (Rinne, Hassan, Goniotakis, Chohan, Sharma, Langdon, Soto, and Bentley, 2013). Bob was also able to show that some subcortical areas were important contributors to attention networks. He found that patients with lesions that included the pulvinar also showed a kind of extinction, but that damage to this structure affected a different cognitive operation from that affected by parietal lesions. I think the aspect of this story that most interested Oscar was the ability to trace subtle deficits in attention long after most neurologists would have pronounced the patient “fully recovered.” The sensitivity of reaction time as a measure of recovery is supported by studies showing that reaction time can detect changes not seen with other behavioral methods for detecting neglect (Rengachary, d’Avossa, Sapir, Shulman, Corbetta, 2009). As Oscar frequently remarked, you could trust patients to tell you that they had a vision problem, even if they attributed it mostly to their eyeglasses. In 1985, when Oscar was spending time in Paris, he suffered a severe stroke. While he was still in the hospital, I received a letter from him. It described his situation in general terms, but did not specify the deficits that the stroke had caused. However, the letter included a selfportrait, striking because it had a detailed view of the www.cogbehavneurol.com |

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right side of his body but not of the left. I remember thinking that some part of Oscar had awareness of the neglect induced by the stroke, sufficient to send the picture, but perhaps not to write a description. Oscar attributed his remarkable recovery to the magnificent effort of the French neurologists to force him into an early and vigorous physical exercise program.

The Cerebellum One of the most notable developments to arise from the lab was the collaboration between Steve Keele and Richard Ivry on the cerebellum. Robert Dow, MD, who founded the Neuroscience Institute, was the first neurologist in the State of Oregon and one of the first scientists to study the physiology of the cerebellum. Steve Keele earned his BS at the University of Oregon and his PhD in psychology at the University of Wisconsin. He returned to Oregon as a postdoctoral fellow in my lab, and later became a professor and one of my closest colleagues. Steve had at first exhibited considerable skepticism about the founding of the cognitive neuropsychology lab, saying that my interest in neuropsychology was “kowtowing to the physiologists.” However, about the time that I left to work in St Louis, Steve, who had a long-standing interest in motor control, came under the spell of Oscar’s enthusiasm during rounds and wanted to learn whether studying patients could help advance understanding of the functional contribution of neural structures within the motor system. Steve used a fine-grained analysis of periodic movements that he learned at the lab from Alan Wing. Alan had developed the model at Cambridge University and took a sabbatical in Portland, where he worked closely with Steve. The Wing model was able to help the team separate peripheral delays in timing from those caused by a central clock. The central clock timing was clearly affected by cerebellar damage. Cerebellar damage also reduced perceptual timing. After Steve’s untimely death in 2005, Richard Ivry described the significance of their findings in a memorial article that reviewed Steve’s legacy: Before that work, the study of cerebellar function had always been in terms of its role in the control of coordinated movements. The [Keele] articles offered a fundamental shift in perspective, suggesting that a specialized computation for timing associated with the cerebellum may be invoked across distinct domains, regardless of whether the tasks require timing for action or timing for perception. As such, Steve’s work provides important insights, both for a functional analysis of the neural systems involved in motor control and for developing psychological models of motor control. [Ivry RB, Mayr U, Corcos DM, Posner MI. 2006. Psychological processes and neural mechanisms for action: the legacy of Steven W. Keele. J Mot Behav. 38:3–6; page 4. Reprinted by permission of Taylor & Francis Ltd.]

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Together with Richard Ivry, Steve argued that the conceptualization of the cerebellum as an internal timing system offers a principled basis for understanding the role of that structure in motor learning. In this and his other work, Steve placed the emphasis on the nature of the underlying computation rather than on the specific task being studied. This approach taken by Keele and Ivry was very much in the spirit of Oscar’s view of neuropsychology. Oscar was delighted that the lab and the patients he had helped recruit were now contributing fundamental insights to neuroscience. Richard Ivry continued many important studies at the University of California Santa Barbara and later at the University of California Berkeley, where he now chairs the Department of Psychology.

Attention and Performance XI: Mechanisms of Attention Many of the methods developed in Oscar’s lab are now being used in clinical settings. I think that, more than any other of the lab’s accomplishments, this would have pleased Oscar, whose primary interest was the role of medicine in helping people. In July 1984, we hosted a meeting of the Association for Attention and Performance in Eugene, Oregon. Our meeting included distinguished neurophysiologists like Alan Cowey, PhD, Giacomo Rizzolatti, MD, and Robert Wurtz, PhD; human electrophysiologists like Stephen Hillyard, PhD, and Risto Na¨a¨ta¨nen, PhD; people using neuropsychological methods, like Bob Rafal, John Duncan, PhD, and Edoardo Bisiach, MD; and classic cognitive psychologists like Max Coltheart, PhD, Anne Treisman, PhD, and Steven Pinker, PhD. The topic was attention, and the excitement in the room at the integration of many methods was high and sustained through the long meeting. The meeting was unique. While it is now common for scientific conferences to bring together researchers using methods ranging from behavioral studies in healthy and neurological populations to cellular recordings in non-human animal models, it was quite uncommon at that time, a period before the term cognitive neuroscience had taken hold. Oscar and I summarized the meeting in the 1985 volume of Attention and Performance XI: Mechanisms of Attention (Posner and Marin, 1985) by saying: With few exceptions, the central emphasis in previous meetings of the Attention and Performance Association was on the information-processing approach to normal human cognition. This emphasis has been supplemented, on occasion, by studies employing EEG methods, but there have not been systematic attempts to relate the information-processing approach to work in the neurosciences. In this volume we seek to emphasize the search for mechanisms with such methods of approach as the following: anatomical, physiological, neuropsychological, behavioral, and computational. We believe this to be in accord with recent developing trends in cognition and particularly with developments in the study of attention. [page xxi] Copyright

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Also in 1985, I moved to St Louis and began work that proved instrumental in introducing the use of neuroimaging methods to observe the human brain during cognitive tasks. This work and many other events led to the development of cognitive neuroscience. Oscar Marin, his department, and his research program were important contributors to the emergence of this new paradigm. He was the guiding hand behind the work of his lab, although often unrecognized because he gave lab members the freedom to pursue their interests. I am sure he would be impressed to see how cognitive neuroscience has become established as a core area of study, and pleased to see how this work contributes to the care of the patients about whom he cared so deeply. ACKNOWLEDGMENTS The author acknowledges the helpful comments of Mary K. Rothbart, Richard Ivry, Bob Rafal, and Eric Sie´roff in constructing this account. Thanks also to Dr Myron Rothbart for his help improving the photograph of the lab members. BIBLIOGRAPHY Selected publications by the Cognitive Neuropsychology Laboratory at Good Samaritan Hospital, Portland, Oregon, and by some of its members after the lab closed in 1987: Friedrich FJ, Glenn CG, Marin OSM. 1984. Interruption of phonological coding in conduction aphasia. Brain Lang. 22:266–291. Friedrich FJ, Walker JA, Posner MI. 1985. Effects of parietal lesions on visual matching: implications for reading errors. Cogn Neuropsychol. 2:250–264. Hayes AE, Davidson MC, Keele SW, Rafal RD. 1998. Toward a functional analysis of the basal ganglia. J Cogn Neurosci. 10:178–198. Inhoff A, Diener H, Rafal R, Ivry R. 1989. The role of cerebellar structures in the execution of serial movements. Brain. 112:565–581. Ivry RB, Keele SW. 1989. Timing functions of the cerebellum. J Cogn Neurosci. 1:136–152. Ivry RB, Keele SW, Diener H. l988. Dissociation of the lateral and medial cerebellum in movement timing and movement execution. Exp Brain Res. 73:167–180. Keele SW, Ivry RB. 1991. Does the cerebellum provide a common computation for diverse tasks? A timing hypothesis. In: Diamond A, ed. The Development and Neural Bases of Higher Cognitive Function. Ann NY Acad Sci. 608:179–211. Keele SW, Rafal RD. 2000. Deficits in attentional set in patients with lesions of the left prefrontal cortex. In: Monsell S, Driver J, eds. Attention and Performance XVIII: Control of Cognitive Processes. Cambridge, Massachusetts: MIT Press; 627–652. Marin OSM. 1982. Neurological aspects of music perception and performance. In: Deutsch D, ed. The Psychology of Music, 1st ed. New York, New York: Academic Press; 453–477. Marin OSM, Glenn CG, Rafal RD. 1983. Visual problem solving in the absence of lexical semantics: evidence from dementia. Brain Cogn. 2:285–311. Marin OSM, Glenn CG, Walker JA. 1982. Changing perspectives in cognitive neuropsychology. Int J Psychol. 17:231–257. Marin OSM, Walker JA. 1988. The grammar of music: review of A Generative Theory of Tonal Music by Fred Lerdahl and Ray Jackendoff. Contemp Psychol. 33:226–228. Posner MI. 1984. Current research in the study of selective attention. In: Donchin E, ed. Cognitive Psychophysiology: Event-related Potentials and the Study of Cognition. Hillsdale, New Jersey: Lawrence Erlbaum; 2:37–50.

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Oscar Marin and the Creation of a Cognitive Neuropsychology Laboratory

Posner MI. 1984. Mechanisms of attention. In: Stevenson H, Ching CC, eds. Studies of Cognition. Proceedings of a joint meeting of the Chinese and US Academy of Sciences. Washington, DC: American Psychological Association; 373–380. Posner MI. 1984. Neural systems and cognitive processes. In: Lagerspetz K, Niemi P, eds. Psychology in the 1990’s. North Holland: Amsterdam, The Netherlands; 241–251. Posner MI. 1984. Selective attention and the storage of information. In: McGaugh J, Lynch G, Weinberger N, eds. Neurobiology of Learning and Memory. New York: Guilford Press; 89–101. Posner MI. 1988. Structures and functions of selective attention. In: Boll T, Bryant B, eds. Master Lectures in Clinical Neuropsychology and Brain Function: Research, Measurement, and Practice. American Psychological Association; 171–202. Posner MI, Cohen Y. 1984. Components of visual orienting. In: Bouma H, Bouwhuis DG, eds. Attention and Performance X. Hillsdale, New Jersey: Lawrence Erlbaum; 32:531–556. Posner MI, Cohen Y, Choate L, Hockey R, Maylor E. 1984. Sustained concentration: passive filtering or active orienting. In: Kornblum S, Requin J, eds. Preparatory States and Processes. Hillsdale, New Jersey: Lawrence Erlbaum; 49–65. Posner MI, Cohen Y, Rafal RD. 1982. Neural systems control of spatial orienting. Philos Trans R Soc Lond B Biol Sci. 298:187–198. Posner MI, Henik A. 1983. Isolating representational systems. In: Beck J, Hope B, Rosenfeld A, eds. Human and Machine Vision. New York, New York: Academic Press; 395–412. Posner MI, Marin OSM, eds. 1985. Attention and Performance XI: Mechanisms of Attention. Hillsdale, New Jersey: Lawrence Erlbaum Associates. Posner MI, McLeod P. 1982. Information processing models: in search of elementary operations. Ann Rev Psychol. 33:477–514. Posner MI, Pea R, Volpe B. 1982. Cognitive neuroscience: developments toward a science of synthesis. In: Mehler J, Walker E, Garrett M, eds. Perspectives on Mental Representations. Hillsdale, New Jersey: Lawrence Erlbaum; 251–276. Posner MI, Rafal RD, Choate L, Vaughan J. 1985. Inhibition of return: neural mechanisms and function. Cogn Neuropsychol. 2:211–228. Posner MI, Walker JA, Friedrich FJ, Rafal RD. 1984. Effects of parietal lobe injury on covert orienting of visual attention. J Neurosci. 4:1863–1874. Rafal RD, Posner MI, Friedman JH, Inhoff AW, Bernstein E. 1988. Orienting of visual attention in progressive supranuclear palsy. Brain. 111:267–280. Rafal RD, Posner MI, Walker JA, Friedrich FA. 1984. Cognition and the basal ganglia: separating mental and motor components of performance in Parkinson’s disease. Brain. 107:1092–1094. Sie´roff E, Pollatsek A, Posner MI. 1988. Recognition of visual letter strings following injury to the posterior visual spatial attention system. Cogn Neuropsychol. 5:427–449. Sie´roff E, Posner MI. 1988. Cueing spatial attention during processing of words and letter strings in normals. Cogn Neuropsychol. 5:451–472.

ADDITIONAL REFERENCES CITED IN THE TEXT Friedrich FJ, Egly R, Rafal RD, Beck D. 1998. Spatial attention deficits in humans: a comparison of superior parietal and temporal-parietal junction lesions. Neuropsychology. 12:193–207. Ivry RB, Mayr U, Corcos DM, Posner MI. 2006. Psychological processes and neural mechanisms for action: the legacy of Steven W. Keele. J Mot Behav. 38:3–6. Keele SW, Ivry RB, Mayr U, Hazeltine E, Heuer H. 2003. The cognitive and neural architecture of sequence representation. Psychol Rev. 110:316–339. Rengachary J, d’Avossa G, Sapir A, Shulman GL, Corbetta M. 2009. Is the Posner Reaction Time Test more accurate than clinical tests in detecting left neglect in acute and chronic stroke? Arch Phys Med Rehabil. 90:2081–2088. Rinne P, Hassan M, Goniotakis D, Chohan K, Sharma P, Langdon D, Soto D, Bentley P. 2013. Triple dissociation of attention networks in stroke according to lesion location. Neurology. 81:812–820.

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Oscar Marin and the Creation of a Cognitive Neuropsychology Laboratory.

During the 1980s, the Cognitive Neuropsychology Laboratory at Good Samaritan Hospital, Portland, Oregon, made important strides in the study of brain ...
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