Carol A. Barnes Award for Distinguished Scientific Contributions Citation “For her groundbreaking work on the neurobiological mechanisms underlying memory changes in normal aging. Carol A. Barnes understood early that a detailed knowledge of the process of normal aging would provide the essential background against which disease-related brain changes could be understood. Her work has been distinguished by the breadth of scientific techniques and levels of analysis she uses to investigate the complex topic of brain aging. She has been an exemplary citizen, serving the scientific community in many ways and as an outstanding mentor to the many students who carry on her work.”
Biography Carol A. Barnes grew up in northern California and com pleted her undergraduate degree in psychology at the Uni versity of California, Riverside. While there, she became interested in the complexity of animal behavior and volun teered in several laboratories to gain research experience in this area. Barnes worked with Sally Sperling to explore the rules of instrumental conditioning using pigeons, com pleted observational studies of dominance hierarchies in nonhuman primates in Austin Reisen’s lab, and collected and analyzed elephant seal mother and pup vocalizations and interactions on Ana Nuevo Island for a project headed by Lew Petrinovich.
730
Based on her interest in psychology programs that em phasized the biological basis of behavior, Barnes then ap plied to a number of graduate schools in the eastern United States and Canada. She ultimately chose Carleton Univer sity, which had a strong biopsychology group, attractive fellowship possibilities, and was located in the beautiful city of Ottawa. Her graduate advisor, Peter Fried, had strong interests in developmental psychopharmacology. Barnes’s first experiments in this area were conducted at a government experimental farm in Ottawa, where she devel oped a set of behavioral tasks for miniature pigs, which provided a promising experimental model because they have digestive systems much like humans. Mostly these animals outsmarted the experimenter, but Barnes was able to establish some routine tests that were useful to scientists at the farm and at the university. Her master’s thesis was the first study in rats to look at the effect of drug (cannabinoid) exposure in early development, on drug tolerance later in life (greater sensitivity), and on brain morphology in adult hood (brain size was reduced). Three things happened in the early 1970s at Carleton University that clarified the direction that Barnes’s final dissertation project should take. The first was prompted by a phone call from her mother, who was concerned about the fact that Barnes’s grandfather was getting a bit “turned around” on some of the long walks he would take. This prompted Barnes to conduct literature searches on aging brain and memory, after which she concluded that little was actually known. The second was the circulation of a mono graph that eventually found its way to her desk, written before the now classic book The Hippocampus as a Cog nitive Map by John O’Keefe and Lynn Nadel. In the mono graph was a description of how the hippocampus has very similar functions in memory in humans and other animals. Finally, in 1973, Terje Lpmo, Tim Bliss, and Tony Gardner-Medwin discovered a biological mechanism in the hip pocampus capable of laying down and retrieving memo ries— one analogous to that articulated by Donald Hebb in his 1949 book The Organization o f Behavior. Based on the method that Lpmo and his colleagues devised, a fully controllable, experimental procedure to study the biology of memory was enabled for the first time. Barnes’s dissertation experiment became clear to her—she would combine be havioral studies with neurobiological experiments to inves tigate how the brain acquires, stores, and retrieves informa tion across the life span. At this time, there were only three labs in the world routinely conducting experiments using methods that could monitor synaptic plasticity in the brain. Graham Goddard’s laboratory at Dalhousie University in Halifax, Nova Scotia, was the only one conducting studies in awake, behaving animals—a requirement in Barnes’s mind for the aging study. As it turned out, her early mentor, Peter Fried, had been one of Goddard’s students, so he connected Goddard
November 2014 • American Psychologist © 2014 American Psychological Association 0003-066X/14/$12.00 Vol. 69, No. 8, 730-732 http://dx.doi.org/10.1037/a0037573
and Barnes and she transferred to Halifax to complete her dissertation. The data from this work provided the first con crete evidence that the persistence of long-term potentiation (LTP) and the durability of memory were related, and that a decline in LTP persistence was associated with poorer spatial memory in old animals. This finding was a milestone because it laid the groundwork for an explosion of research on the biophysical and molecular mechanisms of memory and its decline during normal and abnormal aging. In 1978, Barnes applied to the recently formed National Institute on Aging (NIA) for a postdoctoral fellowship to learn in vitro electrophysiological techniques at the worldrenowned Institute of Neurophysiology in Oslo with Per Andersen. She became NLA’s first postdoctoral fellow in neuroscience at the University of Oslo (1979-1980), where she conducted detailed analyses of the biophysics of aging tissue in vitro. These studies provided some of the early evidence that the pattern of biophysical change in the hip pocampus was not one of general deterioration (as previously widely believed), but rather was highly selective and in some cases appeared compensatory rather than detrimental. After a visit by John O’Keefe to Andersen’s lab in Oslo in the latter part of Barnes’s fellowship, it was clear to her that the application of single-unit recording methods to questions concerning “cognitive maps” in older rats provided an excit ing opportunity. Barnes moved to London and received a National Science Foundation-NATO Postdoctoral Fellow ship for Scientists for the full year of 1981, during which she demonstrated that there were age-related changes in the re liability of spatial representations in hippocampal circuits of older animals. In this same year in London, Bruce McNaughton had the idea for the design of an electrode (the “tetrode” recording probe) that could monitor and distinguish many cells at once in behaving rats, which would dramati cally change the field of in vivo single-cell recording. In 1982, Barnes assumed a faculty position in the Depart ment of Psychology at the University of Colorado Boulder and received her first Research Project Grant (ROl) from NIA that year. She was promoted to associate professor with tenure in 1985 and to full professor in 1989. She continued research on memory, biophysical, and network changes dur ing aging and began to search for possible pharmacological and other treatments (such as exercise) for the amelioration or delay of age-related cognitive declines. Additionally, she initiated collaborations with Aryeh Routtenburg and Paul Worley to develop strategies to study the molecular basis of cognitive and brain plasticity in aging. In 1990, Barnes moved to the University of Arizona (UA) in Tucson, where she co-founded the Arizona Research Lab oratories Division of Neural Systems, Memory, and Aging (NSMA), a dedicated research unit for the study of brain mechanisms of memory and aging. In 2006, she was ap pointed Regents’ Professor, and the McKnight Brain Re search Foundation named her director and endowed chair of November 2014 • American Psychologist
the new Evelyn F. McKnight Brain Institute at UA. In 2009, Barnes was also named associate director of UA’s interdis ciplinary BI05 Institute. Barnes has made notable advances through her research, including the implementation of the hardware and software necessary for true high-density recording using the tetrode recording probes that were first conceived in 1981. Results from ensemble recording studies include data that suggest that old rats show hippocampal map retrieval failures as well as disrupted sequences of spontaneously reactivated activity patterns during rest and sleep that are thought to strengthen memory consolidation processes in cortex. Although the mul tiple tetrode recording method was a large advance over the limitations of recording one or two neurons at a time, samples sizes above —100-200 cells are difficult to achieve. Barnes and collaborators, including Paul Worley (who cloned the Arc gene), developed a method using the immediate early gene Arc that can monitor activity over hundreds of thou sands of cells across the brain (the “catFISH” method). With this method, they have been able to identify a number of selective activity changes with age within hippocampal cir cuits and to identify transcriptional repression mechanisms that may be responsible for the reduction in behavior-induced Arc expression. Another novel project that Barnes initiated involves extending the findings from aging in the rodent to the nonhuman primate, including behavior, imaging, and high-density unit recordings. The recently implemented tele metered recordings in completely unrestrained primates have the potential to contribute substantively to a deeper under standing of the neural basis of behavior. For her career-long service and mentoring contributions, the Society for Neuroscience honored Barnes with its Mika Salpeter Lifetime Achievement Award in 2010, and for her scientific contributions to the field, the Ralph W. Gerard Prize in Neuroscience in 2013. Barnes’s work over the past 40 years has triggered fun damental advancements in the understanding of the adaptive character of the aging brain and has been instrumental in defining neurobiological norms of successful brain aging across mammalian species as well as what changes in the brain are “normal” versus predictive of disease. S e le c te d B i b l io g r a p h y Alexander, G. E., Chen, K., Aschenbrenner, M., Merkley, T. L., SanterreLemmon, L. E„ Shamy, J. L..........Barnes, C. A. (2008). Age-related regional network of magnetic resonance imaging gray matter in the rhesus macaque. The Journal o f Neuroscience 28(11), 2710—2718. doi: 10.1523/JNEUROSCI. 1852-07.2008 Barnes, C. A. (1979). Memory deficits associated with senescence: A neurophysiological and behavioral study in the rat. Journal o f Compar ative and Physiological Psychology 95(1), 74-104. doi: 10.1037/ h0077579 Barnes, C. A., Forster, M. J., Fleshner, M., Ahanotu, E. N., Laudenslager, M. L., Mazzeo, R. S .,. . . Lai, H. (1991). Exercise does not modify spatial memory, brain autoimmunity, or antibody response in aged F-344 rats. Neurobiology o f Aging, 72(1), 47 -5 3 . doi: 10.1016/01974580(91)90038-L
731
Barnes, C. A., & McNaughton, B. L. (1980). Physiological compensation for loss of afferent synapses in rat hippocampal granule cells during senescence. The Journal o f Physiology, 309, 473—485. Barnes, C. A., McNaughton, B. L., & O’Keefe, J. (1983). Loss of place specificity in hippocampal complex spike cells of senescent rat. Neuro biology of Aging, 4(2), 113-119. doi: 10.1016/0197-4580(83)90034-9 Barnes, C. A., Suster, M. S., Shen, J., & McNaughton, B. L. (1997). Multistability of cognitive maps in the hippocampus of old rats. Nature, 388(6639), 272-275. doi: 10.1038/40859 Burke, S. N., Maurer, A. P., Nematollahi, S., Uprety, A., Wallace, J. L., & Barnes, C. A. (2014). Advanced age dissociates dual functions of the perirhinal cortex. The Journal o f Neuroscience, 34(2), 467-480. doi: 10.1523/JNEUROSCI.2875-13.2014 Burke, S. N., Maurer, A. P., Yang, Z., Navratilova, Z., & Barnes, C. A. (2008). Glutamate receptor-mediated restoration of experience-dependent place field expansion plasticity in aged rats. Behavioral Neuroscience, 722(3), 535-548. doi: 10.1037/0735-7044.122.3.535 Burke, S. N., Wallace, J. L., Nematollahi, S., Uprety, A. R., & Barnes, C. A. (2010). Pattern separation deficits may contribute to age-associated rec ognition impairments. Behavioral Neuroscience, 124(5), 559-573. doi: 10.1037/a0020893 Guzowski, J. F., McNaughton, B. L., Barnes, C. A., & Worley, P. F. (1999). Environment-specific expression of the immediate-early gene Arc in hippocampal neuronal ensembles. Nature Neuroscience, 2(12), 11201124. doi:10.1038/16046 Insel, N., Patron, L. A., Hoang, L. T., Nematollahi, S., Schimanski, L. A., Lipa, P., & Barnes, C. A. (2012). Reduced gamma frequency in the medial frontal cortex of aged rats during behavior and rest: Implications for age-related behavioral slowing. The Journal of Neuroscience, 32(46), 16331-16344. doi:10.1523/JNEUROSCI.1577-12.2012 Marrone, D. F., Satvat, E., Shaner, M. J., Worley, P. F., & Barnes, C. A. (2012). Attenuated long-term Arc expression in the aged fascia dentata.
732
Neurobiology o f Aging, 33(5), 979-990. doi:10.1016/j.neurobiolaging .2010.07.022 McNaughton, B. L., O’Keefe, J., & Barnes, C. A. (1983). The stereotrode: A new technique for simultaneous isolation of several single units in the central nervous system from multiple unit records. Journal of Neurosci ence Methods, 8(4), 391-397. doi: 10.1016/0165-0270(83)90097-3 Penner, M. R., Roth, T. L., Chawla, M. K., Hoang, L. T., Roth, E. D., Lubin, F. D....... Barnes, C. A. (2011). Age-related changes in Arc transcription and DNA methylation within the hippocampus. Neurobiology of Aging, 32(12), 2198-2210. doi:10.1016/j.neurobiolaging.2010.01.009 Samson, R. D„ Venkatesh, A., Patel, D. H., Lipa, P., & Barnes, C. A. (2014). Enhanced performance of aged rats in contingency degradation and instrumental extinction tasks. Behavioral Neuroscience, 128(2), 122— 123. doi: 10.1037/a0035986 Schimanski, L. A., Lipa, P., & Barnes, C. A. (2013). Tracking the course of hippocampal representations during learning: When is the map required? The Journal o f Neuroscience, 33(1), 3094-3106. doi: 10.1523/ JNEUROSCI.1348-12.2013 Shen, J., & Barnes, C. A. (1996). Age-related decrease in cholinergic synaptic transmission in three hippocampal subfields. Neurobiology of Aging, 77(3), 439-451. doi:10.1016/0197-4580(96)00020-6 Shen, J., Barnes, C. A., McNaughton, B. L., Skaggs, W. E., & Weaver, K. L. (1997). The effect of aging on experience-dependent plasticity of hip pocampal place cells. The Journal o f Neuroscience, 77(17), 6769-6782. Skaggs, W. E., McNaughton, B. L., Permenter, M., Archibeque, M., Vogt, J., Amaral, D. G., & Barnes, C. A. (2007). EEG sharp waves and sparse ensemble unit activity in the macaque hippocampus. Journal of Neuro physiology, 98(2), 898-910. doi:10.1152/jn.00401.2007 Small, S. A., Chawla, M. K.. Buonocore, M., Rapp, P. R., & Barnes, C. A. (2004). Imaging correlates of brain function in monkeys and rats isolates a hippocampal subregion differentially vulnerable to aging. PNAS: Pro ceedings o f the National Academy o f Sciences, USA, 707(18), 7181-7186. doi: 10.1073/pnas.0400285101
November 2014 • American Psychologist
Copyright of American Psychologist is the property of American Psychological Association and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.
Biography Carol A. Barnes grew up in northern California and com pleted her undergraduate degree in psychology at the Uni versity of California, Riverside. While there, she became interested in the complexity of animal behavior and volun teered in several laboratories to gain research experience in this area. Barnes worked with Sally Sperling to explore the rules of instrumental conditioning using pigeons, com pleted observational studies of dominance hierarchies in nonhuman primates in Austin Reisen’s lab, and collected and analyzed elephant seal mother and pup vocalizations and interactions on Ana Nuevo Island for a project headed by Lew Petrinovich.
730
Based on her interest in psychology programs that em phasized the biological basis of behavior, Barnes then ap plied to a number of graduate schools in the eastern United States and Canada. She ultimately chose Carleton Univer sity, which had a strong biopsychology group, attractive fellowship possibilities, and was located in the beautiful city of Ottawa. Her graduate advisor, Peter Fried, had strong interests in developmental psychopharmacology. Barnes’s first experiments in this area were conducted at a government experimental farm in Ottawa, where she devel oped a set of behavioral tasks for miniature pigs, which provided a promising experimental model because they have digestive systems much like humans. Mostly these animals outsmarted the experimenter, but Barnes was able to establish some routine tests that were useful to scientists at the farm and at the university. Her master’s thesis was the first study in rats to look at the effect of drug (cannabinoid) exposure in early development, on drug tolerance later in life (greater sensitivity), and on brain morphology in adult hood (brain size was reduced). Three things happened in the early 1970s at Carleton University that clarified the direction that Barnes’s final dissertation project should take. The first was prompted by a phone call from her mother, who was concerned about the fact that Barnes’s grandfather was getting a bit “turned around” on some of the long walks he would take. This prompted Barnes to conduct literature searches on aging brain and memory, after which she concluded that little was actually known. The second was the circulation of a mono graph that eventually found its way to her desk, written before the now classic book The Hippocampus as a Cog nitive Map by John O’Keefe and Lynn Nadel. In the mono graph was a description of how the hippocampus has very similar functions in memory in humans and other animals. Finally, in 1973, Terje Lpmo, Tim Bliss, and Tony Gardner-Medwin discovered a biological mechanism in the hip pocampus capable of laying down and retrieving memo ries— one analogous to that articulated by Donald Hebb in his 1949 book The Organization o f Behavior. Based on the method that Lpmo and his colleagues devised, a fully controllable, experimental procedure to study the biology of memory was enabled for the first time. Barnes’s dissertation experiment became clear to her—she would combine be havioral studies with neurobiological experiments to inves tigate how the brain acquires, stores, and retrieves informa tion across the life span. At this time, there were only three labs in the world routinely conducting experiments using methods that could monitor synaptic plasticity in the brain. Graham Goddard’s laboratory at Dalhousie University in Halifax, Nova Scotia, was the only one conducting studies in awake, behaving animals—a requirement in Barnes’s mind for the aging study. As it turned out, her early mentor, Peter Fried, had been one of Goddard’s students, so he connected Goddard
November 2014 • American Psychologist © 2014 American Psychological Association 0003-066X/14/$12.00 Vol. 69, No. 8, 730-732 http://dx.doi.org/10.1037/a0037573
and Barnes and she transferred to Halifax to complete her dissertation. The data from this work provided the first con crete evidence that the persistence of long-term potentiation (LTP) and the durability of memory were related, and that a decline in LTP persistence was associated with poorer spatial memory in old animals. This finding was a milestone because it laid the groundwork for an explosion of research on the biophysical and molecular mechanisms of memory and its decline during normal and abnormal aging. In 1978, Barnes applied to the recently formed National Institute on Aging (NIA) for a postdoctoral fellowship to learn in vitro electrophysiological techniques at the worldrenowned Institute of Neurophysiology in Oslo with Per Andersen. She became NLA’s first postdoctoral fellow in neuroscience at the University of Oslo (1979-1980), where she conducted detailed analyses of the biophysics of aging tissue in vitro. These studies provided some of the early evidence that the pattern of biophysical change in the hip pocampus was not one of general deterioration (as previously widely believed), but rather was highly selective and in some cases appeared compensatory rather than detrimental. After a visit by John O’Keefe to Andersen’s lab in Oslo in the latter part of Barnes’s fellowship, it was clear to her that the application of single-unit recording methods to questions concerning “cognitive maps” in older rats provided an excit ing opportunity. Barnes moved to London and received a National Science Foundation-NATO Postdoctoral Fellow ship for Scientists for the full year of 1981, during which she demonstrated that there were age-related changes in the re liability of spatial representations in hippocampal circuits of older animals. In this same year in London, Bruce McNaughton had the idea for the design of an electrode (the “tetrode” recording probe) that could monitor and distinguish many cells at once in behaving rats, which would dramati cally change the field of in vivo single-cell recording. In 1982, Barnes assumed a faculty position in the Depart ment of Psychology at the University of Colorado Boulder and received her first Research Project Grant (ROl) from NIA that year. She was promoted to associate professor with tenure in 1985 and to full professor in 1989. She continued research on memory, biophysical, and network changes dur ing aging and began to search for possible pharmacological and other treatments (such as exercise) for the amelioration or delay of age-related cognitive declines. Additionally, she initiated collaborations with Aryeh Routtenburg and Paul Worley to develop strategies to study the molecular basis of cognitive and brain plasticity in aging. In 1990, Barnes moved to the University of Arizona (UA) in Tucson, where she co-founded the Arizona Research Lab oratories Division of Neural Systems, Memory, and Aging (NSMA), a dedicated research unit for the study of brain mechanisms of memory and aging. In 2006, she was ap pointed Regents’ Professor, and the McKnight Brain Re search Foundation named her director and endowed chair of November 2014 • American Psychologist
the new Evelyn F. McKnight Brain Institute at UA. In 2009, Barnes was also named associate director of UA’s interdis ciplinary BI05 Institute. Barnes has made notable advances through her research, including the implementation of the hardware and software necessary for true high-density recording using the tetrode recording probes that were first conceived in 1981. Results from ensemble recording studies include data that suggest that old rats show hippocampal map retrieval failures as well as disrupted sequences of spontaneously reactivated activity patterns during rest and sleep that are thought to strengthen memory consolidation processes in cortex. Although the mul tiple tetrode recording method was a large advance over the limitations of recording one or two neurons at a time, samples sizes above —100-200 cells are difficult to achieve. Barnes and collaborators, including Paul Worley (who cloned the Arc gene), developed a method using the immediate early gene Arc that can monitor activity over hundreds of thou sands of cells across the brain (the “catFISH” method). With this method, they have been able to identify a number of selective activity changes with age within hippocampal cir cuits and to identify transcriptional repression mechanisms that may be responsible for the reduction in behavior-induced Arc expression. Another novel project that Barnes initiated involves extending the findings from aging in the rodent to the nonhuman primate, including behavior, imaging, and high-density unit recordings. The recently implemented tele metered recordings in completely unrestrained primates have the potential to contribute substantively to a deeper under standing of the neural basis of behavior. For her career-long service and mentoring contributions, the Society for Neuroscience honored Barnes with its Mika Salpeter Lifetime Achievement Award in 2010, and for her scientific contributions to the field, the Ralph W. Gerard Prize in Neuroscience in 2013. Barnes’s work over the past 40 years has triggered fun damental advancements in the understanding of the adaptive character of the aging brain and has been instrumental in defining neurobiological norms of successful brain aging across mammalian species as well as what changes in the brain are “normal” versus predictive of disease. S e le c te d B i b l io g r a p h y Alexander, G. E., Chen, K., Aschenbrenner, M., Merkley, T. L., SanterreLemmon, L. E„ Shamy, J. L..........Barnes, C. A. (2008). Age-related regional network of magnetic resonance imaging gray matter in the rhesus macaque. The Journal o f Neuroscience 28(11), 2710—2718. doi: 10.1523/JNEUROSCI. 1852-07.2008 Barnes, C. A. (1979). Memory deficits associated with senescence: A neurophysiological and behavioral study in the rat. Journal o f Compar ative and Physiological Psychology 95(1), 74-104. doi: 10.1037/ h0077579 Barnes, C. A., Forster, M. J., Fleshner, M., Ahanotu, E. N., Laudenslager, M. L., Mazzeo, R. S .,. . . Lai, H. (1991). Exercise does not modify spatial memory, brain autoimmunity, or antibody response in aged F-344 rats. Neurobiology o f Aging, 72(1), 47 -5 3 . doi: 10.1016/01974580(91)90038-L
731
Barnes, C. A., & McNaughton, B. L. (1980). Physiological compensation for loss of afferent synapses in rat hippocampal granule cells during senescence. The Journal o f Physiology, 309, 473—485. Barnes, C. A., McNaughton, B. L., & O’Keefe, J. (1983). Loss of place specificity in hippocampal complex spike cells of senescent rat. Neuro biology of Aging, 4(2), 113-119. doi: 10.1016/0197-4580(83)90034-9 Barnes, C. A., Suster, M. S., Shen, J., & McNaughton, B. L. (1997). Multistability of cognitive maps in the hippocampus of old rats. Nature, 388(6639), 272-275. doi: 10.1038/40859 Burke, S. N., Maurer, A. P., Nematollahi, S., Uprety, A., Wallace, J. L., & Barnes, C. A. (2014). Advanced age dissociates dual functions of the perirhinal cortex. The Journal o f Neuroscience, 34(2), 467-480. doi: 10.1523/JNEUROSCI.2875-13.2014 Burke, S. N., Maurer, A. P., Yang, Z., Navratilova, Z., & Barnes, C. A. (2008). Glutamate receptor-mediated restoration of experience-dependent place field expansion plasticity in aged rats. Behavioral Neuroscience, 722(3), 535-548. doi: 10.1037/0735-7044.122.3.535 Burke, S. N., Wallace, J. L., Nematollahi, S., Uprety, A. R., & Barnes, C. A. (2010). Pattern separation deficits may contribute to age-associated rec ognition impairments. Behavioral Neuroscience, 124(5), 559-573. doi: 10.1037/a0020893 Guzowski, J. F., McNaughton, B. L., Barnes, C. A., & Worley, P. F. (1999). Environment-specific expression of the immediate-early gene Arc in hippocampal neuronal ensembles. Nature Neuroscience, 2(12), 11201124. doi:10.1038/16046 Insel, N., Patron, L. A., Hoang, L. T., Nematollahi, S., Schimanski, L. A., Lipa, P., & Barnes, C. A. (2012). Reduced gamma frequency in the medial frontal cortex of aged rats during behavior and rest: Implications for age-related behavioral slowing. The Journal of Neuroscience, 32(46), 16331-16344. doi:10.1523/JNEUROSCI.1577-12.2012 Marrone, D. F., Satvat, E., Shaner, M. J., Worley, P. F., & Barnes, C. A. (2012). Attenuated long-term Arc expression in the aged fascia dentata.
732
Neurobiology o f Aging, 33(5), 979-990. doi:10.1016/j.neurobiolaging .2010.07.022 McNaughton, B. L., O’Keefe, J., & Barnes, C. A. (1983). The stereotrode: A new technique for simultaneous isolation of several single units in the central nervous system from multiple unit records. Journal of Neurosci ence Methods, 8(4), 391-397. doi: 10.1016/0165-0270(83)90097-3 Penner, M. R., Roth, T. L., Chawla, M. K., Hoang, L. T., Roth, E. D., Lubin, F. D....... Barnes, C. A. (2011). Age-related changes in Arc transcription and DNA methylation within the hippocampus. Neurobiology of Aging, 32(12), 2198-2210. doi:10.1016/j.neurobiolaging.2010.01.009 Samson, R. D„ Venkatesh, A., Patel, D. H., Lipa, P., & Barnes, C. A. (2014). Enhanced performance of aged rats in contingency degradation and instrumental extinction tasks. Behavioral Neuroscience, 128(2), 122— 123. doi: 10.1037/a0035986 Schimanski, L. A., Lipa, P., & Barnes, C. A. (2013). Tracking the course of hippocampal representations during learning: When is the map required? The Journal o f Neuroscience, 33(1), 3094-3106. doi: 10.1523/ JNEUROSCI.1348-12.2013 Shen, J., & Barnes, C. A. (1996). Age-related decrease in cholinergic synaptic transmission in three hippocampal subfields. Neurobiology of Aging, 77(3), 439-451. doi:10.1016/0197-4580(96)00020-6 Shen, J., Barnes, C. A., McNaughton, B. L., Skaggs, W. E., & Weaver, K. L. (1997). The effect of aging on experience-dependent plasticity of hip pocampal place cells. The Journal o f Neuroscience, 77(17), 6769-6782. Skaggs, W. E., McNaughton, B. L., Permenter, M., Archibeque, M., Vogt, J., Amaral, D. G., & Barnes, C. A. (2007). EEG sharp waves and sparse ensemble unit activity in the macaque hippocampus. Journal of Neuro physiology, 98(2), 898-910. doi:10.1152/jn.00401.2007 Small, S. A., Chawla, M. K.. Buonocore, M., Rapp, P. R., & Barnes, C. A. (2004). Imaging correlates of brain function in monkeys and rats isolates a hippocampal subregion differentially vulnerable to aging. PNAS: Pro ceedings o f the National Academy o f Sciences, USA, 707(18), 7181-7186. doi: 10.1073/pnas.0400285101
November 2014 • American Psychologist
Copyright of American Psychologist is the property of American Psychological Association and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.
