Terry Earl Robinson

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Terry Earl Robinson
Occupation(s)Biopsychologist and neuroscientist
Academic background
EducationBA., Psychology (1972)
MA., Biopsychology (1974)
PhD., Biopsychology (1978)
Alma materUniversity of Lethbridge
University of Saskatchewan
University of Western Ontario
ThesisBrainstem Influences On Hippocampal And Neocortical Slow Wave Activation During Waking Behavior And Sleep (1978)
Academic work
InstitutionsThe University of Michigan (Ann Arbor)

Terry Earl Robinson is a biopsychologist and neuroscientist, and the Elliot S. Valenstein Distinguished University Professor of Psychology & Neuroscience[1] at The University of Michigan (Ann Arbor).[2]

Robinson is most known for his research on the persistent psychological and neurobiological effects of repeated drug use, and how these may contribute to addiction and relapse. From 2010 onwards, his research has focused on how individual differences in attributing incentive salience to reward-associated cues may contribute to impulse-control disorders like addiction. He has published over 260 articles, edited two books and was listed on ISI HighlyCited.com as one of the highest cited (top 0.5%) scientists in Neuroscience.[3] His papers have been cited over 62,000 times and his h-Index is 110.[4] He is the recipient of APA's D.O Hebb Distinguished Scientific Contribution Award,[5] Distinguished Scientific Contributions Award,[6] and Neal Miller Lecturer,[7] EBPS' Distinguished Scientist Award,[8] APS' William James Fellow Award for Lifetime Achievement,[9] and Grawemeyer Award for Outstanding Ideas in Psychology.[10] He has also received The Henry Russel Lectureship, which is the U-M's highest honor for senior faculty,[11] a Honorary Doctor of Science (honoris causa) degree from the University of Lethbridge, Canada, and was listed on the Stanford University Names World's Top 2% Scientists in 2021.[12]

Robinson is a Fellow of the American Association for the Advancement of Science (AAAS), a Charter Fellow of the American Psychological Society (APS),[13] and a Fellow of Eastern Psychological Association.[14] He was President of the European Behavioral Pharmacology Society (EBPS) from 2015 to 2017.[3] In 2003, he served as chair for the Gordon Research Conference on Catecholamines at The Queen's College, Oxford.[15] He has participated in multiple NIH grant review panels, and held a NIH Research Career Development, NIDA Senior Scientist,[16] and NIDA-funded MERIT Award. In addition, he was the Editor-in-Chief of the journal, Behavioural Brain Research, from 1996 until 2010.[17]

Education

Robinson earned a B.A. in psychology from the University of Lethbridge in 1972, followed by an M.A. in the same field from the University of Saskatchewan in 1974. Subsequently, he obtained a Ph.D. in Biopsychology from the University of Western Ontario in 1978, and received postdoctoral training with Gary Lynch at the University of California, Irvine in the same year.[18]

Career

Robinson completed his Ph.D. research under the mentorship of C.H. Vanderwolf at the University of Western Ontario in 1978. He joined the University of Michigan as an assistant professor of psychology in 1978. In 2001, he was appointed the Elliot S. Valenstein Collegiate Professor of Behavioral Neuroscience, and since 2011 has been the Elliot S. Valenstein Distinguished University Professor of Psychology & Neuroscience at the University of Michigan, Ann Arbor.[19][11]

Research

Robinson has maintained a research program focusing on the psychological and neurobiological basis of addiction, especially the persistent effects of repeated psychostimulant drug use on behavior and neurobiology, and with his colleague Kent C. Berridge he has also contributed highly cited theoretical articles on the role of incentive-sensitization in addiction.[20][21][22][23]

Studies on behavioral sensitization

In the early 1980s, Robinson initiated studies using the amphetamine-induced rotational behavior model to explore the mesostriatal dopamine system's function and the influence of sex and gonadal hormones with Jill Becker. These studies revealed behavioral sensitization, where a single amphetamine injection increased subsequent behavioral responses, indicating drug-induced brain changes.[24][25] He then launched a long series of studies in the 1980s and 1990s to characterize the behavioral and neurobiological basis of sensitization, initially emphasizing it as a model of amphetamine psychosis. These studies include the first reports of sex differences and gonadal steroid modulation of sensitization, enhanced amphetamine-stimulated dopamine release in vitro (1982),[24] and in vivo (1988),[26] sensitization to cocaine after a single injection (1985),[27] cross-sensitization with stress (1985),[28] and its persistence, lasting over a year post-drug treatment (1991).[29]

The incentive-sensitization theory of addiction, and the role of dopamine in reward

In the 1980s, dopamine was believed to mediate the pleasure derived from reward consumption. However, in 1989, Kent Berridge, along with Robinson, reported that complete dopamine depletions had no effect on rats' hedonic reactions to tastes,[30] leading to the hypothesis that dopamine mediates motivation ('wanting') rather than pleasure ('liking'). Building on this, they proposed that addiction may result from neural sensitization, causing pathological 'wanting' for drugs, even if not particularly 'liked'. This concept gave rise to incentive-sensitization theory (1993),[31] influencing subsequent research on the role of incentive motivational processes in addiction. This paper ranked 15th among the 100 most cited articles in Neuroscience[32] and was listed as the single most cited paper in addiction research in 2021.[33] Their papers, are cited widely, and earned them the Grawemeyer Award in Psychology in 2019.[10][34][35][36]

Studies on the modulation of sensitization by environmental and pharmacokinetic factors

Continuing studies on behavioral and neural sensitization, Robinson, with Aldo Badiani, observed that environmental factors significantly influenced both the induction and expression of sensitization. Animals tested in a novel drug context often failed to express behavioral sensitization, termed context-specific sensitization. Simultaneously, the drug's context played a crucial role in sensitization induction, leading to research from 1996 to the mid-2000s on how context modulates the behavioral and neurobiological consequences of stimulant or opiate exposure, affecting dopamine neurotransmission and gene expression.[37][38][39] Additionally, in 2002, it was discovered that the speed of drug delivery to the brain greatly influences sensitization induction. These findings led to the hypothesis that rapidly reaching the brain enhances addiction potential by promoting sensitization-related neuroplasticity.[40]

Studies on structural plasticity associated with exposure to drugs of abuse

Collaborating with Bryan Kolb, Robinson hypothesized that long-lasting behavioral effects of drug exposure involve changes in synaptic connectivity, which would be reflected by changes in dendritic structure. In the late 1990s, they published the first paper on structural plasticity after amphetamine administration in 1997,[41] followed by studies on cocaine and morphine in 1999.[42] They also established patterns of changes in brain regions (e.g., dorsal vs. ventral striatum, prefrontal cortical subregions, other areas of the neocortex), their similarity after experimenter- or self-administered drugs (2002),[43] and the impact of past experience (2003),[44] and context (2004),[45] along with other features.[46]

Studies on individual differences in responding to reward cues and the role of pharmacokinetics in addiction development

Robinson has focused on individual differences in the extent to which reward cues, including drug cues, acquire motivational value (incentive salience). Initial studies, with Shelly Flagel, showed that only some animals (sign-trackers) attribute incentive salience to reward cues, which makes them attention-grabbing and desirable in their own right. It is established that only if reward cues act as incentive stimuli do they come to attract, incite, provoke, spur, and motivate, leading to potentially maladaptive behavior. Notably, sign-tracking is dopamine-dependent whereas goal-tracking, which is observed in animals that fail to attribute motivational value to cues, is not dopamine-dependent. Furthermore, Martin Sarter and colleagues have shown that sign-trackers have deficient choline transporters leading to poor executive/attentional control over behavior, relative to goal-trackers. Robinson has speculated that the combination of enhanced "bottom-up" motivational processes and poor "top-down" inhibitory control may render sign-trackers especially prone to addiction.[47]

Finally, Robinson has initiated an investigation into the impact of pharmacokinetic factors on the emergence of addiction-like behavior, using the Intermittent Access (IntA) self-administration procedure. Their findings have demonstrated IntA cocaine self-administration is especially effective in inducing addiction-like behavior, psychomotor, incentive, and dopamine sensitization, consistent with Incentive-Sensitization Theory.[48][49][50]

Awards and honors

  • 1988 – Fellow, American Association for the Advancement of Science (AAAS)[51]
  • 1989 – Charter Fellow, The American Psychological Society
  • 2010 – D.O Hebb Distinguished Scientific Contribution Award, American Psychological Association[5]
  • 2011 – Fellow, Eastern Psychological Association[14]
  • 2013 – Distinguished Scientist Award, European Behavioral Pharmacology Society[8]
  • 2014 – William James Fellow Award for Lifetime Achievement, Association for Psychological Science[9]
  • 2015 – Neal Miller Lecturer, American Psychological Association[7]
  • 2016 – Distinguished Scientific Contributions Award, American Psychological Association[6]
  • 2016 – Honorary Doctor of Science Degree, University of Lethbridge[52]
  • 2018 – Henry Russel Lectureship, University of Michigan[11]
  • 2019 – Grawemeyer Award for Outstanding Ideas in Psychology, University of Louisville[10]

Bibliography

Edited books

  • Behavioral Approaches to Brain Research (1983) ISBN 9780195032581
  • Microdialysis in the Neurosciences (1991) ISBN 9780444811943

Selected articles

  • Robinson, T. E., & Becker, J. B. (1986). Enduring changes in brain and behavior produced by chronic amphetamine administration: a review and evaluation of animal models of amphetamine psychosis. Brain research reviews, 11(2), 157–198.
  • Robinson, T. E., & Berridge, K. C. (1993). The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain research reviews, 18(3), 247–291.
  • Berridge, K. C., & Robinson, T. E. (1998). What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience?. Brain research reviews, 28(3), 309–369.
  • Berridge, K. C., & Robinson, T. E. (2003). Parsing reward. Trends in neurosciences, 26(9), 507–513.
  • Robinson, T. E., & Berridge, K. C. (2008). The incentive sensitization theory of addiction: some current issues. Philosophical Transactions of the Royal Society B: Biological Sciences, 363(1507), 3137–3146.

References

  1. ^ "Terry Robinson | U-M LSA Department of Psychology". lsa.umich.edu.
  2. ^ "Faculty – Tenured, Tenure Track | U-M LSA Department of Psychology". lsa.umich.edu.
  3. ^ a b "SSIB 2018 | Bonita Springs, Florida". www.ssib.org.
  4. ^ "Google Scholar Citations". accounts.google.com.
  5. ^ a b "Awards for Distinguished Scientific Contributions" (PDF).
  6. ^ a b "Top of the field".
  7. ^ a b "Board of Scientific Affairs (BSA): 2014 Annual Report".
  8. ^ a b "Awardees – EBPS". ebps.org.
  9. ^ a b "Terry E. Robinson Recipient of the 2014 APS William James Award | U-M LSA Department of Psychology". lsa.umich.edu.
  10. ^ a b c "Theory explaining addiction wins Grawemeyer psychology award – Grawemeyer Awards".
  11. ^ a b c "Terry E. Robinson to present Henry Russel Lecture March 5 | The University Record". record.umich.edu.
  12. ^ "Stanford University Names World's Top 2% Scientists, 2021 | U-M LSA Department of Psychology". lsa.umich.edu.
  13. ^ Michels, Kirsten (August 3, 2003). "Wanting and Liking for the Addict". APS Observer. 16 – via www.psychologicalscience.org.
  14. ^ a b "EPA Fellows | Eastern Psychological Association". www.easternpsychological.org.
  15. ^ "Catecholamines - Gordon Research Conferences". www.grc.org.
  16. ^ Kolb, B.; Gorny, G.; Li, Y.; Samaha, A. N.; Robinson, T. E. (2003). "Amphetamine or cocaine limits the ability of later experience to promote structural plasticity in the neocortex and nucleus accumbens | PNAS". Proceedings of the National Academy of Sciences of the United States of America. 100 (18): 10523–10528. Bibcode:2003PNAS..10010523K. doi:10.1073/pnas.1834271100. PMC 193594. PMID 12939407.
  17. ^ "Editorial board - Behavioural Brain Research | ScienceDirect.com by Elsevier". www.sciencedirect.com.
  18. ^ "Robinson Lab – Behavioral Neuroscience Lab in the Department of Psychology".
  19. ^ "Robinson to Speak on Motivation, Addiction". APS Observer. 27. April 11, 2014 – via www.psychologicalscience.org.
  20. ^ Robinson, Terry E; Berridge, Kent C (October 12, 2008). "The incentive sensitization theory of addiction: some current issues". Philosophical Transactions of the Royal Society B: Biological Sciences. 363 (1507): 3137–3146. doi:10.1098/rstb.2008.0093. PMC 2607325. PMID 18640920.
  21. ^ "Parsing reward: Trends in Neurosciences".
  22. ^ Berridge, Kent C; Robinson, Terry E; Aldridge, J Wayne (February 1, 2009). "Dissecting components of reward: 'liking', 'wanting', and learning". Current Opinion in Pharmacology. 9 (1): 65–73. doi:10.1016/j.coph.2008.12.014. PMC 2756052. PMID 19162544.
  23. ^ "Dopamine 'ups and downs' in addiction revisited: Trends in Neurosciences".
  24. ^ a b Robinson, Terry E.; Becker, Jill B.; Presty, Sharon K. (December 16, 1982). "Long-term facilitation of amphetamine-induced rotational behavior and striatal dopamine release produced by a single exposure to amphetamine: Sex differences". Brain Research. 253 (1): 231–241. doi:10.1016/0006-8993(82)90690-4. hdl:2027.42/23769. PMID 6891283. S2CID 15633797 – via ScienceDirect.
  25. ^ Robinson, Terry E.; Becker, Jill B. (June 1, 1986). "Enduring changes in brain and behavior produced by chronic amphetamine administration: A review and evaluation of animal models of amphetamine psychosis". Brain Research Reviews. 11 (2): 157–198. doi:10.1016/0165-0173(86)90002-0. hdl:2027.42/26144. S2CID 205048600 – via ScienceDirect.
  26. ^ Robinson, Terry E.; Jurson, Phillip A.; Bennett, Julie A.; Bentgen, Kris M. (October 18, 1988). "Persistent sensitization of dopamine neurotransmission in ventral striatum (nucleus accumbens) produced by prior experience with (+)-amphetamine: a microdialysis study in freely moving rats". Brain Research. 462 (2): 211–222. doi:10.1016/0006-8993(88)90549-5. hdl:2027.42/27094. PMID 2847849. S2CID 14393258 – via ScienceDirect.
  27. ^ Lin-Chu, Guan; Robinson, Terry E.; Becker, Jill B. (May 1, 1985). "Sensitization of rotational behavior produced by a single exposure to cocaine". Pharmacology Biochemistry and Behavior. 22 (5): 901–903. doi:10.1016/0091-3057(85)90545-3. hdl:2027.42/25693. PMID 3925466. S2CID 1078137 – via ScienceDirect.
  28. ^ Robinson, Terry E.; Angus, Amy L.; Becker, Jill B. (September 16, 1985). "Sensitization to stress: The enduring effects of prior stress on amphetamine-induced rotational behavior". Life Sciences. 37 (11): 1039–1042. doi:10.1016/0024-3205(85)90594-6. hdl:2027.42/25568. PMID 4041000 – via ScienceDirect.
  29. ^ Paulson, Pamela E.; Camp, Dianne M.; Robinson, Terry E. (April 1, 1991). "Time course of transient behavioral depression and persistent behavioral sensitization in relation to regional brain monoamine concentrations during amphetamine withdrawal in rats". Psychopharmacology. 103 (4): 480–492. doi:10.1007/BF02244248. PMC 1865099. PMID 2062986 – via Springer Link.
  30. ^ Berridge, K. C.; Venier, I. L.; Robinson, T. E. (February 23, 1989). "Taste reactivity analysis of 6-hydroxydopamine-induced aphagia: implications for arousal and anhedonia hypotheses of dopamine function". Behavioral Neuroscience. 103 (1): 36–45. doi:10.1037/0735-7044.103.1.36. PMID 2493791 – via PubMed.
  31. ^ Robinson, T. E.; Berridge, K. C. (November 23, 1993). "The neural basis of drug craving: an incentive-sensitization theory of addiction". Brain Research. Brain Research Reviews. 18 (3): 247–291. doi:10.1016/0165-0173(93)90013-p. hdl:2027.42/30601. PMID 8401595. S2CID 13471436 – via PubMed.
  32. ^ Yeung, Andy W. K.; Goto, Tazuko K.; Leung, W. Keung (November 23, 2017). "At the Leading Front of Neuroscience: A Bibliometric Study of the 100 Most-Cited Articles". Frontiers in Human Neuroscience. 11: 363. doi:10.3389/fnhum.2017.00363. PMC 5520389. PMID 28785211.
  33. ^ Valderrama Zurián, Juan Carlos; Bueno Cañigral, Francisco Jesús; Castelló Cogollos, Lourdes; Aleixandre-Benavent, Rafael (April 1, 2021). "The most 100 cited papers in addiction research on cannabis, heroin, cocaine and psychostimulants. A bibliometric cross-sectional analysis". Drug and Alcohol Dependence. 221: 108616. doi:10.1016/j.drugalcdep.2021.108616. PMID 33636599. S2CID 232064840 – via ScienceDirect.
  34. ^ Berridge, Kent C; Robinson, Terry E (December 1, 1998). "What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience?". Brain Research Reviews. 28 (3): 309–369. doi:10.1016/S0165-0173(98)00019-8. PMID 9858756 – via ScienceDirect.
  35. ^ Robinson, Terry E.; Berridge, Kent C. (August 23, 2000). "The psychology and neurobiology of addiction: an incentive–sensitization view". Addiction. 95 (8s2): 91–117. doi:10.1046/j.1360-0443.95.8s2.19.x. hdl:2027.42/75373. PMID 11002906 – via CrossRef.
  36. ^ Robinson, Terry E.; Berridge, Kent C. (February 23, 2003). "Addiction". Annual Review of Psychology. 54 (1): 25–53. doi:10.1146/annurev.psych.54.101601.145237. PMID 12185211 – via CrossRef.
  37. ^ Anagnostaras, Stephan G.; Robinson, Terry E. (December 23, 1996). "Sensitization to the psychomotor stimulant effects of amphetamine: Modulation by associative learning". Behavioral Neuroscience. 110 (6): 1397–1414. doi:10.1037/0735-7044.110.6.1397. PMID 8986341 – via CrossRef.
  38. ^ Badiani, Aldo; Oates, Matthew M.; Day, Heidi E. W.; Watson, Stanley J.; Akil, Huda; Robinson, Terry E. (December 15, 1998). "Amphetamine-Induced Behavior, Dopamine Release, and c-fos mRNA Expression: Modulation by Environmental Novelty". The Journal of Neuroscience. 18 (24): 10579–10593. doi:10.1523/JNEUROSCI.18-24-10579.1998. PMC 6793358. PMID 9852594.
  39. ^ Robinson, Terry E.; Browman, Kaitlin E.; Crombag, Hans S.; Badiani, Aldo (March 1, 1998). "Modulation of the Induction or Expression of Psychostimulant Sensitization by the Circumstances Surrounding Drug Administration". Neuroscience & Biobehavioral Reviews. 22 (2): 347–354. doi:10.1016/S0149-7634(97)00020-1. PMID 9579324. S2CID 20846702 – via ScienceDirect.
  40. ^ Samaha, Anne-Noël; Li, Yilin; Robinson, Terry E. (April 15, 2002). "The Rate of Intravenous Cocaine Administration Determines Susceptibility to Sensitization". Journal of Neuroscience. 22 (8): 3244–3250. doi:10.1523/JNEUROSCI.22-08-03244.2002. PMC 6757529. PMID 11943825 – via www.jneurosci.org.
  41. ^ Robinson, Terry E.; Kolb, Bryan (November 1, 1997). "Persistent Structural Modifications in Nucleus Accumbens and Prefrontal Cortex Neurons Produced by Previous Experience with Amphetamine". Journal of Neuroscience. 17 (21): 8491–8497. doi:10.1523/JNEUROSCI.17-21-08491.1997. PMC 6573726. PMID 9334421 – via www.jneurosci.org.
  42. ^ Robinson, Terry E.; Kolb, Bryan (May 23, 1999). "Alterations in the morphology of dendrites and dendritic spines in the nucleus accumbens and prefrontal cortex following repeated treatment with amphetamine or cocaine". European Journal of Neuroscience. 11 (5): 1598–1604. doi:10.1046/j.1460-9568.1999.00576.x. hdl:2027.42/75023. PMID 10215912. S2CID 14635277.
  43. ^ Robinson, Terry E.; Gorny, Grazyna; Mitton, Elizabeth; Kolb, Bryan (March 1, 2001). "Cocaine self-administration alters the morphology of dendrites and dendritic spines in the nucleus accumbens and neocortex". Synapse. 39 (3): 257–266. doi:10.1002/1098-2396(20010301)39:3<257::AID-SYN1007>3.0.CO;2-1. hdl:2027.42/34991. PMID 11169774. S2CID 10612862 – via CrossRef.
  44. ^ Kolb, Bryan; Gorny, Grazyna; Li, Yilin; Samaha, Anne-Noël; Robinson, Terry E. (September 2, 2003). "Amphetamine or cocaine limits the ability of later experience to promote structural plasticity in the neocortex and nucleus accumbens". Proceedings of the National Academy of Sciences. 100 (18): 10523–10528. Bibcode:2003PNAS..10010523K. doi:10.1073/pnas.1834271100. PMC 193594. PMID 12939407.
  45. ^ Robinson, Terry E.; Kolb, Bryan (January 1, 2004). "Structural plasticity associated with exposure to drugs of abuse". Neuropharmacology. 47: 33–46. doi:10.1016/j.neuropharm.2004.06.025. PMID 15464124. S2CID 1987897 – via ScienceDirect.
  46. ^ Hewer, Mariko (30 September 2014). "Different Roads, Same Reward". Aps Observer. 27.
  47. ^ Flagel, Shelly B.; Clark, Jeremy J.; Robinson, Terry E.; Mayo, Leah; Czuj, Alayna; Willuhn, Ingo; Akers, Christina A.; Clinton, Sarah M.; Phillips, Paul E. M.; Akil, Huda (January 23, 2011). "A selective role for dopamine in stimulus–reward learning". Nature. 469 (7328): 53–57. Bibcode:2011Natur.469...53F. doi:10.1038/nature09588. PMC 3058375. PMID 21150898.
  48. ^ Kawa, Alex B.; Bentzley, Brandon S.; Robinson, Terry E. (October 23, 2016). "Less is more: prolonged intermittent access cocaine self-administration produces incentive-sensitization and addiction-like behavior". Psychopharmacology. 233 (19–20): 3587–3602. doi:10.1007/s00213-016-4393-8. PMC 5023484. PMID 27481050.
  49. ^ Singer, Bryan F.; Fadanelli, Monica; Kawa, Alex B.; Robinson, Terry E. (January 3, 2018). "Are Cocaine-Seeking "Habits" Necessary for the Development of Addiction-Like Behavior in Rats?". The Journal of Neuroscience. 38 (1): 60–73. doi:10.1523/JNEUROSCI.2458-17.2017. PMC 5761437. PMID 29158359.
  50. ^ Kawa, Alex B.; Allain, Florence; Robinson, Terry E.; Samaha, Anne-Noël (April 1, 2019). "The transition to cocaine addiction: the importance of pharmacokinetics for preclinical models". Psychopharmacology. 236 (4): 1145–1157. doi:10.1007/s00213-019-5164-0. PMC 6592776. PMID 30820634 – via Springer Link.
  51. ^ "AAAS Members Elected as Fellows on 15 February 1988". Science. 240 (4853): 810–811. May 6, 1988. Bibcode:1988Sci...240..810.. doi:10.1126/science.240.4853.810 – via CrossRef.
  52. ^ "Distinguished alumnus Dr. Terry Robinson to receive Honorary Degree | UNews". www.ulethbridge.ca.
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