Discussion Questions for Bechara Paper

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Unformatted text preview: Discussion Questions for Bechara Paper 1. There were three individuals examined with brain injuries in this study. What were their brain injuries? 2. In the conditioning experiment what was the Conditioned stimui (hint, there were two experiments) Unconditioned stimulus Unconditioned response 3. How did individuals with damage to the amygdala respond to conditioned stimuli? L o 9 Monogr. 0, 1 (1984); .B. Keith, roceedings f the P 1 World agomorph onference, uelph, ntario, 2 C O G L to 16 August1979, K. Myersand C. D. Maclnnes, Eds. (Univ. f Guelph,Ontario, anada,1981), pp. o C a J 395-440; M. R. Vaughan nd L. B. Keith, . Wildl. T 45, 354 (1981);J. P. Finerty, hePopulaManage. tionEcology f CyclesinSmall ammalsYaleUniv. o M ( Press,New Haven,CT,1980). 2. C. J. Krebs, ikos52, 143 (1988);D. Chitty, an.J. O C Zool. 38, 99 (1960). Studies in animals have established that the amygdala is critical for emotional conreached its greatesthare densityin 1988 and reditioning (1), whereas several human and mained at a plateau until 1990. Controlarea 2 nonhuman primate studies have established reachedits peakdensityin 1990, and control rea1 a that the hippocampus and surrounding rereachedits peak in 1989. By the late peak in 1990 andduringhe declinephase,the control reaswere t a gions are necessary for establishing declaramuchmoresimilaro each otherin haredensities. t tive knowledge (2). Because of the rarity of 7. Theelectric ence was 10-stranded, .2 m inheight, 2 f and carried8600 V. Snow tracking f mammalian patients with selective bilateral damage reo its predators eetingthe fence illustrated effective- stricted to either the amygdala or hipm ness. We excluded mammalian redators irtually p v pocampus, the exact roles of these strucfrom January1989 onward.Our atcontinuously tures in emotional and declarative learning to use monofilament lineas a detertempts fishing rentto birdsof preywas largelyneffective ecause i b have not been established clearly for huice formation nd snow accumulationn the linesin a o mans (3). Here, we report the relative conwintercaused them to break or collapse to the tributions of the amygdala and hippocamWeused monofilament 10 haofthe predon ground. atorexclosurebut did not attemptto use it on the pus to emotional conditioning and to the combinationreatmentarea. The predatorexclot establishment of declarative knowledge in increase phase from 1986 to 1988. Control area 3 B A 3. C. J. Krebs, . S. Gilbert, . Boutin, . R. E.Sinclair, S J J. N. M.Smith, . Anim. col.55,963 (1986); . R. E. E A C J i Sinclair, . J. Krebs, . N. M.Smith,S. Boutin,bid. J A 57, 787 (1988); . N. M.Smith,C. J. Krebs, . R. E. R Sinclair, . Boonstra, bid., p. 269; C. J. Krebs,S. i B Boutin, . S. Gilbert, ecologia70, 194 (1985). O 4. E.A. DesyandG. O. Batzli, cology70, 411 (1989); E G. O. Batzli,nWildlife001: Populations, . R. Mci D 2 and R. H. Barrett, ds. (Elsevier, ondon, E L Cullough 1992),pp. 831-850. 5. Blockswerespaced at least 1 kmapart. ithinach W e c block,we surveyed heckerboard ridsof 20-by-20 g pointswith30.5-m spacingand used these gridsfor snowshoe hare livetrapping. wo experimentalrT a w eas wereprovided ithsupplemental (commerfood cial rabbitchow, 16% protein) ear round.In the y 1 summer f 1987, we built ne electricencearound o o f km2to excludemammalianredators, nd overthe a p following earwe covered10 ha withmonofilament y to reduce avianpredation. he monofilament as T w nevereffectivein preventing vianpredationnside a i the electric ences, andconsequently e didnot rely w f on it as a partof the treatment. nthe summerof I a f 1 1988, we built second electric ence around km2 to use for the combinedpredatorreduction-food addition reatment. e modified he design of the t W t electric ences in 1988 to makethemmoreeffective, f and since then they haveworkedeffectivelyo pret vent mammalian redators romentering he area. f t p The fences are permeable o snowshoe hares.We t could not replicate itherthe predator eduction r e o r the predator eduction-food ddition reatment er a t b cause of maintenance osts and the difficulty f o c e f w w maintaininglectric ences in the Yukon inter ith -45°C temperatures. hefences hadto be checked T every day duringwinter.From1976 to 1985, we t trappedharesinsix areaswithinhe mainstudyrew gionandfoundthattheir opulationrajectories ere p t verysimilar3).We thus have no reasonto suspect ( r strongareaeffectson the unreplicated redator ep ductionplots. 6. Weusedthreecontrol reasbutwerenotableto trap a hares in allof them everyyear.We have moredetaileddata on haresfromcontrolarea 1. The three control reas had quitedifferent istories uring he a h t d to sponded dramatically the added nutrientsC. J. ( Krebset al., unpublished ata). d 9. D. Tilman,n Long-Term tudies in Ecology,G. E. i S New Likens,Ed. (Springer-Verlag, York,1989), pp. 136-157; J. F. Franklin, pp. 3-19. ibid., 10. K.H. Pollock, . D. Nichols, . Brownie, . E. Hines, C J J Wildl. onogr. 07, 1 (1990);K.H. Pollock, . Wildl. J 1 M l w Manage.46, 752 (1982).Confidenceimits eretypically ± 15% of the populationestimates. Snow i c trackingnwinter onfirmed ensityestimates. d 11. L.B. Keith, urr. ammal. , 119 (1990). CM 2 12. S. Boutin ndC. J. Krebs, . Wildl. anage.50, 592 a J M K S C (1986); .H.Pollock, . R.Winterstein,. M.Bunck, P. D. Curtis,bid.53, 7 (1989). i 13. D. Hik,Wildl. es. 22, 115 (1995);S. Boutin t al., R e d unpublished ata. 14. M.O'Donoghue nd C. J. Krebs, . Anim.Ecol.61, a J 631 (1992);J. R. Caryand L.B. Keith, an.J. Zool. C 57, 375 (1979). 15. D. Hik,unpublished ata; R. Boonstraand G. R. d G 9 Singleton, en.Comp.Endocrinol.1,126 (1993). 16. R. Boonstra,Evol.Ecol. 8, 196 (1994); , D. i Hik,G. R. Singleton,n preparation. 17. In snowshoe hares, dispersaloccurs mainly n the i juvenile tage; adultharesare mostlysedentary[S. s 18. 19. 20. 21. B C A J Boutin, . S. Gilbert, . J. Krebs, . R. E.Sinclair, . N. M.Smith,Can.J. Zool.63, 106 (1985)]. rtificial A food addition auses immigration adulthares[S. c of Boutin,Oecologia62, 393 (1984)],and population a changes infood addition reasaremoreaffectedby movements hanare changes at othertreatment r t o control ites. s L.Oksanen,inPerspectives n PlantConsumption, o D.Tilman ndJ. Grace,Eds.(Academic ress, New a P O York,1990),pp. 445-474; S. D. Fretwell, ikos50, J J 291 (1987);S. R. Carpenter, . F. Kitchell, . R. Hodgson,Bioscience35, 634 (1985). L.B. Keith, ikos40, 385 (1983). O J. O. Wolff, col.Monogr. 0, 111 (1980). E 5 Wethankthe Natural ciences and Engineering eS R search Councilof Canadafor supporting his ret search programthrougha Collaborative pecial S t o A Projectgrant; he ArcticInstitute f North merica, o f L Universityf Calgary,orthe use of the Kluane ake research tation; ndallthe graduate tudents,techa s s w nicians,and undergraduates ho have assisted in this projectover the past 9 years, in particular . V Nams,S. Schweiger,and M.O'Donoghue. 6 March 995; accepted 20 June 1995 1 Double Dissociation of Conditioningand Declarative Knowledge Relative to the Amygdala and Hippocampus in Humans Antoine Bechara, Daniel Tranel,Hanna Damasio, RalphAdolphs, Charles Rockland,Antonio R. Damasio* A patient with selective bilateral damage to the amygdala did not acquire conditioned autonomic responses to visual or auditory stimuli but did acquire the declarative facts about which visual or auditory stimuli were paired with the unconditioned stimulus. By contrast, a patient with selective bilateral damage to the hippocampus failed to acquire the facts but did acquire the conditioning. Finally, a patient with bilateral damage to both amygdala and hippocampal formation acquired neither the conditioning nor the facts. These findings demonstrate a double dissociation of conditioning and declarative knowledge relative to the human amygdala and hippocampus. sures thus were mammalian redatorexclosures p andwerestillsubjectto avianpredation. 8. We fertilizedwo 1-km2blocksof forestwithcomt mercialertilizer.nMay1987, we used ammonium I f nitrate t 25 g/m2.InMay1988, we switchedto NPK a fertilizernd used 17.5 g of N/m2,5 g of P/m2,and a 2.5 g of K/m2. n1989,we used half hisamount, nd I t a inthe years1990 to 1994 we used the full mount s a a in 1988. Thefertilizer as spreadaeriallyndwe did w a c ground hecksto makesureitwas uniformly spread. We do not presentthe data hereto show the plant growthresponses, but all elementsof the florare- A. Bechara,D. Tranel, . Adolphs,Departmentf NeuR o o a rology,Division f Behavioral eurology nd Cognitive N o Neuroscience,Universityf IowaCollegeof Medicine, IowaCity,IA52242, USA. H. Damasio ndA. R. Damasio, epartmentf Neuroloa o D o a gy, Universityf IowaCollegeof Medicine, nd Salk InstituteforBiological tudies,LaJolla,CA92186, USA. S C. Rockland,Laboratory Informationnd Decision for a M Systems, MIT, ambridge, A02139, USA. C *Towhomcorrespondence houldbe addressed. s SCIENCE * VOL. 269 * 25 AUGUST 1995 humans. We studied three people with distinct brain lesions: SM046 had bilateral destruction of the amygdala, but bilaterally intact hippocampi; WC1606 had bilateral hippocampal damage, but bilaterally intact amygdalae; and RH1951 had bilateral damage to both hippocampus and amygdala (4) (Table 1 and Fig. 1). Four normal participants of comparable age and education served as controls. Two conditioning experiments were carried out. The first, a visual-auditory conditioning experiment, used monochrome slides as the conditioned stimuli (CS) and a startlingly loud sound (a boat horn delivered at 100 dB) as the unconditioned stimulus (US). The second, an auditory-auditory conditioning experiment, used computergenerated tones as the CS (the US was the same as in the visual-auditory experiment). In both experiments, the skin conductance response (SCR) was the dependent measure of autonomic response (5). Each conditioning experiment was performed three times in SM046 and twice in WC1606 and 1115 1115 ative learning in human, and thus offer insight on how the ensung and different formsof knowledgemay come togetherin the humanbrain. REFERENCESAND NOTES 1. J. E. LeDoux, in Handbook o Physiology: The Nervous System V, F. Plum, Ed. (American hysiological P Society, Bethesda, MD, 198,), pp. 419-459; J. E. LeDoux, Sci. Am. 270, 50 (,une 1994); M. Davis, Annu. Rev. Neurosci. 15, 353(1992); Trends Neurosci. 17, 208 (1994). 2. M. Mishkinand E. A. Murray, urr. Opin. Neurobiol. o 4, 200 (1994); L. R. Squire and S. Zola-Morgan, Science 253, 1380 (1991). 3. S. Zola-Morgan, L. R. Squire,D. G. Amaral,J. Neu4. ParticipantSM046 has bilateral amygdala damage because of Urbach-Wiethe disease. Detailed information pertainingto her neuropsychological profile, her neuroanatomicalstatus, and facts about her daily life(especially with regard to impairmentsin emotional reactivity)is published [R. Adolphs, D. Tranel, H. Damasio, A. Damasio, Nature 372, 669 (1994); R. Adolphs, D. Tranel, H. Damasio, A. R. Damasio, J. Neurosci., in press]. In brief, she has low average intellect and normal anterograde declarative memory, as measured by conventional procedures (Table 1). Although the exact point at which SM046 acquired her amygdala damage is not clear, the literature on Urbach-Wiethe disease and reports of SM046's childhood suggest that the neurological symptoms resulting from the disease were progressively acquired throughout late childhood and adolescence. In her daily life, SM046 has a history of inadequate decision-making and inappropriate social behavior. WC1606 has bilateral hippocampal damage. Fouryears before our experiments, he suffered a series of cardiac arrests and ventricularfibrillation, which produced severe ischemia-anoxia and consequent bilateralhippocampal injury see Fig. 1). ( He was left with a severe anterograde declarative memory impairment. He has low average intellect (Table 1). RH1951 has bilateraldamage to both the hippocampus and amygdala because of herpes simplex encephalitis, suffered 14 years before our experiments. The disease produced bilateral medial temporal lobe lesions and a severe impairment in anterograde declarative memory. His intellectual abilities remain well above average (Table 1). Based on (i) review of the academic and occupational histories of the patients, (ii)multiple assessments over 5. 6. 7. 8. several years, which indicate stable intellectualfunctioning, and (iii)lack of significant "scatter" among the various subsets from the WAIS-R(16), there is no indicationof general intellectualdeteriorationinthese patients. The fact that SM046 and WC1606 are wellmatched in intelligence quotient (IQ),but have different conditioning and declarative learning outcomes, argues against the possibilitythat intellectualfactors could account for our findings. Procedures of SCR recordings have been described in detail elsewhere [D. Tranel and H. Damasio, Psychophysiology 31, 427 (1994)]. Allparticipantsgave informed consent before participation in the experiments. After electrodes were attached, each participantwas seated in a comfortable chair, 0.45 m in front of the screens of a Caramate 4000 slide projector and of a computer for generating tones. The participant was asked to relax, to remain silent, and to attend to the color of the slides appearing on the screen. No motor or verbal response was to be given. Each slide was shown for 2 s, and the interval between two consecutive slides was between 10 and 20 s. The intertrialntervalwas i determined by the status of the electrodermal activity. A new slide was not presented if the participant was generating, or was in the steep recovery limb, of an SCR. The auditory-auditoryconditioning procedure was identical to the visual-auditoryprocedure, except that computer-generated tones were used instead of color slides. Each tone was presented for 2 s, and the intervalbetween two consecutive tones was 10to 20s. In the conditioning phase, the sequence of blue slides followed by the US, blue slides not followed by the US, and unpaired slides was as follows: (B-US)R-(B-no US)-R-(B-US)-R-R-(B-US)-R-(B-no US)-GR-(B-US)-Y-R-(B-no US)-(B-US)-R-G-(B-no US)-GR-(B-no US)-G-(B-US)-(B-no US) (where B, blue; G, green; R, red; and Y, yellow). Inauditory-auditory onditioning, the same format of c questions was used, but because it was difficultto give a verbal description of the computer tones, six tones were replayed and the participantwas asked to identifythe familiartones as well as the tone followed by the horn. To quantify each participant's abilityto acquire these specific facts about the experiment, we ascribed a maximum score of 4 if all answers were correct. Because the most significant fact in the conditioning experiment was to learn that the blue slide (or the one computer tone) was followed by the horn, a correct answer to this question was ascribed a score of 2.5. Any answer to this question that included more than one color (ortone), or a color other than blue (or other than the specific tone paired with the horn), resulted in a score of 0. Each of the remainingthree questions was ascribed a score of 0.5 for a correct answer, and a score of 0 for an incorrect one. Participants were asked to declare their knowledge, and they were not requiredto guess an answer or to respond in a forced choice format. All participants answered all the questions. 9. D. Tranel and B. T. Hyman, Arch. Neurol. 47, 349 (1 990). 10. D. Tranel and H. Damasio, Neuropsychologia 27, 381 (1989); G. P. Lee et al., Neuropsychiat. Neuropsychol. Behav. Neurol. 1, 1 19 (1988). 11. In follow-up experiments, we have found that some patients, though not all, with unilateral amygdala damage resultingfrom rightor left temporal lobectomies failed to acquire conditioned SCRs. These findings are consistent with a recent report [K.S. LeBar, E. A. Phelps, J. E. LeDoux, Soc. Neurosci. Abstr. 20, 360 (1994); K. S. LeBar, J. E. LeDoux, D. D. Spencer, E. A. Phelps, J. Neurosci., in press] that unilateral temporal lobectomies may produce impaired fear conditioning. 12. G. W. Van Hoesen, Ann. N.Y. Acad. Sci. 444, 97 (1985); D. G. Amaral, in Handbook of Physiology: The Nervous System V, F. Plum, Ed. (American Physiological Society, Bethesda, MD, 1987), pp. 211-294. 13. F. K. D. Nahm, D. Tranel, H. Damasio, A. R. Damasio, Neuropsychologia 31, 727 (1993). 14. A. R. Damasio, Descartes' Error:Emotion, Reason, and the Human Brain (Grosset/Putnam, New York, 1994). 15. R. G. Phillips and J. E. LeDoux, Behav. Neurosci. 106, 274 (1992); J. J. Kim and M. S. Fanselow, Science 256, 675 (1992); R. J. McDonald and N. M. White, Behav. Neurosci. 107, 3 (1993); J. J. Kim, R. A. Rison, M. S. Fanselow, ibid., p. 1093. 16. D. Wechsler, Manual for the Wechsler Adult Intelligence Scale-Revised (New York Psychological Corporation, New York, 1991); Manual for the Wechsler Memory Scale-Revised (New York Psychological Corporation, New York, 1987). 17. H. Damasio and R. Frank, Arch. Neurol. 49, 137 (1992). 18. T. W. Berger and W. B. Orr,Behav. BrainRes. 8, 49 (1983). 19. Supported by the National Institute of Neurological Disease and Stroke (grant P01 NS19632), the James S. McDonnell Foundation, and the Medical Research Council (Canada). R.A. is a BurroughsWellcome Fund Fellow of the LifeSciences Research Foundation. 20 March 1995; accepted 24 July 1995 AAAS-Newcomb Cleveland The AAAS-Newcomb Cleveland Prize is awarded to the author of an outstanding paper published in Science. The value of the prize is $5000; the winner also receives a bronze medal. The currentcompetition period began with the 2 June 1995 issue and ends with the issue of 31 May 1996. Reports, Research Articles, and Articles thatinclude original research data, theories, or syntheses and are fundamentalcontributions to basic knowledge or technical achievements of farreaching consequence are eligible for consideration for the prize. The paper must be a first-time publication of the author's own work. Reference to pertinentearlierwork by the authormay be included to give perspective. Prize To Be Awarded for a Report, Research Article, or an Article Published in Science Throughout the competition period, readers are invited to nominate papers appearingin the Reports, Research Articles, or Articles sections. Nominations must be typed, and the following informationprovided: the title of the paper, issue in which it was published, author's name, and a brief statement of justification for nomination. Nominations should be submittedto the AAASNewcomb Cleveland Prize, AAAS, Room 924, 1333 H Street, NW, Washington, DC 20005, and must be received on or before 30 June 1996. Final selectionwill rest with a panel of diss tinguished cientists appointed by the editor-in-chief of Science. The award will be presented at the 1997 AAAS annual meeting. In cases of multiple authorship, the prize will be divided equally between or among the authors. 1118 SCIENCE * VOL. 269 * 25 AUGUST 1995 L o 9 Monogr. 0, 1 (1984); .B. Keith, roceedings f the P 1 World agomorph onference, uelph, ntario, 2 C O G L to 16 August1979, K. Myersand C. D. Maclnnes, Eds. (Univ. f Guelph,Ontario, anada,1981), pp. o C a J 395-440; M. R. Vaughan nd L. B. Keith, . Wildl. T 45, 354 (1981);J. P. Finerty, hePopulaManage. tionEcology f CyclesinSmall ammalsYaleUniv. o M ( Press,New Haven,CT,1980). 2. C. J. Krebs, ikos52, 143 (1988);D. Chitty, an.J. O C Zool. 38, 99 (1960). Studies in animals have established that the amygdala is critical for emotional conreached its greatesthare densityin 1988 and reditioning (1), whereas several human and mained at a plateau until 1990. Controlarea 2 nonhuman primate studies have established reachedits peakdensityin 1990, and control rea1 a that the hippocampus and surrounding rereachedits peak in 1989. By the late peak in 1990 andduringhe declinephase,the control reaswere t a gions are necessary for establishing declaramuchmoresimilaro each otherin haredensities. t tive knowledge (2). Because of the rarity of 7. Theelectric ence was 10-stranded, .2 m inheight, 2 f and carried8600 V. Snow tracking f mammalian patients with selective bilateral damage reo its predators eetingthe fence illustrated effective- stricted to either the amygdala or hipm ness. We excluded mammalian redators irtually p v pocampus, the exact roles of these strucfrom January1989 onward.Our atcontinuously tures in emotional and declarative learning to use monofilament lineas a detertempts fishing rentto birdsof preywas largelyneffective ecause i b have not been established clearly for huice formation nd snow accumulationn the linesin a o mans (3). Here, we report the relative conwintercaused them to break or collapse to the tributions of the amygdala and hippocamWeused monofilament 10 haofthe predon ground. atorexclosurebut did not attemptto use it on the pus to emotional conditioning and to the combinationreatmentarea. The predatorexclot establishment of declarative knowledge in increase phase from 1986 to 1988. Control area 3 B A 3. C. J. Krebs, . S. Gilbert, . Boutin, . R. E.Sinclair, S J J. N. M.Smith, . Anim. col.55,963 (1986); . R. E. E A C J i Sinclair, . J. Krebs, . N. M.Smith,S. Boutin,bid. J A 57, 787 (1988); . N. M.Smith,C. J. Krebs, . R. E. R Sinclair, . Boonstra, bid., p. 269; C. J. Krebs,S. i B Boutin, . S. Gilbert, ecologia70, 194 (1985). O 4. E.A. DesyandG. O. Batzli, cology70, 411 (1989); E G. O. Batzli,nWildlife001: Populations, . R. Mci D 2 and R. H. Barrett, ds. (Elsevier, ondon, E L Cullough 1992),pp. 831-850. 5. Blockswerespaced at least 1 kmapart. ithinach W e c block,we surveyed heckerboard ridsof 20-by-20 g pointswith30.5-m spacingand used these gridsfor snowshoe hare livetrapping. wo experimentalrT a w eas wereprovided ithsupplemental (commerfood cial rabbitchow, 16% protein) ear round.In the y 1 summer f 1987, we built ne electricencearound o o f km2to excludemammalianredators, nd overthe a p following earwe covered10 ha withmonofilament y to reduce avianpredation. he monofilament as T w nevereffectivein preventing vianpredationnside a i the electric ences, andconsequently e didnot rely w f on it as a partof the treatment. nthe summerof I a f 1 1988, we built second electric ence around km2 to use for the combinedpredatorreduction-food addition reatment. e modified he design of the t W t electric ences in 1988 to makethemmoreeffective, f and since then they haveworkedeffectivelyo pret vent mammalian redators romentering he area. f t p The fences are permeable o snowshoe hares.We t could not replicate itherthe predator eduction r e o r the predator eduction-food ddition reatment er a t b cause of maintenance osts and the difficulty f o c e f w w maintaininglectric ences in the Yukon inter ith -45°C temperatures. hefences hadto be checked T every day duringwinter.From1976 to 1985, we t trappedharesinsix areaswithinhe mainstudyrew gionandfoundthattheir opulationrajectories ere p t verysimilar3).We thus have no reasonto suspect ( r strongareaeffectson the unreplicated redator ep ductionplots. 6. Weusedthreecontrol reasbutwerenotableto trap a hares in allof them everyyear.We have moredetaileddata on haresfromcontrolarea 1. The three control reas had quitedifferent istories uring he a h t d to sponded dramatically the added nutrientsC. J. ( Krebset al., unpublished ata). d 9. D. Tilman,n Long-Term tudies in Ecology,G. E. i S New Likens,Ed. (Springer-Verlag, York,1989), pp. 136-157; J. F. Franklin, pp. 3-19. ibid., 10. K.H. Pollock, . D. Nichols, . Brownie, . E. Hines, C J J Wildl. onogr. 07, 1 (1990);K.H. Pollock, . Wildl. J 1 M l w Manage.46, 752 (1982).Confidenceimits eretypically ± 15% of the populationestimates. Snow i c trackingnwinter onfirmed ensityestimates. d 11. L.B. Keith, urr. ammal. , 119 (1990). CM 2 12. S. Boutin ndC. J. Krebs, . Wildl. anage.50, 592 a J M K S C (1986); .H.Pollock, . R.Winterstein,. M.Bunck, P. D. Curtis,bid.53, 7 (1989). i 13. D. Hik,Wildl. es. 22, 115 (1995);S. Boutin t al., R e d unpublished ata. 14. M.O'Donoghue nd C. J. Krebs, . Anim.Ecol.61, a J 631 (1992);J. R. Caryand L.B. Keith, an.J. Zool. C 57, 375 (1979). 15. D. Hik,unpublished ata; R. Boonstraand G. R. d G 9 Singleton, en.Comp.Endocrinol.1,126 (1993). 16. R. Boonstra,Evol.Ecol. 8, 196 (1994); , D. i Hik,G. R. Singleton,n preparation. 17. In snowshoe hares, dispersaloccurs mainly n the i juvenile tage; adultharesare mostlysedentary[S. s 18. 19. 20. 21. B C A J Boutin, . S. Gilbert, . J. Krebs, . R. E.Sinclair, . N. M.Smith,Can.J. Zool.63, 106 (1985)]. rtificial A food addition auses immigration adulthares[S. c of Boutin,Oecologia62, 393 (1984)],and population a changes infood addition reasaremoreaffectedby movements hanare changes at othertreatment r t o control ites. s L.Oksanen,inPerspectives n PlantConsumption, o D.Tilman ndJ. Grace,Eds.(Academic ress, New a P O York,1990),pp. 445-474; S. D. Fretwell, ikos50, J J 291 (1987);S. R. Carpenter, . F. Kitchell, . R. Hodgson,Bioscience35, 634 (1985). L.B. Keith, ikos40, 385 (1983). O J. O. Wolff, col.Monogr. 0, 111 (1980). E 5 Wethankthe Natural ciences and Engineering eS R search Councilof Canadafor supporting his ret search programthrougha Collaborative pecial S t o A Projectgrant; he ArcticInstitute f North merica, o f L Universityf Calgary,orthe use of the Kluane ake research tation; ndallthe graduate tudents,techa s s w nicians,and undergraduates ho have assisted in this projectover the past 9 years, in particular . V Nams,S. Schweiger,and M.O'Donoghue. 6 March 995; accepted 20 June 1995 1 Double Dissociation of Conditioningand Declarative Knowledge Relative to the Amygdala and Hippocampus in Humans Antoine Bechara, Daniel Tranel,Hanna Damasio, RalphAdolphs, Charles Rockland,Antonio R. Damasio* A patient with selective bilateral damage to the amygdala did not acquire conditioned autonomic responses to visual or auditory stimuli but did acquire the declarative facts about which visual or auditory stimuli were paired with the unconditioned stimulus. By contrast, a patient with selective bilateral damage to the hippocampus failed to acquire the facts but did acquire the conditioning. Finally, a patient with bilateral damage to both amygdala and hippocampal formation acquired neither the conditioning nor the facts. These findings demonstrate a double dissociation of conditioning and declarative knowledge relative to the human amygdala and hippocampus. sures thus were mammalian redatorexclosures p andwerestillsubjectto avianpredation. 8. We fertilizedwo 1-km2blocksof forestwithcomt mercialertilizer.nMay1987, we used ammonium I f nitrate t 25 g/m2.InMay1988, we switchedto NPK a fertilizernd used 17.5 g of N/m2,5 g of P/m2,and a 2.5 g of K/m2. n1989,we used half hisamount, nd I t a inthe years1990 to 1994 we used the full mount s a a in 1988. Thefertilizer as spreadaeriallyndwe did w a c ground hecksto makesureitwas uniformly spread. We do not presentthe data hereto show the plant growthresponses, but all elementsof the florare- A. Bechara,D. Tranel, . Adolphs,Departmentf NeuR o o a rology,Division f Behavioral eurology nd Cognitive N o Neuroscience,Universityf IowaCollegeof Medicine, IowaCity,IA52242, USA. H. Damasio ndA. R. Damasio, epartmentf Neuroloa o D o a gy, Universityf IowaCollegeof Medicine, nd Salk InstituteforBiological tudies,LaJolla,CA92186, USA. S C. Rockland,Laboratory Informationnd Decision for a M Systems, MIT, ambridge, A02139, USA. C *Towhomcorrespondence houldbe addressed. s SCIENCE * VOL. 269 * 25 AUGUST 1995 humans. We studied three people with distinct brain lesions: SM046 had bilateral destruction of the amygdala, but bilaterally intact hippocampi; WC1606 had bilateral hippocampal damage, but bilaterally intact amygdalae; and RH1951 had bilateral damage to both hippocampus and amygdala (4) (Table 1 and Fig. 1). Four normal participants of comparable age and education served as controls. Two conditioning experiments were carried out. The first, a visual-auditory conditioning experiment, used monochrome slides as the conditioned stimuli (CS) and a startlingly loud sound (a boat horn delivered at 100 dB) as the unconditioned stimulus (US). The second, an auditory-auditory conditioning experiment, used computergenerated tones as the CS (the US was the same as in the visual-auditory experiment). In both experiments, the skin conductance response (SCR) was the dependent measure of autonomic response (5). Each conditioning experiment was performed three times in SM046 and twice in WC1606 and 1115 1115 ative learning in human, and thus offer insight on how the ensung and different formsof knowledgemay come togetherin the humanbrain. REFERENCESAND NOTES 1. J. E. LeDoux, in Handbook o Physiology: The Nervous System V, F. Plum, Ed. (American hysiological P Society, Bethesda, MD, 198,), pp. 419-459; J. E. LeDoux, Sci. Am. 270, 50 (,une 1994); M. Davis, Annu. Rev. Neurosci. 15, 353(1992); Trends Neurosci. 17, 208 (1994). 2. M. Mishkinand E. A. Murray, urr. Opin. Neurobiol. o 4, 200 (1994); L. R. Squire and S. Zola-Morgan, Science 253, 1380 (1991). 3. S. Zola-Morgan, L. R. Squire,D. G. Amaral,J. Neu4. ParticipantSM046 has bilateral amygdala damage because of Urbach-Wiethe disease. Detailed information pertainingto her neuropsychological profile, her neuroanatomicalstatus, and facts about her daily life(especially with regard to impairmentsin emotional reactivity)is published [R. Adolphs, D. Tranel, H. Damasio, A. Damasio, Nature 372, 669 (1994); R. Adolphs, D. Tranel, H. Damasio, A. R. Damasio, J. Neurosci., in press]. In brief, she has low average intellect and normal anterograde declarative memory, as measured by conventional procedures (Table 1). Although the exact point at which SM046 acquired her amygdala damage is not clear, the literature on Urbach-Wiethe disease and reports of SM046's childhood suggest that the neurological symptoms resulting from the disease were progressively acquired throughout late childhood and adolescence. In her daily life, SM046 has a history of inadequate decision-making and inappropriate social behavior. WC1606 has bilateral hippocampal damage. Fouryears before our experiments, he suffered a series of cardiac arrests and ventricularfibrillation, which produced severe ischemia-anoxia and consequent bilateralhippocampal injury see Fig. 1). ( He was left with a severe anterograde declarative memory impairment. He has low average intellect (Table 1). RH1951 has bilateraldamage to both the hippocampus and amygdala because of herpes simplex encephalitis, suffered 14 years before our experiments. The disease produced bilateral medial temporal lobe lesions and a severe impairment in anterograde declarative memory. His intellectual abilities remain well above average (Table 1). Based on (i) review of the academic and occupational histories of the patients, (ii)multiple assessments over 5. 6. 7. 8. several years, which indicate stable intellectualfunctioning, and (iii)lack of significant "scatter" among the various subsets from the WAIS-R(16), there is no indicationof general intellectualdeteriorationinthese patients. The fact that SM046 and WC1606 are wellmatched in intelligence quotient (IQ),but have different conditioning and declarative learning outcomes, argues against the possibilitythat intellectualfactors could account for our findings. Procedures of SCR recordings have been described in detail elsewhere [D. Tranel and H. Damasio, Psychophysiology 31, 427 (1994)]. Allparticipantsgave informed consent before participation in the experiments. After electrodes were attached, each participantwas seated in a comfortable chair, 0.45 m in front of the screens of a Caramate 4000 slide projector and of a computer for generating tones. The participant was asked to relax, to remain silent, and to attend to the color of the slides appearing on the screen. No motor or verbal response was to be given. Each slide was shown for 2 s, and the interval between two consecutive slides was between 10 and 20 s. The intertrialntervalwas i determined by the status of the electrodermal activity. A new slide was not presented if the participant was generating, or was in the steep recovery limb, of an SCR. The auditory-auditoryconditioning procedure was identical to the visual-auditoryprocedure, except that computer-generated tones were used instead of color slides. Each tone was presented for 2 s, and the intervalbetween two consecutive tones was 10to 20s. In the conditioning phase, the sequence of blue slides followed by the US, blue slides not followed by the US, and unpaired slides was as follows: (B-US)R-(B-no US)-R-(B-US)-R-R-(B-US)-R-(B-no US)-GR-(B-US)-Y-R-(B-no US)-(B-US)-R-G-(B-no US)-GR-(B-no US)-G-(B-US)-(B-no US) (where B, blue; G, green; R, red; and Y, yellow). Inauditory-auditory onditioning, the same format of c questions was used, but because it was difficultto give a verbal description of the computer tones, six tones were replayed and the participantwas asked to identifythe familiartones as well as the tone followed by the horn. To quantify each participant's abilityto acquire these specific facts about the experiment, we ascribed a maximum score of 4 if all answers were correct. Because the most significant fact in the conditioning experiment was to learn that the blue slide (or the one computer tone) was followed by the horn, a correct answer to this question was ascribed a score of 2.5. Any answer to this question that included more than one color (ortone), or a color other than blue (or other than the specific tone paired with the horn), resulted in a score of 0. Each of the remainingthree questions was ascribed a score of 0.5 for a correct answer, and a score of 0 for an incorrect one. Participants were asked to declare their knowledge, and they were not requiredto guess an answer or to respond in a forced choice format. All participants answered all the questions. 9. D. Tranel and B. T. Hyman, Arch. Neurol. 47, 349 (1 990). 10. D. Tranel and H. Damasio, Neuropsychologia 27, 381 (1989); G. P. Lee et al., Neuropsychiat. Neuropsychol. Behav. Neurol. 1, 1 19 (1988). 11. In follow-up experiments, we have found that some patients, though not all, with unilateral amygdala damage resultingfrom rightor left temporal lobectomies failed to acquire conditioned SCRs. These findings are consistent with a recent report [K.S. LeBar, E. A. Phelps, J. E. LeDoux, Soc. Neurosci. Abstr. 20, 360 (1994); K. S. LeBar, J. E. LeDoux, D. D. Spencer, E. A. Phelps, J. Neurosci., in press] that unilateral temporal lobectomies may produce impaired fear conditioning. 12. G. W. Van Hoesen, Ann. N.Y. Acad. Sci. 444, 97 (1985); D. G. Amaral, in Handbook of Physiology: The Nervous System V, F. Plum, Ed. (American Physiological Society, Bethesda, MD, 1987), pp. 211-294. 13. F. K. D. Nahm, D. Tranel, H. Damasio, A. R. Damasio, Neuropsychologia 31, 727 (1993). 14. A. R. Damasio, Descartes' Error:Emotion, Reason, and the Human Brain (Grosset/Putnam, New York, 1994). 15. R. G. Phillips and J. E. LeDoux, Behav. Neurosci. 106, 274 (1992); J. J. Kim and M. S. Fanselow, Science 256, 675 (1992); R. J. McDonald and N. M. White, Behav. Neurosci. 107, 3 (1993); J. J. Kim, R. A. Rison, M. S. Fanselow, ibid., p. 1093. 16. D. Wechsler, Manual for the Wechsler Adult Intelligence Scale-Revised (New York Psychological Corporation, New York, 1991); Manual for the Wechsler Memory Scale-Revised (New York Psychological Corporation, New York, 1987). 17. H. Damasio and R. Frank, Arch. Neurol. 49, 137 (1992). 18. T. W. Berger and W. B. Orr,Behav. BrainRes. 8, 49 (1983). 19. Supported by the National Institute of Neurological Disease and Stroke (grant P01 NS19632), the James S. McDonnell Foundation, and the Medical Research Council (Canada). R.A. is a BurroughsWellcome Fund Fellow of the LifeSciences Research Foundation. 20 March 1995; accepted 24 July 1995 AAAS-Newcomb Cleveland The AAAS-Newcomb Cleveland Prize is awarded to the author of an outstanding paper published in Science. The value of the prize is $5000; the winner also receives a bronze medal. The currentcompetition period began with the 2 June 1995 issue and ends with the issue of 31 May 1996. Reports, Research Articles, and Articles thatinclude original research data, theories, or syntheses and are fundamentalcontributions to basic knowledge or technical achievements of farreaching consequence are eligible for consideration for the prize. The paper must be a first-time publication of the author's own work. Reference to pertinentearlierwork by the authormay be included to give perspective. Prize To Be Awarded for a Report, Research Article, or an Article Published in Science Throughout the competition period, readers are invited to nominate papers appearingin the Reports, Research Articles, or Articles sections. Nominations must be typed, and the following informationprovided: the title of the paper, issue in which it was published, author's name, and a brief statement of justification for nomination. Nominations should be submittedto the AAASNewcomb Cleveland Prize, AAAS, Room 924, 1333 H Street, NW, Washington, DC 20005, and must be received on or before 30 June 1996. Final selectionwill rest with a panel of diss tinguished cientists appointed by the editor-in-chief of Science. The award will be presented at the 1997 AAAS annual meeting. In cases of multiple authorship, the prize will be divided equally between or among the authors. 1118 SCIENCE * VOL. 269 * 25 AUGUST 1995 ...
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