Uncoupling of behavioral and autonomic responses after lesions of the primate orbitofrontal cortex

Proceedings of the National Academy of Sciences of the United States of America

Volumn 105, Issue 28, 2008, Pages 9787-9792

  Reekie, Y L ^a   Braesicke, K ^a,b   Man, M S ^a,b   Roberts, A C ^a,b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Behavioral inhibition; Emotion; Reversal learning

Indexed keywords

ADAPTATION; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APPETITE; AROUSAL; ARTICLE; AUTISM; AUTONOMIC NERVOUS SYSTEM; BEHAVIOR; BRAIN DAMAGE; CARDIOVASCULAR SYSTEM; CONTROLLED STUDY; EMOTION; EMOTIONAL STRESS; MARMOSET; NONHUMAN; ORBITAL CORTEX; PRIORITY JOURNAL; REWARD; SCHIZOPHRENIA;

ANIMALS; AUTONOMIC NERVOUS SYSTEM; BEHAVIOR, ANIMAL; CALLITHRIX; CONDITIONING (PSYCHOLOGY); FRONTAL LOBE; HEMODYNAMICS; PREFRONTAL CORTEX; REWARD;

ANIMALIA; MARMOSETS; PRIMATES;

EID: 47749126184     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0800417105     Document Type: Article

References (55)

1. Butter CM, Mishkin M, Rosvold HE (1963) Conditioning and extinction of a food-rewarded response after selective ablations of frontal cortex in rhesus monkeys. Exp Neurol 7:65-75.
2. Iversen SD, Mishkin M (1970) Perseverative interference in monkeys following selective lesions of the inferior prefrontal convexity. Experimental Brain Res 11:376-386.
3. Butter CM (1969) Perseveration in extinction and in discrimination reversal tasks following selective frontal ablations in Macaca mulatta. Physiology and Behavior 4:163-171.
4. Jones B, Mishkin M (1972) Limbic lesions and the problem of stimulus-reinforcement associations. Exp Neurol 36:362-377.
5. Rolls ET, Hornak J, Wade D, McGrath J (1994) Emotion-related learning in patients with social and emotional changes associated with frontal lobe damage. J Neurol Neurosurg Psychiatry 57:1518-1524.
6. Dias R, Robbins TW, Roberts AC (1996) Dissociation in prefrontal cortex of affective and attentional shifts. Nature 380:69-72.
7. Chudasama Y, Robbins TW (2003) Dissociable contributions of the orbitofrontal and infralimbic cortex to Pavlovian autoshaping and discrimination reversal learning: Further evidence for the functional heterogeneity of the rodent frontal cortex. J Neurosci 23:8771-8780.
8. Fellows LK, Farah MJ (2003) Ventromedial frontal cortex mediates affective shifting in humans: Evidence from a reversal learning paradigm. Brain 126:1830-1837.
9. Izquierdo A, Suda RK, Murray EA (2004) Bilateral orbital prefrontal cortex lesions in rhesus monkeys disrupt choices guided by both reward value and reward contingency. J Neurosci 24:7540-7548.
10. Butter CM, McDonald JA, Snyder DR (1969) Orality, preference behavior, and reinforcement value of nonfood object in monkeys with orbital frontal lesions. Science 164:1306-1307.
11. Izquierdo A, Murray EA (2005) Opposing effects of amygdala and orbital prefrontal cortex lesions on the extinction of instrumental responding in macaque monkeys. Eur J Neurosci 22:2341-2346.
12. Pavlov IP (1927) Extinction of conditioned reflexes. Conditioned Reflexes (Oxford Univ Press, Oxford), pp 48-67.
13. Brutkowski S (1954) Effect of excision of the frontal lobes on salivary conditioned reflexes in dogs. Acta Physiol Pol 5:505-507.
14. Brutkowski S (1959) Effects of prefrontal ablations on salivation during the alimentary unconditioned reflex and after its cessation. Acta Biol Exp 19:281-290.
15. Auleytner B, Brutkowski S (1960) Effects of bilateral prefrontal lobectomy on the classical (type i) defensive conditioned reflexes and some other responses related to defensive behaviour in dogs. Acta Biol Exp 20:243-262.
16. Hall RE, Cornish K (1977) Role of the orbital cortex in cardiac dysfunction in unanesthetized rhesus monkey. Exp Neurol 56:289-297.
17. Barbas H (1995) Anatomic basis of cognitive-emotional interactions in the primate prefrontal cortex. Neurosci Biobehav Rev 19:499-510.
18. Öngür D, An X, Price JL (1998) Prefrontal cortical projections to the hypothalamus in macaque monkeys. J Comp Neurol 401:480-505.
19. Floyd NS, Price JL, Ferry AT, Keay KA, Bandler R (2000) Orbitomedial prefrontal cortical projections to distinct longitudinal columns of the periaqueductal gray in the rat. J Comp Neurol 422:556-578.
20. Barbas H, Saha S, Rempel-Clower N, Ghashghaei T (2003) Serial pathways from primate prefrontal cortex to autonomic areas may influence emotional expression. BMC Neurosci 4:25.
21. Holland PC (1977) Conditioned stimulus as a determinant of the form of the Pavlovian conditioned response. J Exp Psychol Anim Behav Process 3:77-104.
22. Roberts AC (2006) A componential analysis of the functions of primate orbitofrontal cortex. The Oribitofrontal Cortex, ed Zald DH, Rauch SL (Oxford Univ Press, Oxford), pp 237-264.
23. Bechara A, Damasio H, Damasio AR, Lee GP (1999) Different contributions of the human amygdala and ventromedial prefrontal cortex to decision-making. J Neurosci 19:5473-5481.
24. Morgan MA, LeDoux JE (1995) Differential Contribution of dorsal and ventral medial prefrontal cortex to the acquisition and extinction of conditioned fear in rats. Behav Neurosci 109:681-688.
25. Quirk GJ, Russo GK, Barron JL, Lebron K (2000) The role of ventromedial prefrontal cortex in the recovery of extinguished fear. J Neurosci 20:6225-6231.
26. Rhodes SE, Killcross S (2004) Lesions of rat infralimbic cortex enhance recovery and reinstatement of an appetitive Pavlovian response. Learn Mem 11:611-616.
27. Rhodes SE, Killcross AS (2007) Lesions of rat infralimbic cortex result in disrupted retardation but normal summation test performance following training on a Pavlovian conditioned inhibition procedure. Eur J Neurosci 26:2654-2660.
28. Jackson DC, et al. (2003) Now you feel it, now you don't: Frontal brain electrical asymmetry and individual differences in emotion regulation. Psychol Sci 14:612-617.
29. Tugade MM, Fredrickson BL (2004) Resilient individuals use positive emotions to bounce back from negative emotional experiences. J Pers Soc Psychol 86:320-333.
30. Saddoris MP, Gallagher M, Schoenbaum G (2005) Rapid associative encoding in basolateral amygdala depends on connections with orbitofrontal cortex. Neuron 46:321-331.
31. Izquierdo A, Murray EA (2007) Selective bilateral amygdala lesions in rhesus monkeys fail to disrupt object reversal learning. J Neurosci 27:1054-1062.
32. Stalnaker TA, Franz TM, Singh T, Schoenbaum G (2007) Basolateral amygdala lesions abolish orbitofrontal-dependent reversal impairments. Neuron 54:51-58.
33. Braesicke K, et al. (2005) Autonomic arousal in an appetitive context in primates: A behavioural and neural analysis. Eur J Neurosci 21:1733-1740.
34. Parkinson JA, Robbins TW, Everitt BJ (2000) Dissociable roles of the central and basolateral amygdala in appetitive emotional learning. Eur J Neurosci 12:405-413.
35. McDannald M, Kerfoot E, Gallagher M, Holland PC (2004) Amygdala central nucleus function is necessary for learning but not expression of conditioned visual orienting. Eur J Neurosci 20:240-248.
36. Groshek F, et al. (2005) Amygdala central nucleus function is necessary for learning, but not expression, of conditioned auditory orienting. Behav Neurosci 119:202-212.
37. Cardinal RN, et al. (2002) Effects of selective excitotoxic lesions of the nucleus accumbens core, anterior cingulate cortex, and central nucleus of the amygdala on autoshaping performance in rats. Behav Neurosci 116:553-567.
38. Han JS, McMahn RW, Holland P, Gallagher M (1997) The role of an amygdalanigrostriatal pathway in associative learning. J Neurosci 17:3913-3919.
39. An X, Bandler R, Ongur D, Price JL (1998) Prefrontal cortical projections to longitudinal columns in the midbrain periaqueductal gray in macaque monkeys. J Comp Neurol 401:455-479.
40. Craig AD (2002) How do you feel? Interoception: The sense of the physiological condition of the body. Nat Rev Neurosci 3:655-666.
41. Damasio A (2003) Feelings of emotion and the self. Ann NY Acad Sci 1001:253-261.
42. Nicotra A, Critchley HD, Mathias CJ, Dolan RJ (2006) Emotional and autonomic consequences of spinal cord injury explored using functional brain imaging. Brain 129:718-728.
43. Critchley HD, et al. (2007) Vagus nerve stimulation for treatment-resistant depression: behavioral and neural effects on encoding negative material. Psychosom Med 69:17-22.
44. Critchley HD, Wiens S, Rotshtein P, Ohman A, Dolan RJ (2004) Neural systems supporting interoceptive awareness. Nat Neurosci 7:189-195.
45. Aleman A, Kahn RS (2005) Strange feelings: Do amygdala abnormalities dysregulate the emotional brain in schizophrenia? Prog Neurobiol 77:283-298.
46. Williams LM, et al. (2007) Fronto-limbic and autonomic disjunctions to negative emotion distinguish schizophrenia subtypes. Psychiatry Res 155:29-44.
47. Hirstein W, Iversen P, Ramachandran VS (2001) Autonomic responses of autistic children to people and objects. Proc Biol Sci 268:1883-1888.
48. Baare WF, et al. (1999) Volumetric analysis of frontal lobe regions in schizophrenia: relation to cognitive function and symptomatology. Biol Psychiatry 45:1597-1605.
49. Bachevalier J, Loveland KA (2006) The orbitofrontal-amygdala circuit and self-regulation of social-emotional behavior in autism. Neurosci Biobehav Rev 30:97-117.
50. Konorski J (1967) Integrative Activity of the Brain (Chicago Univ Press, Chicago).
51. Holland PC (1984) Origins of behaviour in Pavlovian conditioning. The Psychology of Learning and Motivation. (Prentice-Hall, Englewood Cliffs, NJ).
52. Pears A, Parkinson JA, Hopewell L, Everitt BJ, Roberts AC (2003) Lesions of the orbitofrontal but not medial prefrontal cortex disrupt conditioned reinforcement in primates. J Neurosci 23:11189-11201.
53. Howell DC (2002) Graduate-Level Statistics for Psychology and Neuroscience: ANOVA in Practice, and Complex ANOVA Designs (Duxbury, Belmont, CA).
54. Cardinal R, Aitken MRF (2006) ANOVA for the Behavioural Sciences Researcher. (Lawrence Erlbaum, Mahwah, NJ).
55. Roberts AC, et al. (2007) Forebrain connectivity of the prefrontal cortex in the marmoset monkey (Callithrix jacchus): An anterograde and retrograde tract-tracing study. J Comp Neurol 502:86-112.