Comparison of the Effects of Bilateral Orbital Prefrontal Cortex Lesions and Amygdala Lesions on Emotional Responses in Rhesus Monkeys

Overview

Journal J Neurosci

Specialty Neurology

Date 2005 Sep 16

PMID 16162935

Citations 100

Authors

Alicia Izquierdo

Robin K Suda

Elisabeth A Murray

Affiliations

Soon will be listed here.

Abstract

The present study examines the effects of bilateral orbital prefrontal cortex (PFo) lesions on monkeys' emotional responses in two different contexts: in the presence of a rubber snake and in the presence of a human intruder. For comparison, we also assessed the responses of rhesus monkeys with selective amygdala lesions on these same tasks. Monkeys with PFo lesions, like those with amygdala lesions, displayed blunted emotional responses to the fake snake. Unlike monkeys with amygdala lesions, however, monkeys with PFo lesions displayed more mild aggression than controls in the presence of a human intruder. The findings support the idea that the PFo helps integrate sensory signals in the service of choosing among competing responses. In addition, they point to a divergence of the roles of the PFo and amygdala in responding to a social stimulus, the human intruder.

Citing Articles

Aberrant functional connectivity of amygdala subregions in temporal lobe epilepsy with ictal panic.

Zhang X, Chen X, Qu C, Fan L, Zheng J Neurol Sci. 2024; 46(1):381-391.

PMID: 39187672 DOI: 10.1007/s10072-024-07730-2.

Aspiration removal of orbitofrontal cortex disrupts cholinergic fibers of passage to anterior cingulate cortex in rhesus macaques.

Eldridge M, Mohanty A, Hines B, Kaskan P, Murray E Brain Struct Funct. 2024; 229(4):1011-1019.

PMID: 38502331 PMC: 11003915. DOI: 10.1007/s00429-024-02776-6.

Understanding the heterogeneity of anxiety using a translational neuroscience approach.

Drzewiecki C, Fox A Cogn Affect Behav Neurosci. 2024; 24(2):228-245.

PMID: 38356013 PMC: 11039504. DOI: 10.3758/s13415-024-01162-3.

Prefrontal influences on the function of the neural circuitry underlying anxious temperament in primates.

Kenwood M, Oler J, Tromp D, Fox A, Riedel M, Roseboom P Oxf Open Neurosci. 2023; 2.

PMID: 37583705 PMC: 10426770. DOI: 10.1093/oons/kvac016.

Morphological abnormalities in youth with bipolar disorder and their relationship to clinical characteristics.

Li W, Lei D, Tallman M, Welge J, Blom T, Fleck D J Affect Disord. 2023; 338:312-320.

PMID: 37301295 PMC: 10527418. DOI: 10.1016/j.jad.2023.05.070.

References

Rogers R, Everitt B, Baldacchino A, Blackshaw A, Swainson R, Wynne K . Dissociable deficits in the decision-making cognition of chronic amphetamine abusers, opiate abusers, patients with focal damage to prefrontal cortex, and tryptophan-depleted normal volunteers: evidence for monoaminergic mechanisms. Neuropsychopharmacology. 1999; 20(4):322-39. DOI: 10.1016/S0893-133X(98)00091-8. View

Bechara A, Damasio H, Damasio A, Lee G . Different contributions of the human amygdala and ventromedial prefrontal cortex to decision-making. J Neurosci. 1999; 19(13):5473-81. PMC: 6782338. View

Gallagher M, McMahan R, Schoenbaum G . Orbitofrontal cortex and representation of incentive value in associative learning. J Neurosci. 1999; 19(15):6610-4. PMC: 6782791. View

Meunier M, Bachevalier J, Murray E, Malkova L, Mishkin M . Effects of aspiration versus neurotoxic lesions of the amygdala on emotional responses in monkeys. Eur J Neurosci. 1999; 11(12):4403-18. DOI: 10.1046/j.1460-9568.1999.00854.x. View

Tremblay L, Schultz W . Modifications of reward expectation-related neuronal activity during learning in primate orbitofrontal cortex. J Neurophysiol. 2000; 83(4):1877-85. DOI: 10.1152/jn.2000.83.4.1877. View

Baxter M, Parker A, Lindner C, Izquierdo A, Murray E . Control of response selection by reinforcer value requires interaction of amygdala and orbital prefrontal cortex. J Neurosci. 2000; 20(11):4311-9. PMC: 6772657. View

Bechara A, Tranel D, Damasio H . Characterization of the decision-making deficit of patients with ventromedial prefrontal cortex lesions. Brain. 2000; 123 ( Pt 11):2189-202. DOI: 10.1093/brain/123.11.2189. View

Kalin N, Shelton S, Davidson R, Kelley A . The primate amygdala mediates acute fear but not the behavioral and physiological components of anxious temperament. J Neurosci. 2001; 21(6):2067-74. PMC: 6762619. View

Malkova L, Lex C, Mishkin M, Saunders R . MRI-Based evaluation of locus and extent of neurotoxic lesions in monkeys. Hippocampus. 2001; 11(4):361-70. DOI: 10.1002/hipo.1050. View

10.

Bussey T, Wise S, Murray E . The role of ventral and orbital prefrontal cortex in conditional visuomotor learning and strategy use in rhesus monkeys (Macaca mulatta). Behav Neurosci. 2001; 115(5):971-82. DOI: 10.1037//0735-7044.115.5.971. View

11.

Blair R . Neurocognitive models of aggression, the antisocial personality disorders, and psychopathy. J Neurol Neurosurg Psychiatry. 2001; 71(6):727-31. PMC: 1737625. DOI: 10.1136/jnnp.71.6.727. View

12.

Nemanic S, Alvarado M, Price R, Jackson E, Bachevalier J . Assessment of locus and extent of neurotoxic lesions in monkeys using neuroimaging techniques: a replication. J Neurosci Methods. 2002; 121(2):199-209. DOI: 10.1016/s0165-0270(02)00264-9. View

13.

Kheramin S, Body S, Mobini S, Ho M, Velazquez-Martinez D, Bradshaw C . Effects of quinolinic acid-induced lesions of the orbital prefrontal cortex on inter-temporal choice: a quantitative analysis. Psychopharmacology (Berl). 2002; 165(1):9-17. DOI: 10.1007/s00213-002-1228-6. View

14.

Fredrikson M, Furmark T . Amygdaloid regional cerebral blood flow and subjective fear during symptom provocation in anxiety disorders. Ann N Y Acad Sci. 2003; 985:341-7. DOI: 10.1111/j.1749-6632.2003.tb07092.x. View

15.

Nelson E, Shelton S, Kalin N . Individual differences in the responses of naïve rhesus monkeys to snakes. Emotion. 2003; 3(1):3-11. DOI: 10.1037/1528-3542.3.1.3. View

16.

Schoenbaum G, Setlow B, Saddoris M, Gallagher M . Encoding predicted outcome and acquired value in orbitofrontal cortex during cue sampling depends upon input from basolateral amygdala. Neuron. 2003; 39(5):855-67. DOI: 10.1016/s0896-6273(03)00474-4. View

17.

Wallis J, Miller E . Neuronal activity in primate dorsolateral and orbital prefrontal cortex during performance of a reward preference task. Eur J Neurosci. 2003; 18(7):2069-81. DOI: 10.1046/j.1460-9568.2003.02922.x. View

18.

Izquierdo A, Murray E . Combined unilateral lesions of the amygdala and orbital prefrontal cortex impair affective processing in rhesus monkeys. J Neurophysiol. 2004; 91(5):2023-39. DOI: 10.1152/jn.00968.2003. View

19.

Roesch M, Olson C . Neuronal activity related to reward value and motivation in primate frontal cortex. Science. 2004; 304(5668):307-10. DOI: 10.1126/science.1093223. View

20.

Holland P, Gallagher M . Amygdala-frontal interactions and reward expectancy. Curr Opin Neurobiol. 2004; 14(2):148-55. DOI: 10.1016/j.conb.2004.03.007. View