Using two distinct testing environments to assess decision-making skills in rhesus monkeys (Macaca mulatta) after selective amygdala, hippocampal or orbital frontal cortex lesions

C.J. Machado and J. Bachevalier

Neurobiology & Anatomy, University of Texas, Houston Health Science Center, Houston, U.S.A.

 

For both human [2] and non-human primates [1,3], the amygdala and orbital frontal cortex appear to be integral parts of a neural network responsible for advantageous decision-making. However, conclusions drawn from studies of human lesion patients are tenuous, due to the non-specific nature of their lesions. Furthermore, the role of the amygdala and orbital frontal cortex in non-human primate decision-making has never been assessed in a semi-naturalistic setting. Therefore, we compared the decision-making skills of sham-operated monkeys (SHAM, n = 6) to those of monkeys with selective lesions of either the amygdala (AMYG-ibotenic, n = 6), orbital frontal cortex (ORB-aspiration, n = 3, and ORB-ibotenic, n = 3) or hippocampal formation (HIPP-ibotenic, n = 6).

To measure decision-making skills, we examined baseline preference for foods and non-foods, as well as subjects' abilities to alter choice strategy when a highly preferred food is suddenly made less rewarding (via satiation). These variables were measured in two different experimental paradigms: (1) a two-alternative free choice task (TAFC), conducted in a Wisconsin General Testing Apparatus; and (2) a semi-naturalistic free foraging task (FF), conducted in a large rectangular enclosure. Preferences for food and non-food items were measured in each task, both pre- and post-surgery.

While none of the lesions altered subjects' preference for foods in the TAFC task, AMYG showed higher preference for foods post-surgery in the FF task, specifically for those that were least preferred by all animals prior to surgery (lemon, garlic and standard monkey chow; p < 0.05). Selection of non-food items was unaltered in SHAM and ORB, whereas HIPP and AMYG selected more non-food items after surgery (p < 0.05) in the TAFC task, though only HIPP showed this trend in the FF task (p = 0.06).

These results indicate that the amygdala and hippocampus are important for inhibiting the selection of items that normal animals typically avoid (non-foods and less palatable foods), regardless of context. To examine how amygdala, hippocampal and orbital frontal cortex lesions impact on subjects' abilities to flexibly alter choice strategies, we determined each animal's favourite food and allowed them to eat from a surplus of this food until they refused. Subjects were then retested in both TAFC and FF tasks. In both the TAFC and FF tasks, SHAM, AMYG and HIPP showed a decrease in their selection frequency for the satiated item (p values < 0.05), but ORB did not. Therefore, the orbital frontal cortex appears to modulate choice strategy when reward contingencies change, regardless of context.

Supported by: MH58846, HD35471 and T32 NS07467.

References

  1. Baxter, M.G.; Parker, A.; Lindner, C.C.; Izquierdo, A.D.; Murray, E.A. (2000). J Neurosci, 20, 4311-4319.
  2. Bechara, A.; Damasio, H.; Damasio, A.R.; Lee, G.P. (1999). J. Neurosci, 19(13), 5473 -54 81.
  3. Málková, L.; Gaffan, D.; Murray, E.A. (1997). J. Neurosci, 17, 6011-6020.


Paper presented at Measuring Behavior 2002 , 4th International Conference on Methods and Techniques in Behavioral Research, 27-30 August 2002, Amsterdam, The Netherlands

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