The Journal of Neuroscience, April 1, 2000, 20(7):2649-2656
Impaired Preference Conditioning after Anterior Temporal Lobe
Resection in Humans
Ingrid S.
Johnsrude1,
Adrian M.
Owen1,
Norman M.
White2,
W. Vivienne
Zhao2, and
Veronique
Bohbot3
1 Medical Research Council Cognition and Brain Sciences
Unit, Cambridge, CB2 2EF United Kingdom, 2 Department
of Psychology, and 3 Brain Imaging Centre, Montreal
Neurological Institute, McGill University, Montreal, Quebec H3A 2T5,
Canada
Research with animals suggests that structures within the
amygdaloid nuclear complex (ANC) are critical for acquiring
associations between rewarding events and neutral stimuli, a form of
conditioning often manifested in a subsequent preference for those
(conditioned) stimuli. In this study, we investigated the relationship
between the ANC and preference learning in humans. Three abstract
monochrome patterns were presented to each subject over 180 trials in
the context of a counting task requiring working memory. One pattern was paired with food reward on 90% of the trials in which it was presented and with no food reward on the other 10% of trials. The
other patterns were similarly reinforced, but at ratios of 50:50% and
10:90% with reward and nonreward, respectively. Subsequently, a group
of 21 normal participants preferred the pattern paired most often with
reward to that paired least often with reward, and they did not
explicitly relate their preferences to the conditioning procedure, but
instead attributed them to the characteristics of the patterns
themselves. Unlike the normal controls, a group of patients with
unilateral surgical lesions that included the ANC (15 left, 18 right)
did not show conditioned preferences, but performed normally on a
measure of working memory. In contrast, 13 patients with unilateral
damage confined to frontal cortex exhibited normal conditioned
preferences but were impaired on the working memory task. This double
dissociation provides clear evidence that, in humans as in other
animals, reward-related learning (conditioned reward) critically
depends on a circuit involving inferotemporal cortex and the ANC.
Key words:
amygdaloid body; conditioning; emotion; frontal lobe; reward; temporal lobe; working memory
Copyright © 2000 Society for Neuroscience 0270-6474/00/2072649-08$05.00/0
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