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The primate amygdala combines information about space and value

Abstract

A stimulus predicting reinforcement can trigger emotional responses, such as arousal, and cognitive ones, such as increased attention toward the stimulus. Neuroscientists have long appreciated that the amygdala mediates spatially nonspecific emotional responses, but it remains unclear whether the amygdala links motivational and spatial representations. To test whether amygdala neurons encode spatial and motivational information, we presented reward-predictive cues in different spatial configurations to monkeys and assessed how these cues influenced spatial attention. Cue configuration and predicted reward magnitude modulated amygdala neural activity in a coordinated fashion. Moreover, fluctuations in activity were correlated with trial-to-trial variability in spatial attention. Thus, the amygdala integrates spatial and motivational information, which may influence the spatial allocation of cognitive resources. These results suggest that amygdala dysfunction may contribute to deficits in cognitive processes normally coordinated with emotional responses, such as the directing of attention toward the location of emotionally relevant stimuli.

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Figure 1: Motivational cues bias spatial attention.
Figure 2: Reconstruction of recording locations.
Figure 3: Amygdala neurons encode the value and spatial configuration of cues.
Figure 4: Latency of value discrimination by amygdala neurons depends on cue spatial configuration.
Figure 5: Latency of visual information is insensitive to spatial location.
Figure 6: The encoding of space, value and stimulus identity by amygdala neurons evolves according to task demands.
Figure 7: Trial-to-trial variations in firing rates are correlated with reaction time.

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Acknowledgements

We thank E. Kandel and K. Louie for discussions and comments on the manuscript, S. Dashnaw for MRI support, G. Asfaw for veterinary support, and K. Marmon and N. Macfarlane for technical support. This research was supported by grants to C.D.S. from the US National Institute of Mental Health (NIMH) (R01 MH082017) and the US National Institute on Drug Abuse (R01 DA020656), and by a core grant from the US National Eye Institute (NEI) (P30-EY19007) to Columbia University; C.J.P. received support from NIH (T32-HD07430, T32-NS06492 and T32-EY139333); B.L. received support from the NIMH (T32-MH015144) and the Helen Hay Whitney Foundation.

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B.L. initiated the project; C.J.P. and B.L. designed the experiments, collected the data and wrote the manuscript; C.J.P. analyzed data with assistance from B.L.; C.D.S. supervised and provided input about all aspects of the project and edited the manuscript.

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Correspondence to C Daniel Salzman.

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The authors declare no competing financial interests.

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Peck, C., Lau, B. & Salzman, C. The primate amygdala combines information about space and value. Nat Neurosci 16, 340–348 (2013). https://doi.org/10.1038/nn.3328

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