Specific contributions of ventromedial, anterior cingulate, and lateral prefrontal cortex for attentional selection and stimulus valuation.

Authors

Daniel Kaping, Department of Biology, Centre for Vision Research, York University, Toronto, Ontario, Canada & Department of Physiology and Pharmacology, University of Western Ontario, London, Ontario, Canada
Martin Vinck, Cognitive and Systems Neuroscience Group, Center for Neuroscience, University of Amsterdam, Amsterdam, The Netherlands
R Matthew Hutchison, Department of Physiology and Pharmacology, University of Western Ontario, London, Ontario, Canada
Stefan Everling, Department of Physiology and Pharmacology, University of Western Ontario, London, Ontario, Canada & Robarts Research Institute, London, Ontario, Canada
Thilo Womelsdorf, Department of Biology, Centre for Vision Research, York University, Toronto, Ontario, Canada & Department of Physiology and Pharmacology, University of Western Ontario, London, Ontario, Canada

Document Type

Article

Publication Date

12-1-2011

Journal

PLoS biology

Volume

9

Issue

12

First Page

1001224

Last Page

1001224

URL with Digital Object Identifier

10.1371/journal.pbio.1001224

Abstract

Attentional control ensures that neuronal processes prioritize the most relevant stimulus in a given environment. Controlling which stimulus is attended thus originates from neurons encoding the relevance of stimuli, i.e. their expected value, in hand with neurons encoding contextual information about stimulus locations, features, and rules that guide the conditional allocation of attention. Here, we examined how these distinct processes are encoded and integrated in macaque prefrontal cortex (PFC) by mapping their functional topographies at the time of attentional stimulus selection. We find confined clusters of neurons in ventromedial PFC (vmPFC) that predominantly convey stimulus valuation information during attention shifts. These valuation signals were topographically largely separated from neurons predicting the stimulus location to which attention covertly shifted, and which were evident across the complete medial-to-lateral extent of the PFC, encompassing anterior cingulate cortex (ACC), and lateral PFC (LPFC). LPFC responses showed particularly early-onset selectivity and primarily facilitated attention shifts to contralateral targets. Spatial selectivity within ACC was delayed and heterogeneous, with similar proportions of facilitated and suppressed responses during contralateral attention shifts. The integration of spatial and valuation signals about attentional target stimuli was observed in a confined cluster of neurons at the intersection of vmPFC, ACC, and LPFC. These results suggest that valuation processes reflecting stimulus-specific outcome predictions are recruited during covert attentional control. Value predictions and the spatial identification of attentional targets were conveyed by largely separate neuronal populations, but were integrated locally at the intersection of three major prefrontal areas, which may constitute a functional hub within the larger attentional control network.