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Different time courses of learning-related activity in the prefrontal cortex and striatum

Abstract

To navigate our complex world, our brains have evolved a sophisticated ability to quickly learn arbitrary rules such as ‘stop at red’. Studies in monkeys using a laboratory test of this capacity—conditional association learning—have revealed that frontal lobe structures (including the prefrontal cortex) as well as subcortical nuclei of the basal ganglia are involved in such learning1,2,3,4,5. Neural correlates of associative learning have been observed in both brain regions6,7,8,9,10,11,12,13,14, but whether or not these regions have unique functions is unclear, as they have typically been studied separately using different tasks. Here we show that during associative learning in monkeys, neural activity in these areas changes at different rates: the striatum (an input structure of the basal ganglia) showed rapid, almost bistable, changes compared with a slower trend in the prefrontal cortex that was more in accordance with slow improvements in behavioural performance. Also, pre-saccadic activity began progressively earlier in the striatum but not in the prefrontal cortex as learning took place. These results support the hypothesis that rewarded associations are first identified by the basal ganglia, the output of which ‘trains’ slower learning mechanisms in the frontal cortex15.

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Figure 1: Task and behaviour.
Figure 2: Change in peri-cue saccade direction selectivity in prefrontal cortex and caudate nucleus with learning.
Figure 3: Change in saccade direction selectivity at the time of saccade execution during the learning process.

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Acknowledgements

We thank M. H. Histed for valuable discussions; K. J. MacCully for technical assistance; W. F. Asaad, A. J. Bastian, T. Buschman, A. C. Diogo, J. Feingold, D. J. Freedman, M. Machon, J. McDermott, J. E. Roy and M. Wicherski for helpful comments. This work was supported by a grant from the N.I.N.D.S. A.P. was supported by the Tourette's Syndrome Association.

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Correspondence to Anitha Pasupathy.

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Supplementary information

Supplementary Figure 1

Demonstration of peri-cue epoch saccade direction selectivity and its development with learning in single PFC and Cd neurons. (PDF 701 kb)

Supplementary Figure 2

Example of a single Cd neuron showing rapid backward progression of direction selectivity within a few correct trials. (PDF 520 kb)

Supplementary Figure 3

This file contains the supplementary figure comparing population direction selectivity on correct and error trials for the prefrontal (PFC) cortex and the caudate nucleus (Cd). Peri-cue direction selectivity on error trials is significantly weaker than on correct trials in the PFC but not Cd. (PDF 237 kb)

Supplementary Figure 4

Comparison of the evolution of average direction selectivity as a function of correct trials between the PFC and Cd populations. (PDF 189 kb)

Supplementary Figure Legends

This file contains legends for Supplementary figures 1-4. (DOC 30 kb)

Supplementary Notes

This file contains twelve supplementary notes that report results and methods that could not be fit in the main body. (DOC 43 kb)

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Pasupathy, A., Miller, E. Different time courses of learning-related activity in the prefrontal cortex and striatum. Nature 433, 873–876 (2005). https://doi.org/10.1038/nature03287

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