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Prefrontal neurons transmit signals to parietal neurons that reflect executive control of cognition
NATURE NEUROSCIENCE, no. 10 (2013): 1484.0-+
Abstract
Prefrontal cortex influences behavior largely through its connections with other association cortices; however, the nature of the information conveyed by prefrontal output signals and what effect these signals have on computations performed by target structures is largely unknown. To address these questions, we simultaneously recorded the...More
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Introduction
- Prefrontal cortex is anatomically situated at the center of a complex array of projections that link it to other cortical association areas, one of which is the posterior parietal cortex[1,2,3,4].
- The authors recorded neural activity in parietal and prefrontal cortex simultaneously and used pattern classification to decode spatial category from firing rates in a sequence of 50-ms time bins
- This produced a time series of posterior probabilities quantifying the strengths of category representation in the two areas.
- The authors provide evidence that physiological signals encoding rule-dependent categories are transmitted selectively in a topdown direction from prefrontal to parietal neurons
- This identifies a neural mechanism by which prefrontal output could rapidly adapt computations performed by distributed cortical networks to changing environmental demands
Highlights
- Prefrontal cortex is anatomically situated at the center of a complex array of projections that link it to other cortical association areas, one of which is the posterior parietal cortex[1,2,3,4]
- To determine whether neural signals encoding rule-dependent spatial categories were transmitted between prefrontal and parietal neurons during the trial, we evaluated whether rapid fluctuations in the strength of these signals were correlated between cortical areas over time
- We found evidence that rule signals were transmitted in a top-down direction from prefrontal to parietal neurons (Supplementary Fig. 9b), as based on the activity of neurons that varied as a function of the rule only and not spatial category
- Evaluating neural signals encoding the position of the sample in parietal and prefrontal cortex, we found evidence that position signals covaried strongly and significantly between cortical areas at lag 0 (Supplementary Fig. 9c), an effect that peaked in the delay period following the offset of the sample stimulus. (Our analysis had limited ability to resolve transmission earlier in the trial, during the cue period, when feedforward transmission might be expected, because data had to be aggregated over a sequence of bins longer than the cue period before transmission could be detected.)
- Interactions between category signals in prefrontal and parietal cortex were significant at lag 1 but not lag 0, providing evidence that one cortical area drove the other, rather than both being driven by common input
- Our results identify a specific neural signal related to the executive control of cognition that is transmitted from prefrontal to parietal cortex
Methods
- Methods and any associated references are available in the online version of the paper.
Note: Any Supplementary Information and Source Data files are available in the online version of the paper. - When the rule cue was a vertical line, it instructed the horizontal categorization rule and divided the circular sample array into the spatial categories ‘left’ and ‘right’ on opposite sides of the boundary (Fig. 1a,c).
- When the rule cue was a horizontal line, it instructed the vertical (‘above’ or ‘below’) categorization rule, requiring monkeys to reassign the same set of sample positions to a new set of spatial categories (Fig. 1b,d).
- If the choice stimulus that was visible at the time of the motor response matched the spatial category of the sample, defined by the sample location and the orientation of the rule cue, the monkey was rewarded with a drop of juice
Results
- The authors trained two monkeys to perform a rule-based spatial categorization task[18] (Fig. 1).
- In this task, monkeys viewed a spot visual stimulus.
- Decode accuracy Proportion correct a Sample Delay 1 Rule cue Choice 1.
- Task, behavioral performance and network representation of spatial categories.
- (a) Stimulus sequence on a trial employing Gaze target Left Right.
- Response the horizontal categorization rule
- Task, behavioral performance and network representation of spatial categories. (a) Stimulus sequence on a trial employing Gaze target Left Right
Conclusion
- The authors obtained evidence that neural signals encoding rule-dependent spatial categories, and reflecting the executive control of a cognitive process, were selectively transmitted in a top-down direction from prefrontal to parietal neurons.
- Transmission was directional and selective for the nature of the transmitted information, depended on simultaneously recorded neural activity in the two areas, occurred at a restricted time scale and was modulated as a function of behavior.
- These data effectively translate the information content of a physiological signal transmitted from prefrontal to parietal neurons during cognitive processing.
- Interactions between category signals in prefrontal and parietal cortex were significant at lag 1 but not lag 0, providing evidence that one cortical area drove the other, rather than both being driven by common input
Funding
- Supported by the US National Institutes of Health (grant R01 MH077779 and R24MH069675), the Department of Veterans Affairs and the American Legion Brain Sciences Chair
- Blackman was supported by US National Institutes of Health grant T32 GM008244
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