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The Journal of Neuroscience, April 27, 2005, 25(17):4207-4216; doi:10.1523/JNEUROSCI.4697-04.2005

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Behavioral/Systems/Cognitive
Redundancy and Synergy of Neuronal Ensembles in Motor Cortex

Nandakumar S. Narayanan,1,2 Eyal Y. Kimchi,1,2 and Mark Laubach1,2,3,4

1The John B. Pierce Laboratory, 2Interdepartmental Neuroscience Program, and Departments of 3Neurobiology and 4Biomedical Engineering, Yale University School of Medicine, New Haven, Connecticut 06519

We examined the ability of neuronal ensembles from rat motor cortex to predict behavioral performance during a reaction time task. We found that neurons that were the best individual predictors of task performance were not necessarily the neurons that contributed the most predictive information to an ensemble of neurons. To understand this result, we applied a framework for quantifying statistical relationships between neurons (Schneidman et al., 2003) to all possible combinations of neurons within our ensembles. We found that almost all neurons (96%) contributed redundant predictive information to the ensembles. This redundancy resulted in the maintenance of predictive information despite the removal of many neurons from each ensemble. Moreover, the balance of synergistic and redundant interactions depended on the number of neurons in the ensemble. Small ensembles could exhibit synergistic interactions (e.g., 23 ± 9% of ensembles with two neurons were synergistic). In contrast, larger ensembles exhibited mostly redundant interactions (e.g., 99 ± 0.1% of ensembles with eight neurons were redundant). We discuss these results with regard to constraints on interpreting neuronal ensemble data and with respect to motor cortex involvement in reaction time performance.

Key words: motor cortex; population coding; neuronal ensembles; reaction time; synergy; redundancy


Received June 4, 2004; revised March 11, 2005; accepted March 14, 2005.




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