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Simultaneous encoding of tactile information by three primate cortical areas

Abstract

We used simultaneous multi-site neural ensemble recordings to investigate the representation of tactile information in three areas of the primate somatosensory cortex (areas 3b, SII and 2). Small neural ensembles (30–40 neurons) of broadly tuned somatosensory neurons were able to identify correctly the location of a single tactile stimulus on a single trial, almost simultaneously. Furthermore, each of these cortical areas could use different combinations of encoding strategies, such as mean firing rate (areas 3b and 2) or temporal patterns of ensemble firing (area SII), to represent the location of a tactile stimulus. Based on these results, we propose that ensembles of broadly tuned neurons, located in three distinct areas of the primate somatosensory cortex, obtain information about the location of a tactile stimulus almost concurrently.

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Figure 1: Location of chronically implanted microwire arrays used to record neuronal ensemble activity in the somatosensory and motor cortex.
Figure 2: Single-neuron responses to tactile stimulation at different sites on the hand.
Figure 3: Post-stimulus time histograms depict the simultaneously recorded sensory responses of ensembles of neurons in areas SII and 2 following the punctate tactile stimulation of hair located in the dorsal hand of a monkey.
Figure 4: Distributed responses of area SII and 2 neural ensembles.
Figure 5: Concurrent activation of somatosensory cortical areas following punctate tactile stimulation.
Figure 6: Multiple statistical pattern recognition approaches cross-validate results of neural ensemble performances.
Figure 7: Single-trial discrimination by neural ensembles located in three somatosensory cortical areas (3b, SII and area 2) as measured by an artificial neural network trained with a learning vector quantization algorithm.
Figure 8: For all three cortical areas analyzed (3b, SII and 2), the single-trial discrimination capability varied as a function of the ensemble size.
Figure 9: The effect of bin clumping on the discrimination capability of cortical areas.

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Acknowledgements

We thank Bret Carswell, Scott Votaw and Marshall Shuler for technical assistance, and Harvey Wiggins (Plexon), Alex Kirilov (Plexon) and Larry Andrews (NBLABS) for hardware and software support. This work was supported by the McDonnell Pew Foundation, the Duke-Sandoz program, a contract from the NINDS Neuroprosthetic program to J.K.C. and M.A.L.N. and a Whitehead Scholar award to M.A.L.N.

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Correspondence to Miguel A. L. Nicolelis.

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Nicolelis, M., Ghazanfar, A., Stambaugh, C. et al. Simultaneous encoding of tactile information by three primate cortical areas. Nat Neurosci 1, 621–630 (1998). https://doi.org/10.1038/2855

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