Artificial spatiotemporal touch inputs reveal complementary decoding in neocortical neurons

Calogero M Oddo,Alberto Mazzoni,Anton Spanne,Domenico Camboni,Hannes Mogensen,Jonas M D Enander,Henrik Jörntell,Fredrik Bengtsson,Silvestro Micera

doi:10.1038/srep45898

Abstract

Investigations of the mechanisms of touch perception and decoding has been hampered by difficulties in achieving invariant patterns of skin sensor activation. To obtain reproducible spatiotemporal patterns of activation of sensory afferents, we used an artificial fingertip equipped with an array of neuromorphic sensors. The artificial fingertip was used to transduce real-world haptic stimuli into spatiotemporal patterns of spikes. These spike patterns were delivered to the skin afferents of the second digit of rats via an array of stimulation electrodes. Combined with low-noise intra- and extracellular recordings from neocortical neurons in vivo, this approach provided a previously inaccessible high resolution analysis of the representation of tactile information in the neocortical neuronal circuitry. The results indicate high information content in individual neurons and reveal multiple novel neuronal tactile coding features such as heterogeneous and complementary spatiotemporal input selectivity also between neighboring neurons. Such neuronal heterogeneity and complementariness can potentially support a very high decoding capacity in a limited population of neurons. Our results also indicate a potential neuroprosthetic approach to communicate with the brain at a very high resolution and provide a potential novel solution for evaluating the degree or state of neurological disease in animal models.

Highlights

Of a ‘frozen state’ of sensor activation, isolated from the uncertainty in the mechanotransduction step
In auditory and visual cortical systems, ‘natural scenes’ of sensory input have been shown to evoke very different cortical responses compared to those evoked by simplified inputs[17,18]. This may indicate that the circuitry structure is adapted to some general features in the spatiotemporal patterns of sensor activation that may occur during natural behavior, and that this circuitry structure constrains the way the individual neurons in the network are activated
Our aim was to study the decoding capacity of central neurons in isolation, separated from noise arising from mechanical interfacing with the skin and from intrinsic skin sensor noise

Summary

Introduction

Of a ‘frozen state’ of sensor activation, isolated from the uncertainty in the mechanotransduction step. In auditory and visual cortical systems, ‘natural scenes’ of sensory input have been shown to evoke very different cortical responses compared to those evoked by simplified inputs[17,18] This may indicate that the circuitry structure is adapted to some general features in the spatiotemporal patterns of sensor activation that may occur during natural behavior, and that this circuitry structure constrains the way the individual neurons in the network are activated. The spatiotemporal patterns of spike output generated from this system during dynamic touch were delivered as electrical stimuli to the distal tactile afferents from the volar side of the second digit of the rat forepaw With this approach, we hoped to mimic at least the general envelope of the overall temporal modulation of activation in the local population of skin sensors as it may occur in a conceivable natural touch. We find that the decoding performance of individual neurons can be much higher than previously described and that there is a complementarity in their response profiles that provides for a very high decoding capacity even in small groups of neurons

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Conclusion