Artificial spatiotemporal touch inputs reveal complementary decoding in neocortical neurons

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.

Focal neocortical lesions impair distant neuronal information processing

“…Note that we have previously reported that there is no relationship between recording depth and decoding of the tactile afferent inputs we used (Oddo et al . ). The ECoG electrode was placed at the rostral end of the craniotomy.…”

“…the same approach as reported in a previous study (Oddo et al . ). For each skin site the stimulation pulse was set to an intensity of 0.5 mA with a duration of 0.14 ms (DS3 Isolated Stimulator, Digitimer, Welwyn Garden City, UK), which is 2.5 times the threshold for activating tactile afferents (Rasmusson & Northgrave, ; Bengtsson et al .…”

“…Through this interface eight predefined spatiotemporal patterns of skin activation were delivered (the stimulation patterns are indicated as F5, S5, F10, S10, F20, S20, F∞ and S∞, and were exactly the same as in the paper of Oddo et al . ). These stimulus patterns lasted less than 350 ms (range 213–346 ms) and consecutive deliveries were separated by 1.8 s. The spatiotemporal patterns were presented repeatedly up to 100 times in a pseudo‐random order.…”

“…The generation of the stimulation patterns has been described in detail previously (Oddo et al . ) and that paper also contains an extensive discussion on the advantages and limitations of this approach. Since each stimulation pattern was repeated 100 times, we could display the evoked responses as peristimulus time histograms (PSTHs).…”

“…Here we analyse the effects of distant localized cortical stroke‐like lesions using a gradable measure of the information processing in individual neurons in the primary somatosensory cortex (S1), based on the delivery of a highly reproducible set of spatiotemporal tactile afferent activation patterns to the second digit (Oddo et al . ; Genna et al . ).…”