Bilateral Tactile Input Patterns Decoded at Comparable Levels But Different Time Scales in Neocortical Neurons

Abstract

The presence of contralateral tactile input can profoundly affect ipsilateral tactile perception, and unilateral stroke in somatosensory areas can result in bilateral tactile deficits, suggesting that bilateral tactile integration is an important part of brain function. Although previous studies have shown that bilateral tactile inputs exist and that there are neural interactions between inputs from the two sides, no previous study explored to what extent the local neuronal circuitry processing contains detailed information about the nature of the tactile input from the two sides. To address this question, we used a recently introduced approach to deliver a set of electrical, reproducible, tactile afferent, spatiotemporal activation patterns, which permits a high-resolution analysis of the neuronal decoding capacity, to the skin of the second forepaw digits of the anesthetized male rat. Surprisingly, we found that individual neurons of the primary somatosensory can decode contralateral and ipsilateral input patterns to comparable extents. Although the contralateral input was stronger and more rapidly decoded, given sufficient poststimulus processing time, ipsilateral decoding levels essentially caught up to contralateral levels. Moreover, there was a weak but significant correlation for neurons with high decoding performance for contralateral tactile input to also perform well on decoding ipsilateral input. Our findings shed new light on the brain mechanisms underlying bimanual haptic integration. Here we demonstrate that the spiking activity of single neocortical neurons in the somatosensory cortex of the rat can be used to decode patterned tactile stimuli delivered to the distal ventral skin of the second forepaw digits on both sides of the body. Even though comparable levels of decoding of the tactile input were achieved faster for contralateral input, given sufficient integration time each neuron was found to decode ipsilateral input with a comparable level of accuracy. Given that the neocortical neurons could decode ipsilateral inputs with such small differences between the patterns suggests that S1 cortex has access to very precise information about ipsilateral events. The findings shed new light on possible network mechanisms underlying bimanual haptic processing.

Somatosensory Cortical Neurons Decode Tactile Input Patterns and Location from Both Dominant and Non-dominant Digits

“…We use a recently introduced approach that is based on low-intensity electrical activation of tactile afferents in predefined complex spatiotemporal patterns, with the primary purpose of obtaining maximal reproducibility for a varied set of non-trivial tactile input patterns. This approach overcomes limitations associated with mechanical skin stimulation (see Discussion) and provides a highly sensitive tool to analyze the precision by which the spike output of a neuron contains information about the type of tactile input received (Genna et al, 2018;Oddo et al, 2017). We find that individual neurons can decode tactile input patterns to a non-adjacent, non-dominant digit at a comparable or even a higher level than for inputs to the dominant digit while also decoding which digit the input originated from.…”

Multi-Structure Cortical States Deduced from Intracellular Representations of Fixed Tactile Input Patterns

“…In order to achieve as realistic spatiotemporal patterns of tactile sensor activation as possible, while preserving the aim of high reproducibility of the patterns, we used an artificial fingertip equipped with four neuromorphic sensors to generate a set of spatiotemporal patterns of skin activation to be used in the electrical interface with the rat skin. The procedures have previously been described in greater detail and the patterns used here were the same as before (Oddo et al , 2017; Genna et al , 2018; Enander et al , 2019). As discussed in this previous work, the artificial fingertip allowed synthesising spatiotemporal patterns of skin sensor activation at quasi-natural firing rates that follow a natural overall temporal modulation, or ‘envelope’, that the biological skin sensors are known to display under dynamic indentation (Jenmalm et al , 2003).…”

Ubiquitous Neocortical Decoding of Tactile Input Patterns

“…We previously introduced a method to deliver such reproducible and diversified spatiotemporal input patterns by electrical activation of tactile afferents in local digit skin and showed that cells in the primary somatosensory cortex (S1) of the rat are capable of decoding these tactile inputs with high accuracy (Oddo et al, 2017). Using this approach, we recently reported that the neurons of the S1 cortex have access to information about the “what” component of ipsilateral tactile inputs, just like they have for contralateral inputs (Genna et al, 2018). Here, we show that in non-paw S1 regions and in non-S1 regions across the dorsal neocortical surface, including within visual cortical areas, the responses of individual neocortical neurons contain information about the “what” component of tactile inputs to the second digit of the forepaw.…”