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.

Whereas functional localization historically has been a key concept in neuroscience, direct neuronal recordings show that input of a particular modality can be recorded well outside its primary receiving areas in the neocortex. Here, we wanted to explore if such spatially unbounded inputs potentially contain any information about the quality of the input received. We utilized a recently introduced approach to study the neuronal decoding capacity at a high resolution by delivering a set of electrical, highly reproducible spatiotemporal tactile afferent activation patterns to the skin of the contralateral second digit of the forepaw of the anesthetized rat. Surprisingly, we found that neurons in all areas recorded from, across all cortical depths tested, could decode the tactile input patterns, including neurons of the primary visual cortex. Within both somatosensory and visual cortical areas, the combined decoding accuracy of a population of neurons was higher than for the best performing single neuron within the respective area. Such cooperative decoding indicates that not only did individual neurons decode the input, they also did so by generating responses with different temporal profiles compared to other neurons, which suggests that each neuron could have unique contributions to the tactile information processing. These findings suggest that tactile processing in principle could be globally distributed in the neocortex, possibly for comparison with internal expectations and disambiguation processes relying on other modalities.

Summary The neocortex has a globally encompassing network structure, which for each given input constrains the possible combinations of neuronal activations across it. Hence, its network contains solutions. But in addition, the cortex has an ever-changing multidimensional internal state, causing each given input to result in a wide range of specific neuronal activations. Here we use intracellular recordings in somatosensory cortex (SI) neurons of anesthetized rats to show that remote, subthreshold intracortical electrical perturbation can impact such constraints on the responses to a set of spatiotemporal tactile input patterns. Whereas each given input pattern normally induces a wide set of preferred response states, when combined with cortical perturbation response states that did not otherwise occur were induced and consequently made other response states less likely. The findings indicate that the physiological network structure can dynamically change as the state of any given cortical region changes, thereby enabling a rich, multifactorial, perceptual capability.

The brain has a never-ending internal activity, whose spatiotemporal evolution interacts with external inputs to constrain their impact on brain activity and thereby how we perceive them. We used reproducible touch-related spatiotemporal sensory inputs and recorded intracellularly from rat (Sprague-Dawley, male) neocortical neurons to characterize this interaction. The synaptic responses, or the summed input of the networks connected to the neuron, varied greatly to repeated presentations of the same tactile input pattern delivered to the tip of digit 2. Surprisingly, however, these responses tended to sort into a set of specific time-evolving response types, unique for each neuron. Further, using a set of eight such tactile input patterns, we found each neuron to exhibit a set of specific response types for each input provided. Response types were not determined by the global cortical state, but instead likely depended on the time-varying state of the specific subnetworks connected to each neuron. The fact that some types of responses recurred indicates that the cortical network had a non-continuous landscape of solutions for these tactile inputs. Therefore, our data suggest that sensory inputs combine with the internal dynamics of the brain networks, thereby causing them to fall into one of the multiple possible perceptual attractor states. The neuron-specific instantiations of response types we observed suggest that the subnetworks connected to each neuron represent different components of those attractor states. Our results indicate that the impact of cortical internal states on external inputs is substantially more richly resolvable than previously shown.

Key points Parts of the fields of neuroscience and neurology consider the neocortex to be a functionally parcelled structure. Viewed through such a conceptual filter, there are multiple clinical observations after localized stroke lesions that seem paradoxical. We tested the effect that localized stroke‐like lesions have on neuronal information processing in a part of the neocortex that is distant to the lesion using animal experiments. We find that the distant lesion degrades the quality of neuronal information processing of tactile input patterns in primary somatosensory cortex. The findings suggest that even the processing of primary sensory information depends on an intact neocortical network, with the implication that all neocortical processing may rely on widespread interactions across large parts of the cortex. Abstract Recent clinical studies report a surprisingly weak relationship between the location of cortical brain lesions and the resulting functional deficits. From a neuroscience point of view, such findings raise questions as to what extent functional localization applies in the neocortex and to what extent the functions of different regions depend on the integrity of others. Here we provide an in‐depth analysis of the changes in the function of the neocortical neuronal networks after distant focal stroke‐like lesions in the anaesthetized rat. Using a recently introduced high resolution analysis of neuronal information processing, consisting of pre‐set spatiotemporal patterns of tactile afferent activation against which the neuronal decoding performance can be quantified, we found that stroke‐like lesions in distant parts of the cortex significantly degraded the decoding performance of individual neocortical neurons in the primary somatosensory cortex (decoding performance decreased from 30.9% to 24.2% for n = 22 neurons, Wilcoxon signed rank test, P = 0.028). This degrading effect was not due to changes in the firing frequency of the neuron (Wilcoxon signed rank test, P = 0.499) and was stronger the higher the decoding performance of the neuron, indicating a specific impact on the information processing capacity in the cortex. These findings suggest that even primary sensory processing depends on widely distributed cortical networks and could explain observations of focal stroke lesions affecting a large range of functions.