Remote cortical perturbation dynamically changes the network solutions to given tactile inputs in neocortical neurons

Abstract

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.

Profound impact of hippocampal output on the interpretation of tactile input patterns in SI neurons

“…We made whole cell patch clamp recordings from putative pyramidal neurons (see Methods; also (Norrlid et al, 2021)) between layers III-V in the forepaw region of the SI cortex, while stimulating the distal part of the second digit with eight fixed spatiotemporal tactile activation (TA) patterns delivered in pseudorandom order (Figure 1A), a protocol we’ve used in numerous previous publications (Enander and Jorntell, 2019; Enander et al, 2019; Etemadi et al, 2022; Norrlid et al, 2021; Oddo et al, 2017; Wahlbom et al, 2019). Here, these TA input patterns were provided in isolation or in combination with a preceding brief stimulation of the subiculum/terminal CA1 region of the hippocampus (HIPTA) (Figure 1A-C).…”

“…We used the same method to cluster the responses as we used in a previous publication (Etemadi 2022). This identifies clusters of similar responses, with respect to their time-voltage curves, evoked by the same stimulation pattern, in an unsupervised manner.…”

“…In order to verify that the differences in response types observed in the above example occurred systematically, we performed a quantitative comparison of the temporal profiles of the responses using a PCA+kNN classification analysis (see Methods; same approach as that used in (Etemadi et al, 2022)). We first compared the clusters evoked by the same TA input pattern, but separated based on the condition (i.e.…”

“…We have previously shown that the processing of tactile information also at the cellular level in SI is dependent on other parts of the cortex. This was shown both by stroke-like lesions and by electrical manipulation of brain activity in neocortical areas with a remote location to the SI (Etemadi et al, 2022; Wahlbom et al, 2019). Recent anatomical studies have indicated that the extent of connections made by individual corticocortical axons have previously been greatly underestimated (Ahrlund-Richter et al, 2019; Gerfen et al, 2018) (see also https://www.janelia.org/project-team/mouselight; https://mouse.braindatacenter.cn/), hence giving structural support for these observations.…”

“…The relative orthogonality of these response states suggested the presence of attractor-type dynamics (Norrlid et al, 2021; Ringach, 2009), reminiscent of what has also been proposed to characterize the neuron population activity dynamics in the hippocampus (Gardner et al, 2022; Gardner et al, 2019). More recently, we showed that manipulation of the internal cortical state through electrical activation of a remote neocortical area can change the preferred network solutions, or the types of response states observed in SI neurons, for every given tactile input pattern (Etemadi et al, 2022). Remarkably, this change occurred despite that the remote cortical perturbation did not induce any overt response in the recorded neurons.…”