Abstract

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.

Highlights

  • Behavioral, mental, and perceptual functions of the neocortex depend on its internal state

  • Evaluation of the Specificity of the Identified Response Types for Each Stimulation Pattern in the Same Neuron We evaluated the separability of the whole membrane voltage-time curve vectors for each of the identified response types, for each stimulation pattern in each neuron separately, as well as their separability vs. the ‘‘ungrouped’’ responses, using a combination of principal component analysis (PCA) and k-nearest neighbors-classification (Figure 3A)

  • Our results show that the responses evoked by tactile sensory input patterns fall into a limited subset of preferred response states that are specific to each input pattern and each cortical neuron

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Summary

Introduction

Behavioral, mental, and perceptual functions of the neocortex depend on its internal state. The internal state is a high-dimensional latent state (Stringer et al, 2019a,b) more detailed physiological characterization of the state-dependent influence on cortical circuitry responses to naturalistic sensory input is so far lacking. This is not surprising given that a direct demonstration would require a precise estimate of what the experimental subject is thinking and how that thinking is instantiated in the circuitry, at the time of the stimulus delivery. We aimed to deduce information about the character of the interactions between the time-evolving cortical internal state and external inputs, based on an analysis of the detailed nature of the cortical neuron responses evoked by inputs consisting of several alternative fixed spatiotemporal patterns of tactile sensory activation, each delivered at a high number of repetitions

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