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

Abstract

The brain has a never-ending internal activity, whose spatiotemporal evolution interacts with external inputs to define how we perceive them. We used reproducible touch-related spatiotemporal inputs and recorded intracellularly from rat neocortical neurons to characterise 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 sorted into a set of specific 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 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 were recurrent, i.e. more likely than others, indicates that the cortical network had a non-continuous landscape of solutions for these tactile inputs. Therefore, our data suggests that sensory inputs combine with the internal dynamics of the brain networks, thereby causing them to fall into one of 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 summaryO_LIIt is known that the internal state of the neocortical network profoundly impacts cortical neuronal responses to sensory input. C_LIO_LILittle is known of how the internal neocortical activity combines with a given sensory input to generate the response. C_LIO_LIWe used eight reproducible patterns of skin sensor activation and made intracellular recordings in neocortical neurons to explore the response variations in the specific subnetworks connected to each recorded neuron. C_LIO_LIWe found that each neuron exhibited multiple, specific recurring response types to the exact same skin stimulation pattern and that each given stimulation pattern evoked a unique set of response types. C_LIO_LIThe findings indicate a multi-structure internal state that combines with peripheral information to define cortical responses; we suggest this mechanism is a prerequisite for the formation of perception (and illusions) and indicates that the cortical networks work according to attractor dynamics. C_LI