Abstract

The cortex is organized in vertical and horizontal circuits that determine the spatiotemporal properties of distributed cortical activity. Despite detailed knowledge of synaptic interactions among individual cells in the neocortex, little is known about the rules governing interactions among local populations. Here, we used self-sustained recurrent activity generated in cortex, also known as up-states, in rat thalamocortical slices in vitro to understand interactions among laminar and horizontal circuits. By means of intracellular recordings and fast optical imaging with voltage-sensitive dyes, we show that single thalamic inputs activate the cortical column in a preferential layer 4 (L4) → layer 2/3 (L2/3) → layer 5 (L5) sequence, followed by horizontal propagation with a leading front in supragranular and infragranular layers. To understand the laminar and columnar interactions, we used focal injections of TTX to block activity in small local populations, while preserving functional connectivity in the rest of the network. We show that L2/3 alone, without underlying L5, does not generate self-sustained activity and is inefficient propagating activity horizontally. In contrast, L5 sustains activity in the absence of L2/3 and is necessary and sufficient to propagate activity horizontally. However, loss of L2/3 delays horizontal propagation via L5. Finally, L5 amplifies activity in L2/3. Our results show for the first time that columnar interactions between supragranular and infragranular layers are required for the normal propagation of activity in the neocortex. Our data suggest that supragranular and infragranular circuits, with their specific and complex set of inputs and outputs, work in tandem to determine the patterns of cortical activation observed in vivo.

Links

Publisher Full Text

Authors

Wester JC, Contreras D

Institution

Department of Neuroscience, University of Pennsylvania Perelman School of Medicine, Philadelphia, Pennsylvania 19104, USA.

Source

The Journal of neuroscience : the official journal of the Society for Neuroscience 32:16 2012 Apr 18 pg 5454-71

MeSH

Animals
Animals, Newborn
Brain Mapping
Electric Stimulation
Electron Transport Complex IV
Membrane Potentials
Neocortex
Nerve Net
Neural Pathways
Optics and Photonics
Rats
Rats, Sprague-Dawley
Recruitment, Neurophysiological
Sodium Channel Blockers
Tetrodotoxin
Thalamus
Voltage-Sensitive Dye Imaging

Pub Type(s)

In Vitro
Journal Article
Research Support, N.I.H., Extramural

Language

eng

PubMed ID

22514308