Excitatory cortical neurons form fine-scale functional networks.
The specificity of cortical neuron connections creates columns of functionally similar neurons spanning from the pia to the white matter. Here we investigate whether there is an additional, finer level of specificity that creates subnetworks of excitatory neurons within functional columns. We tested for fine-scale specificity of connections to cortical layer 2/3 pyramidal neurons in rat visual cortex by using cross-correlation analyses of synaptic currents evoked by photostimulation. Recording simultaneously from adjacent layer 2/3 pyramidal cells, we find that when they are connected to each other (20% of all recorded pairs) they share common input from layer 4 and within layer 2/3. When adjacent layer 2/3 neurons are not connected to each other, they share very little (if any) common excitatory input from layers 4 and 2/3. In contrast, all layer 2/3 neurons share common excitatory input from layer 5 and inhibitory input from layers 2/3 and 4, regardless of whether they are connected to each other. Thus, excitatory connections from layer 4 to layer 2/3 and within layer 2/3 form fine-scale assemblies of selectively interconnected neurons; inhibitory connections and excitatory connections from layer 5 link neurons across these fine-scale subnetworks. Relatively independent subnetworks of excitatory neurons are therefore embedded within the larger-scale functional architecture; this allows neighbouring neurons to convey information more independently than suggested by previous descriptions of cortical circuitry.
Yoshimura
Yumiko
Y
Systems Neurobiology Laboratories, The Salk Institute for Biological Studies, 10010 North Torrey Pines Road, La Jolla, California 92037, USA.
Dantzker
Jami L M
JL
Callaway
Edward M
EM
D000200:Action Potentials / Q000502:physiology / Q000528:radiation effects; D000344:Afferent Pathways / Q000502:physiology* / Q000528:radiation effects; D000818:Animals; D019706:Excitatory Postsynaptic Potentials / Q000502:physiology / Q000528:radiation effects; D066298:In Vitro Techniques; D010812:Physical Stimulation; D011336:Probability; D017966:Pyramidal Cells / Q000166:cytology* / Q000502:physiology* / Q000528:radiation effects; D051381:Rats; D020318:Rats, Long-Evans; D014793:Visual Cortex / Q000166:cytology* / Q000502:physiology* / Q000528:radiation effects