TY - JOUR
T1 - Hierarchical excitatory synaptic connectivity in mouse olfactory cortex
AU - McGinley, Matthew J.
AU - Westbrook, Gary L.
PY - 2013/10/1
Y1 - 2013/10/1
N2 - Topological motifs in synaptic connectivity-such as the cortical column-are fundamental to processing of information in cortical structures. However, the mesoscale topology of cortical networks beyond columns remains largely unknown. In the olfactory cortex, which lacks an obvious columnar structure, sensory-evoked patterns of activity have failed to reveal organizational principles of the network and its structure has been considered to be random. We probed the excitatory network in the mouse olfactory cortex using variance analysis of paired whole-cell recording in olfactory cortex slices. On a given trial, triggered network-wide bursts in disinhibited slices had remarkably similar time courses in widely separated and randomly selected cell pairs of pyramidal neurons despite significant trial-to-trial variability within each neuron. Simulated excitatory network models with random topologies only partially reproduced the experimental burst-variance patterns. Network models with local (columnar) or distributed subnetworks, which have been predicted as the basis of encoding odor objects, were also inconsistent with the experimental data, showing greater variability between cells than across trials. Rather, network models with power-law and especially hierarchical connectivity showed the best fit. Our results suggest that distributed subnetworks are weak or absent in the olfactory cortex, whereas a hierarchical excitatory topology may predominate. A hierarchical excitatory network organization likely underlies burst generation in this epileptogenic region, and may also shape processing of sensory information in the olfactory cortex.
AB - Topological motifs in synaptic connectivity-such as the cortical column-are fundamental to processing of information in cortical structures. However, the mesoscale topology of cortical networks beyond columns remains largely unknown. In the olfactory cortex, which lacks an obvious columnar structure, sensory-evoked patterns of activity have failed to reveal organizational principles of the network and its structure has been considered to be random. We probed the excitatory network in the mouse olfactory cortex using variance analysis of paired whole-cell recording in olfactory cortex slices. On a given trial, triggered network-wide bursts in disinhibited slices had remarkably similar time courses in widely separated and randomly selected cell pairs of pyramidal neurons despite significant trial-to-trial variability within each neuron. Simulated excitatory network models with random topologies only partially reproduced the experimental burst-variance patterns. Network models with local (columnar) or distributed subnetworks, which have been predicted as the basis of encoding odor objects, were also inconsistent with the experimental data, showing greater variability between cells than across trials. Rather, network models with power-law and especially hierarchical connectivity showed the best fit. Our results suggest that distributed subnetworks are weak or absent in the olfactory cortex, whereas a hierarchical excitatory topology may predominate. A hierarchical excitatory network organization likely underlies burst generation in this epileptogenic region, and may also shape processing of sensory information in the olfactory cortex.
KW - Endopiriform nucleus
KW - Functional connectome
KW - Network topology
KW - Piriform cortex
KW - Small world
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U2 - 10.1073/pnas.1303813110
DO - 10.1073/pnas.1303813110
M3 - Article
C2 - 24043834
AN - SCOPUS:84885083797
SN - 0027-8424
VL - 110
SP - 16193
EP - 16198
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 40
ER -