Abstract
How different is local cortical circuitry from a random network? To answer this question, we probed synaptic connections with several hundred simultaneous quadruple whole-cell recordings from layer 5 pyramidal neurons in the rat visual cortex. Analysis of this dataset revealed several nonrandom features in synaptic connectivity. We confirmed previous reports that bidirectional connections are more common than expected in a random network. We found that several highly clustered three-neuron connectivity patterns are overrepresented, suggesting that connections tend to cluster together. We also analyzed synaptic connection strength as defined by the peak excitatory postsynaptic potential amplitude. We found that the distribution of synaptic connection strength differs significantly from the Poisson distribution and can be fitted by a lognormal distribution. Such a distribution has a heavier tail and implies that synaptic weight is concentrated among few synaptic connections. In addition, the strengths of synaptic connections sharing pre- or postsynaptic neurons are correlated, implying that strong connections are even more clustered than the weak ones. Therefore, the local cortical network structure can be viewed as a skeleton of stronger connections in a sea of weaker ones. Such a skeleton is likely to play an important role in network dynamics and should be investigated further.
Highlights
Understanding cortical function requires unraveling synaptic connectivity in cortical circuits, that is, establishing the wiring diagrams
We studied connectivity among thick tufted layer 5 neurons in rat visual cortex with quadruple whole-cell recordings (Figure 1A and 1B)
Synaptic connection strengths were assessed by evoking action potentials in each of the four cells and measuring the averaged peak excitatory postsynaptic potential (EPSP) amplitudes in the other three cells
Summary
Understanding cortical function requires unraveling synaptic connectivity in cortical circuits, that is, establishing the wiring diagrams. Smaller wiring diagrams can be reconstructed using electron microscopy [1], reconstruction on the scale of a cortical column is impossible with current technology (but see [2] for a promising approach) Even if such a possibility were within reach, synaptic connectivity likely varies from animal to animal and within one animal over time. Electrophysiological recordings from neuronal pairs showed that the probability of connection is often low [3,5,6,7,8,9,10,11], suggesting that the network is sparse Such statistical approaches may create the impression that synaptic connectivity in local cortical circuits is random. This view is consistent with previous suggestions [12,13,14], but hard to reconcile with cortical functionality, which must rely on specificity of connections [15,16,17,18]
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