The fractions of short- and long-range connections in the visual cortex

When analyzing synaptic connectivity in a brain tissue slice, it is difficult to discern between synapses made by local neurons and those arising from long-range axonal projections. We analyzed a data set of excitatory neurons and inhibitory basket cells reconstructed from cat primary visual cortex in an attempt to provide a quantitative answer to the question: What fraction of cortical synapses is local, and what fraction is mediated by long-range projections? We found an unexpectedly high proportion of nonlocal synapses. For example, 92% of excitatory synapses near the axis of a 200-μm-diameter iso-orientation column come from neurons located outside the column, and this fraction remains high—76%—even for an 800-μm ocular dominance column. The long-range nature of connectivity has dramatic implications for experiments in cortical tissue slices. Our estimate indicates that in a 300-μm-thick section cut perpendicularly to the cortical surface, the number of viable excitatory synapses is reduced to about 10%, and the number of synapses made by inhibitory basket cell axons is reduced to 38%. This uneven reduction in the numbers of excitatory and inhibitory synapses changes the excitation–inhibition balance by a factor of 3.8 toward inhibition, and may result in cortical tissue that is less excitable than in vivo. We found that electrophysiological studies conducted in tissue sections may significantly underestimate the extent of cortical connectivity; for example, for some projections, the reported probabilities of finding connected nearby neuron pairs in slices could understate the in vivo probabilities by a factor of 3

Evolutionary constraints on visual cortex architecture from the dynamics of hallucinations

In the cat or primate primary visual cortex (V1), normal vision corresponds to a state where neural excitation patterns are driven by external visual stimuli. A spectacular failure mode of V1 occurs when such patterns are overwhelmed by spontaneously generated spatially self-organized patterns of neural excitation. These are experienced as geometric visual hallucinations. The problem of identifying the mechanisms by which V1 avoids this failure is made acute by recent advances in the statistical mechanics of pattern formation, which suggest that the hallucinatory state should be very robust. Here, we report how incorporating physiologically realistic long-range connections between inhibitory neurons changes the behavior of a model of V1. We find that the sparsity of long-range inhibition in V1 plays a previously unrecognized but key functional role in preserving the normal vision state. Surprisingly, it also contributes to the observed regularity of geometric visual hallucinations. Our results provide an explanation for the observed sparsity of long-range inhibition in V1—this generic architectural feature is an evolutionary adaptation that tunes V1 to the normal vision state. In addition, it has been shown that exactly the same long-range connections play a key role in the development of orientation preference maps. Thus V1’s most striking long-range features—patchy excitatory connections and sparse inhibitory connections—are strongly constrained by two requirements: the need for the visual state to be robust and the developmental requirements of the orientational preference map.National Natural Science Foundation (Grant NSF-EF-0526747)University of Illinois at Urbana-Champaign. Dept. of Physics. Drickamer Fellowshi

Cooperative synapse formation in the neocortex

Neuron morphology plays an important role in defining synaptic connectivity. Clearly, only pairs of neurons with closely positioned axonal and dendritic branches can be synaptically coupled. For excitatory neurons in the cerebral cortex, such axo-dendritic oppositions, termed potential synapses, must be bridged by dendritic spines to form synaptic connections. To explore the rules by which synaptic connections are formed within the constraints imposed by neuron morphology, we compared the distributions of the numbers of actual and potential synapses between pre- and postsynaptic neurons forming different laminar projections in rat barrel cortex. Quantitative comparison explicitly ruled out the hypothesis that individual synapses between neurons are formed independently of each other. Instead, the data are consistent with a cooperative scheme of synapse formation where multiple-synaptic connections between neurons are stabilized while neurons that do not establish a critical number of synapses are not likely to remain synaptically coupled