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And Long-Range Connections in the Visual Cortex

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And Long-Range Connections in the Visual Cortex The fractions of short- and long-range connections in the visual cortex Armen Stepanyantsa,1, Luis M. Martinezb, Alex S. Ferecsko´ c,d, and Zolta´ n F. Kisva´ rdaye aDepartment of Physics and Center for Interdisciplinary Research on Complex Systems, Northeastern University, Boston, MA 02115; bInstituto de Neurociencias de Alicante, CSIC-UMH, 03550 Sant Joan d’Alacant, Spain; cCentre de Recherche Universite´Laval Robert-Giffard, Laval University, Quebec, Canada G1J 2G3; dDepartment of Neurophysiology, Division of Neuroscience, The Medical School, University of Birmingham, Birmingham B15 2TT, United Kingdom; and eDepartment of Anatomy, Histology, and Embryology, University of Debrecen, 4032 Debrecen, Hungary Edited by Charles F. Stevens, The Salk Institute for Biological Studies, La Jolla, CA, and approved December 24, 2008 (received for review October 21, 2008) When analyzing synaptic connectivity in a brain tissue slice, it is stellate) and 17 inhibitory basket cells (7, 8) labeled in vivo at difficult to discern between synapses made by local neurons and different depths spanning the entire thickness of the cat primary those arising from long-range axonal projections. We analyzed a visual cortex (area 17). We reconstructed neurons from multiple data set of excitatory neurons and inhibitory basket cells recon- tissue sections [supporting information (SI) Fig. S1], which structed from cat primary visual cortex in an attempt to provide a allowed us to recover all of the dendritic arbors and inhibitory quantitative answer to the question: What fraction of cortical basket cell axonal arbors in their entirety (2). But axonal synapses is local, and what fraction is mediated by long-range branches of excitatory neurons extending beyond 1 mm from the projections? We found an unexpectedly high proportion of non- neurons’ somata in the cortical plane were truncated; thus, we local synapses. For example, 92% of excitatory synapses near the have good knowledge of dendritic and local axonal arbors of axis of a 200-␮m-diameter iso-orientation column come from neurons spanning the entire thickness of the cortex, yet little or neurons located outside the column, and this fraction remains no information about the long-range projections of excitatory high—76%—even for an 800-␮m ocular dominance column. The neurons. Using techniques developed previously (2, 9, 10), we long-range nature of connectivity has dramatic implications for put together the reconstructed arbors (in numbers specified by experiments in cortical tissue slices. Our estimate indicates that in densities of neurons in different cortical layers) and determined a 300-␮m-thick section cut perpendicularly to the cortical surface, the densities of local synaptic connections in different cortical NEUROSCIENCE the number of viable excitatory synapses is reduced to about 10%, layers. To delineate the fractions of local and long-range exci- and the number of synapses made by inhibitory basket cell axons tatory synaptic connections, we compared the densities of local is reduced to 38%. This uneven reduction in the numbers of connections and asymmetric synapses obtained from previous excitatory and inhibitory synapses changes the excitation– electron microscopy studies of cat area 17. inhibition balance by a factor of 3.8 toward inhibition, and may Much of the experimental neuroscience research is done in result in cortical tissue that is less excitable than in vivo. We found 300- to 500-␮m brain tissue sections. But how much of synaptic that electrophysiological studies conducted in tissue sections may connectivity remains intact after cortical tissue is sliced? Be- significantly underestimate the extent of cortical connectivity; for cause the sizes of dendritic and axonal arbors of cortical neurons example, for some projections, the reported probabilities of find- are on the order of or much larger than the typical section ing connected nearby neuron pairs in slices could understate the in thickness, a substantial tissue slicing artifact can be expected. vivo probabilities by a factor of 3. Our experimental framework allowed us to provide a quantita- tive estimate of this effect by calculating the fractions of intact ͉ ͉ ͉ axon connectivity local slice excitatory and inhibitory synapses, that is, synapses that remain linked to the presynaptic and postsynaptic cells of their origins hen examining drawings (1) and 3-dimensional recon- after the tissue is sliced. With the overall reduction in the number Wstructions (2, 3) of cortical excitatory neurons, it is of intact synapses, connections between pairs of neurons in slices difficult to evade the impression that most of the excitatory are altered as well. As a result, the numbers of synapses between neurons’ axons, and, consequently, most of their synapses, are synaptically connected pairs of neurons (11) and the probability confined to a few hundred micrometer columnar domains of finding synaptically connected pairs of neurons (12) observed surrounding the neurons’ somata (Fig. 1A). Only a few branches in tissue slice experiments may significantly underestimate the in occasionally escape through the boundaries of the local domain. vivo connectivity. This interpretation of neuron images can be misleading, how- ever. The few axonal branches that extend beyond the local Results domain could ramify over large territories (e.g., the entire Connectivity Within a Cortical Column. We began our analysis by cortex) and thus could carry a significant fraction of all synapses. calculating the volume densities of dendritic spines of excitatory Such long-range projections may include interareal and intra- neurons in different cortical layers. Dendritic spines in a given areal connections, feedback from higher cortical areas, inter- cortical layer may originate from local neurons as well as neurons hemispheric projections, and feed-forward inputs from subcor- in other layers; thus, an accurate estimate of the volume density tical structures. These projections can be easily observed with of dendritic spines must take into account details of dendritic single neuron or bulk injections of tracers (4–6), but quantifying their fraction is difficult. This is because an accurate estimate of the amount of long-range axons must be made on the scale of the Author contributions: A.S., L.M.M., and Z.K.F. designed research; A.S. performed research; entire cortex, which presents a significant challenge. In practice, A.S.F. contributed new reagents/analytic tools; A.S. analyzed data; and A.S., L.M.M., A.S.F., long-range axons are truncated in the reconstruction process, and Z.F.K. wrote the paper. and thus their length and richness (density), and the number of The authors declare no conflict of interest. synapses that they mediate, cannot be estimated reliably. This article is a PNAS Direct Submission. We devised an approach to delineate the fractions of local and 1To whom correspondence should be addressed. E-mail: [email protected]. long-range synaptic connections in different cortical layers. Our This article contains supporting information online at www.pnas.org/cgi/content/full/ method is based on an analysis of dendritic and local axonal 0810390106/DCSupplemental. arbors of 24 excitatory neurons (20 pyramidal and 4 spiny © 2009 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.0810390106 PNAS ͉ March 3, 2009 ͉ vol. 106 ͉ no. 9 ͉ 3555–3560 Downloaded by guest on September 23, 2021 L1 L2/3 L4 L5 L6 Having verified that our method produces reasonable results, A ] 0.5 B -3 we next estimated the volume density of boutons of excitatory 0.4 neuron axons. This calculation is similar to that of the volume density of dendritic spines. Because the axons of excitatory 0.3 neurons in our data set are truncated, we could estimate the 0.2 volume density of boutons only on local axons, that is, axons confined to the domain of the local arbor, as defined by the 0.1 column of radius R (Fig. 1A). The results for 2 definitions of locality, R ϭ 250 ␮m and R ϭ 500 ␮m, are shown in Fig. 1C. 0 Ϯ asymmetric synapses, [µm volume density of spines and 0 500 1000 1500 Layer 2/3 contains the highest density of local boutons, 0.10 ␮ Ϫ3 ϭ ␮ R = 500µm cortical depth, z [µm] 0.02 m for R 500 m. This density decays monotonically toward the deeper layers, similar to the volume density of L1 L2/3 L4 L5 L6 dendritic spines. ] 0.3 D 1 C -3 To estimate the overall volume density of boutons (i.e., the inhibitory 0.8 axons volume density of boutons on local and long-range axons), we 0.2 note that because in cat area 17 most of the boutons on excitatory 0.6 neuron axons contain only a single asymmetric synapse, this excitatory density is approximately equal to the density of asymmetric 0.4 axons 0.1 synapses (14–18). As shown in Fig. 1C, the density of local R = 500µm 0.2 boutons in each layer is only a small fraction of the overall R = 250µm bouton density. Layer 1 contains the highest total density of 0 fraction of local synapses 0 Ϯ ␮ Ϫ3 asymmetric synapses, [µm 0 500 1000 1500 0 100 200 300 400 500 asymmetric synapses, 0.28 0.01 m . In comparison, the volume density of boutons and Ϯ ␮ Ϫ3 cortical depth, z [µm] columnar radius, R [µm] volume density of local boutons in layer 1 is 0.018 0.005 m for R ϭ 500 ␮m, which is smaller by 16-fold. Fig. 1. Local and long-range synapses in the cortical column. (A) Example of Fig. 1D shows how the fractions of local presynaptic terminals a layer 2/3 pyramidal cell reconstructed from cat area 17. The axon is shown in on excitatory and inhibitory axons (or excitatory and inhibitory black, and dendrites are in red. The gray cylinder (radius R ϭ 500 ␮m) synapses) averaged over the entire cortical depth depend on the demarcates the extent of the local axonal arbor.
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