Publications - Salk Institute for Biological Studies

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Adusei, M., Callaway, E.M., Usrey, W.M., Briggs, F. Parallel streams of direct corticogeniculate feedback from mid-level extrastriate cortex in the macaque monkey. (2024) eNeuro. DOI: 10.1523/ENEURO.0364-23.2024

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First order thalamic nuclei receive feedforward signals from peripheral receptors and relay these signals to primary sensory cortex. Primary sensory cortex, in turn, provides reciprocal feedback to first order thalamus. Because the vast majority of sensory thalamocortical inputs target primary sensory cortex, their complementary corticothalamic neurons are assumed to be similarly restricted to primary sensory cortex. We upend this assumption by characterizing morphologically diverse neurons in multiple mid-level visual cortical areas of the primate () brain that provide direct feedback to the primary visual thalamus, the dorsal lateral geniculate nucleus (LGN). Although the majority of geniculocortical neurons project to primary visual cortex (V1), a minority, located mainly in the koniocellular LGN layers, provide direct input to extrastriate visual cortex. These "V1-bypassing" projections may be implicated in blindsight. We hypothesized that geniculocortical inputs directly targeting extrastriate cortex should be complemented by reciprocal corticogeniculate circuits. Using virus-mediated circuit tracing, we discovered corticogeniculate neurons throughout three mid-level extrastriate areas: MT, MST, and V4. Quantitative morphological analyses revealed non-uniform distributions of unique cell types across areas. Many extrastriate corticogeniculate neurons had spiny stellate morphology, suggesting possible targeting of koniocellular LGN layers. Importantly though, multiple morphological types were observed across areas. Such morphological diversity could suggest parallel streams of V1-bypassing corticogeniculate feedback at multiple stages of the visual processing hierarchy. Furthermore, the presence of corticogeniculate neurons across visual cortex necessitates a reevaluation of the LGN as a hub for visual information rather than a simple relay. First order thalamic nuclei are most strongly connected in feedforward and feedback directions with primary sensory cortex. In the visual system, direct feedforward circuits link the visual thalamus with higher-order, extrastriate visual areas, although the function of these less-common pathways remains unknown. Here we demonstrate for the first time the presence of complementary direct feedback connections between multiple extrastriate visual cortical areas and the visual thalamus in the primate brain. Although sparse, extrastriate corticogeniculate circuits are consistently present and contain morphologically diverse neurons, suggesting parallel streams of extrastriate feedback. These findings indicate an evolutionary conservation of circuits that integrate information from throughout the visual processing hierarchy within the visual thalamus.

Wang, H., Dey, O., Lagos, W.N., Behnam, N., Callaway, E.M., Stafford, B.K. Parallel pathways carrying direction-and orientation-selective retinal signals to layer 4 of the mouse visual cortex. (2024) Cell Reports. 43(3):113830. DOI: 10.1016/j.celrep.2024.113830

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Zhang, L.A., Li, P., Callaway, E.M. High-Resolution Laminar Identification in Macaque Primary Visual Cortex Using Neuropixels Probes. (2024) bioRxiv. DOI: 10.1101/2024.01.23.576944

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Zhou, J., Zhang, Z., Wu, M., Liu, H., Pang, Y., Bartlett, A., Peng, Z., Ding, W., Rivkin, A., Lagos, W.N., Williams, E., Lee, C.T., Miyazaki, P.A., Aldridge, A., Zeng, Q., Salinda, J.L.A., Claffey, N., Liem, M., Fitzpatrick, C., Boggeman, L., Yao, Z., Smith, K.A., Tasic, B., Altshul, J., Kenworthy, M.A., Valadon, C., Nery, J.R., Castanon, R.G., Patne, N.S., Vu, M., Rashid, M., Jacobs, M., Ito, T., Osteen, J., Emerson, N., Lee, J., Cho, S., Rink, J., Huang, H.H., Pinto-Duartec, A., Dominguez, B., Smith, J.B., O'Connor, C., Zeng, H., Chen, S., Lee, K.F., Mukamel, E.A., Jin, X., Margarita Behrens, M., Ecker, J.R., Callaway, E.M. Brain-wide correspondence of neuronal epigenomics and distant projections. (2023) Nature. 624(7991):355-365. DOI: 10.1038/s41586-023-06823-w

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Zemke, N.R., Armand, E.J., Wang, W., Lee, S., Zhou, J., Li, Y.E., Liu, H., Tian, W., Nery, J.R., Castanon, R.G., Bartlett, A., Osteen, J.K., Li, D., Zhuo, X., Xu, V., Chang, L., Dong, K., Indralingam, H.S., Rink, J.A., Xie, Y., Miller, M., Krienen, F.M., Zhang, Q., Taskin, N., Ting, J., Feng, G., McCarroll, S.A., Callaway, E.M., Wang, T., Lein, E.S., Behrens, M.M., Ecker, J.R., Ren, B. Conserved and divergent gene regulatory programs of the mammalian neocortex. (2023) Nature. 624(7991):390-402. DOI: 10.1038/s41586-023-06819-6

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Patiño, M., Lagos, W.N., Patne, N.S., Miyazaki, P.A., Bhamidipati, S.K., Collman, F., Callaway, E.M. Postsynaptic cell type and synaptic distance do not determine efficiency of monosynaptic rabies virus spread measured at synaptic resolution. (2023) Elife. 12. DOI: 10.7554/eLife.89297

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Jorstad, N.L., Close, J., Johansen, N., Yanny, A.M., Barkan, E.R., Travaglini, K.J., Bertagnolli, D., Campos, J., Casper, T., Crichton, K., Dee, N., Ding, S.L., Gelfand, E., Goldy, J., Hirschstein, D., Kiick, K., Kroll, M., Kunst, M., Lathia, K., Long, B., Martin, N., McMillen, D., Pham, T., Rimorin, C., Ruiz, A., Shapovalova, N., Shehata, S., Siletti, K., Somasundaram, S., Sulc, J., Tieu, M., Torkelson, A., Tung, H., Callaway, E.M., Hof, P.R., Keene, C.D., Levi, B.P., Linnarsson, S., Mitra, P.P., Smith, K., Hodge, R.D., Bakken, T.E., Lein, E.S. Transcriptomic cytoarchitecture reveals principles of human neocortex organization. (2023) Science. 382(6667):eadf6812. DOI: 10.1126/science.adf6812

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Klug, J.R., Yan, X., Hoffman, H.A., Engelhardt, M.D., Osakada, F., Callaway, E.M., Jin, X. Asymmetric cortical projections to striatal direct and indirect pathways distinctly control actions. (2023) bioRxiv. DOI: 10.1101/2023.10.02.560589

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Wang, H., Dey, O., Lagos, W.N., Behnam, N., Callaway, E.M., Stafford, B.K. Parallel pathways carrying direction and orientation selective retinal signals to layer 4 of mouse visual cortex. (2023) bioRxiv. DOI: 10.1101/2023.09.18.558281

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Zemke, N.R., Armand, E.J., Wang, W., Lee, S., Zhou, J., Li, Y.E., Liu, H., Tian, W., Nery, J.R., Castanon, R.G., Bartlett, A., Osteen, J.K., Li, D., Zhuo, X., Xu, V., Miller, M., Krienen, F.M., Zhang, Q., Taskin, N., Ting, J., Feng, G., McCarroll, S.A., Callaway, E.M., Wang, T., Behrens, M.M., Lein, E.S., Ecker, J.R., Ren, B. Comparative single cell epigenomic analysis of gene regulatory programs in the rodent and primate neocortex. (2023) bioRxiv. DOI: 10.1101/2023.04.08.536119

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Fischer, K.B., Collins, H.K., Pang, Y., Roy, D.S., Zhang, Y., Feng, G., Li, S.J., Kepecs, A., Callaway, E.M. Monosynaptic restriction of the anterograde herpes simplex virus strain H129 for neural circuit tracing. (2023) Journal of Comparative Neurology. DOI: 10.1002/cne.25451

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Li, P., Garg, A.K., Zhang, L.A., Rashid, M.S., Callaway, E.M. Cone opponent functional domains in primary visual cortex combine signals for color appearance mechanisms. (2022) Nature Communications. 13(1):6344. DOI: 10.1038/s41467-022-34020-2

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Wang, H., Dey, O., Lagos, W.N., Callaway, E.M. Diversity in spatial frequency, temporal frequency, and speed tuning across mouse visual cortical areas and layers. (2022) Journal of Comparative Neurology. DOI: 10.1002/cne.25404

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Zhang, Y., Roy, D.S., Zhu, Y., Chen, Y., Aida, T., Hou, Y., Shen, C., Lea, N.E., Schroeder, M.E., Skaggs, K.M., Sullivan, H.A., Fischer, K.B., Callaway, E.M., Wickersham, I.R., Dai, J., Li, X.M., Lu, Z., Feng, G. Targeting thalamic circuits rescues motor and mood deficits in PD mice. (2022) Nature. DOI: 10.1038/s41586-022-04806-x

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Patiño, M., Lagos, W.N., Patne, N.S., Tasic, B., Zeng, H., Callaway, E.M. Single-cell transcriptomic classification of rabies-infected cortical neurons. (2022) Proceedings of the National Academy of Sciences of the United States of America. 119(22):e2203677119. DOI: 10.1073/pnas.2203677119

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Cook, J.R., Li, H., Nguyen, B., Huang, H.H., Mahdavian, P., Kirchgessner, M.A., Strassmann, P., Engelhardt, M., Callaway, E.M., Jin, X. Secondary auditory cortex mediates a sensorimotor mechanism for action timing. (2022) Nature Neuroscience. 25(3):330-344. DOI: 10.1038/s41593-022-01025-5

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Liu, H., Zhou, J., Tian, W., Luo, C., Bartlett, A., Aldridge, A., Lucero, J., Osteen, J.K., Nery, J.R., Chen, H., Rivkin, A., Castanon, R.G., Clock, B., Li, Y.E., Hou, X., Poirion, O.B., Preissl, S., Pinto-Duarte, A., O'Connor, C., Boggeman, L., Fitzpatrick, C., Nunn, M., Mukamel, E.A., Zhang, Z., Callaway, E.M., Ren, B., Dixon, J.R., Behrens, M.M., Ecker, J.R. DNA methylation atlas of the mouse brain at single-cell resolution. (2021) Nature. 598(7879):120-128. DOI: 10.1038/s41586-020-03182-8

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Zhang, Z., Zhou, J., Tan, P., Pang, Y., Rivkin, A.C., Kirchgessner, M.A., Williams, E., Lee, C.T., Liu, H., Franklin, A.D., Miyazaki, P.A., Bartlett, A., Aldridge, A.I., Vu, M., Boggeman, L., Fitzpatrick, C., Nery, J.R., Castanon, R.G., Rashid, M., Jacobs, M.W., Ito-Cole, T., O'Connor, C., Pinto-Duartec, A., Dominguez, B., Smith, J.B., Niu, S.Y., Lee, K.F., Jin, X., Mukamel, E.A., Behrens, M.M., Ecker, J.R., Callaway, E.M. Epigenomic diversity of cortical projection neurons in the mouse brain. (2021) Nature. 598(7879):167-173. DOI: 10.1038/s41586-021-03223-w

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Neuronal cell types are classically defined by their molecular properties, anatomy and functions. Although recent advances in single-cell genomics have led to high-resolution molecular characterization of cell type diversity in the brain, neuronal cell types are often studied out of the context of their anatomical properties. To improve our understanding of the relationship between molecular and anatomical features that define cortical neurons, here we combined retrograde labelling with single-nucleus DNA methylation sequencing to link neural epigenomic properties to projections. We examined 11,827 single neocortical neurons from 63 cortico-cortical and cortico-subcortical long-distance projections. Our results showed unique epigenetic signatures of projection neurons that correspond to their laminar and regional location and projection patterns. On the basis of their epigenomes, intra-telencephalic cells that project to different cortical targets could be further distinguished, and some layer 5 neurons that project to extra-telencephalic targets (L5 ET) formed separate clusters that aligned with their axonal projections. Such separation varied between cortical areas, which suggests that there are area-specific differences in L5 ET subtypes, which were further validated by anatomical studies. Notably, a population of cortico-cortical projection neurons clustered with L5 ET rather than intra-telencephalic neurons, which suggests that a population of L5 ET cortical neurons projects to both targets. We verified the existence of these neurons by dual retrograde labelling and anterograde tracing of cortico-cortical projection neurons, which revealed axon terminals in extra-telencephalic targets including the thalamus, superior colliculus and pons. These findings highlight the power of single-cell epigenomic approaches to connect the molecular properties of neurons with their anatomical and projection properties.

Kirchgessner, M.A., Franklin, A.D., Callaway, E.M. Distinct "driving" versus "modulatory" influences of different visual corticothalamic pathways. (2021) Current Biology. DOI: 10.1016/j.cub.2021.09.025

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Faulkner, R.L., Wall, N.R., Callaway, E.M., Cline, H.T. Application of Recombinant Rabies Virus to Xenopus Tadpole Brain. (2021) eNeuro. DOI: 10.1523/ENEURO.0477-20.2021

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The Xenopus laevis experimental system has provided significant insight into the development and plasticity of neural circuits. Xenopus neuroscience research would be enhanced by additional tools to study neural circuit structure and function. Rabies viruses are powerful tools to label and manipulate neural circuits and have been widely used to study mesoscale connectomics. Whether rabies virus can be used to transduce neurons and express transgenes in Xenopus has not been systematically investigated. Glycoprotein-deleted rabies virus transduces neurons at the axon terminal and retrogradely labels their cell bodies. We show that glycoprotein-deleted rabies virus infects local and projection neurons in the Xenopus tadpole when directly injected into brain tissue. Pseudotyping glycoprotein-deleted rabies with EnvA restricts infection to cells with exogenous expression of the EnvA receptor, TVA. EnvA pseudotyped virus specifically infects tadpole neurons with promoter-driven expression of TVA, demonstrating its utility to label targeted neuronal populations. Neuronal cell types are defined by a combination of features including anatomical location, expression of genetic markers, axon projection sites, morphology, and physiological properties. We show that driving TVA expression in one hemisphere and injecting EnvA pseudotyped virus into the contralateral hemisphere, retrogradely labels neurons defined by cell body location and axon projection site. Using this approach, rabies can be used to identify cell types in Xenopus brain and simultaneously to express transgenes which enable monitoring or manipulation of neuronal activity. This makes rabies a valuable tool to study the structure and function of neural circuits in Xenopus.Studies in Xenopus have contributed a great deal to our understanding of brain circuit development and plasticity, regeneration, and hormonal regulation of behavior and metamorphosis. Here, we show that recombinant rabies virus transduces neurons in the Xenopus tadpole, enlarging the toolbox that can be applied to studying Xenopus brain. Rabies can be used for retrograde labeling and expression of a broad range of transgenes including fluorescent proteins for anatomical tracing and studying neuronal morphology, voltage or calcium indicators to visualize neuronal activity, and photo- or chemosensitive channels to control neuronal activity. The versatility of these tools enables diverse experiments to analyze and manipulate Xenopus brain structure and function, including mesoscale connectivity.

Abbott, L.F., Bock, D.D., Callaway, E.M., Denk, W., Dulac, C., Fairhall, A.L., Fiete, I., Harris, K.M., Helmstaedter, M., Jain, V., Kasthuri, N., LeCun, Y., Lichtman, J.W., Littlewood, P.B., Luo, L., Maunsell, J.H.R., Reid, R.C., Rosen, B.R., Rubin, G.M., Sejnowski, T.J., Seung, H.S., Svoboda, K., Tank, D.W., Tsao, D., Van Essen, D.C. The Mind of a Mouse. (2020) Cell. 182(6):1372-1376. DOI: 10.1016/j.cell.2020.08.010

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Yang, C.F., Kim, E.J., Callaway, E.M., Feldman, J.L. Monosynaptic Projections to Excitatory and Inhibitory preBötzinger Complex Neurons. (2020) Frontiers in Neuroanatomy. 14:58. DOI: 10.3389/fnana.2020.00058

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Kim, E.J., Zhang, Z., Huang, L., Ito-Cole, T., Jacobs, M.W., Juavinett, A.L., Senturk, G., Hu, M., Ku, M., Ecker, J.R., Callaway, E.M. Extraction of Distinct Neuronal Cell Types from within a Genetically Continuous Population. (2020) Neuron. DOI: 10.1016/j.neuron.2020.04.018

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Kirchgessner, M.A., Franklin, A.D., Callaway, E.M. Context-dependent and dynamic functional influence of corticothalamic pathways to first- and higher-order visual thalamus. (2020) Proceedings of the National Academy of Sciences of the United States of America. DOI: 10.1073/pnas.2002080117

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Fischer, K.B., Collins, H.K., Callaway, E.M. Sources of off-target expression from recombinase-dependent AAV vectors and mitigation with cross-over insensitive ATG-out vectors. (2019) Proceedings of the National Academy of Sciences of the United States of America. 116(52):27001–27010. DOI: 10.1073/pnas.1915974116

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Hafner, G., Witte, M., Guy, J., Subhashini, N., Fenno, L.E., Ramakrishnan, C., Kim, Y.S., Deisseroth, K., Callaway, E.M., Oberhuber, M., Conzelmann, K.K., Staiger, J.F. Mapping Brain-Wide Afferent Inputs of Parvalbumin-Expressing GABAergic Neurons in Barrel Cortex Reveals Local and Long-Range Circuit Motifs. (2019) Cell Reports. 28(13):3450-3461.e8. DOI: 10.1016/j.celrep.2019.08.064

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Juavinett, A.L., Kim, E.J., Collins, H.C., Callaway, E.M. A systematic topographical relationship between mouse lateral posterior thalamic neurons and their visual cortical projection targets. (2019) Journal of Comparative Neurology. 528(1):95-107. DOI: 10.1002/cne.24737

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Garg, A.K., Li, P., Rashid, M.S., Callaway, E.M. Color and orientation are jointly coded and spatially organized in primate primary visual cortex. (2019) Science. 364(6447):1275-1279. DOI: 10.1126/science.aaw5868

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McBride, E.G., Lee, S.J., Callaway, E.M. Local and Global Influences of Visual Spatial Selection and Locomotion in Mouse Primary Visual Cortex. (2019) Current Biology. 29(10):1592-1605. DOI: 10.1016/j.cub.2019.03.065

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Bennett, C., Gale, S.D., Garrett, M.E., Newton, M.L., Callaway, E.M., Murphy, G.J., Olsen, S.R. Higher-Order Thalamic Circuits Channel Parallel Streams of Visual Information in Mice. (2019) Neuron. 102(2):477-492. DOI: 10.1016/j.neuron.2019.02.010

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Padmanabhan, K., Osakada, F., Tarabrina, A., Kizer, E., Callaway, E.M., Gage, F.H., Sejnowski, T.J. Centrifugal Inputs to the Main Olfactory Bulb Revealed Through Whole Brain Circuit-Mapping. (2019) Frontiers in Neuroanatomy. 12:115. DOI: 10.3389/fnana.2018.00115

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Yetman, M.J., Washburn, E., Hyun, J.H., Osakada, F., Hayano, Y., Zeng, H., Callaway, E.M., Kwon, H.B., Taniguchi, H. Intersectional monosynaptic tracing for dissecting subtype-specific organization of GABAergic interneuron inputs. (2019) Nature Neuroscience. 22:492-502. DOI: 10.1038/s41593-018-0322-y

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Dhande, O.S., Stafford, B.K., Franke, K., El-Danaf, R., Percival, K.A., Phan, A.H., Li, P., Hansen, B.J., Nguyen, P.L., Berens, P., Taylor, W.R., Callaway, E., Euler, T., Huberman, A.D. Molecular fingerprinting of On-Off direction selective retinal ganglion cells across species and relevance to primate visual circuits. (2018) Journal of Neuroscience. DOI: 10.1523/JNEUROSCI.1784-18.2018

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The ability to detect moving objects is an ethologically salient function. Direction selective neurons have been identified in the retina, thalamus, and cortex of many species, but their homology has remained opaque. For instance, it is unknown whether direction-selective retinal ganglion cells (DSGCs) exist in primates, and if so, whether they are the equivalent to mouse and rabbit DSGCs. Here, we used a molecular/circuit approach in both sexes to address these issues. In mice, we identify the transcription factor Satb2 (Special AT-rich sequence-binding protein 2) as a selective marker for three RGC types: On-Off DSGCs encoding motion in either the anterior or posterior direction, a newly identified type of Off-DSGC and an Off-sustained RGC type. In rabbits, we find that expression of Satb2 is conserved in On-Off DSGCs; however, has evolved to include On-Off DSGCs encoding upward and downward motion, in addition to anterior and posterior motion. Next, we show that macaque RGCs express Satb2 most likely in a single type. We used rabies-virus based circuit mapping tools to reveal the identity of macaque Satb2-RGCs and discovered their dendritic arbors are relatively large and monostratified. Together, these data indicate Satb2-expressing On-Off DSGCs are likely not present in the primate retina. Moreover, if DSGCs are present in the primate retina, it is unlikely that they express Satb2.The ability to detect object-motion is a fundamental feature of almost all visual systems. Here we identify a novel marker for retinal ganglion cells encoding directional motion that is evolutionarily conserved in mice and rabbits, but not in primates. We show that in macaque monkeys the retinal ganglion cells that express this marker comprise a single type and are morphologically distinct from mouse and rabbit direction-selective retinal ganglion cells. Our findings indicate that On-Off direction-selective retinal neurons may have evolutionarily diverged in primates and more generally provide novel insight into the identity and organization of primate parallel visual pathways.

Luo, L., Callaway, E.M., Svoboda, K. Genetic Dissection of Neural Circuits: A Decade of Progress. (2018) Neuron. 98(2):256-281. DOI: 10.1016/j.neuron.2018.03.040

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Callaway, E.M., Garg, A.K. Brain technology: Neurons recorded en masse. (2017) Nature. 551(7679):172-173. DOI: 10.1038/551172a

Juavinett, A.L., Nauhaus, I., Garrett, M.E., Zhuang, J., Callaway, E.M. Automated identification of mouse visual areas with intrinsic signal imaging. (2017) Nature Protocols. 12(1):32-43. DOI: 10.1038/nprot.2016.158

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Suzuki, K., Tsunekawa, Y., Hernandez-Benitez, R., Wu, J., Zhu, J., Kim, E.J., Hatanaka, F., Yamamoto, M., Araoka, T., Li, Z., Kurita, M., Hishida, T., Li, M., Aizawa, E., Guo, S., Chen, S., Goebl, A., Soligalla, R.D., Qu, J., Jiang, T., Fu, X., Jafari, M., Esteban, C.R., Berggren, W.T., Lajara, J., Nuñez-Delicado, E., Guillen, P., Campistol, J.M., Matsuzaki, F., Liu, G.H., Magistretti, P., Zhang, K., Callaway, E.M., Zhang, K., Belmonte, J.C. In vivo genome editing via CRISPR/Cas9 mediated homology-independent targeted integration. (2016) Nature. 540(7631):144-149. DOI: 10.1038/nature20565

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Dimidschstein, J., Chen, Q., Tremblay, R., Rogers, S.L., Saldi, G.A., Guo, L., Xu, Q., Liu, R., Lu, C., Chu, J., Grimley, J.S., Krostag, A.R., Kaykas, A., Avery, M.C., Rashid, M.S., Baek, M., Jacob, A.L., Smith, G.B., Wilson, D.E., Kosche, G., Kruglikov, I., Rusielewicz, T., Kotak, V.C., Mowery, T.M., Anderson, S.A., Callaway, E.M., Dasen, J.S., Fitzpatrick, D., Fossati, V., Long, M.A., Noggle, S., Reynolds, J.H., Sanes, D.H., Rudy, B., Feng, G., Fishell, G. A viral strategy for targeting and manipulating interneurons across vertebrate species. (2016) Nature Neuroscience. 19(12):1743-1749. DOI: 10.1038/nn.4430

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Xu, C., Krabbe, S., Gründemann, J., Botta, P., Fadok, J.P., Osakada, F., Saur, D., Grewe, B.F., Schnitzer, M.J., Callaway, E.M., Lüthi, A. Distinct Hippocampal Pathways Mediate Dissociable Roles of Context in Memory Retrieval. (2016) Cell. 167(4):961-972. DOI: 10.1016/j.cell.2016.09.051

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Tian, J., Huang, R., Cohen, J.Y., Osakada, F., Kobak, D., Machens, C.K., Callaway, E.M., Uchida, N., Watabe-Uchida, M. Distributed and Mixed Information in Monosynaptic Inputs to Dopamine Neurons. (2016) Neuron. 91(6):1374-1389. DOI: 10.1016/j.neuron.2016.08.018

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Barth, L., Burkhalter, A., Callaway, E.M., Connors, B.W., Cauli, B., DeFelipe, J., Feldmeyer, D., Freund, T., Kawaguchi, Y., Kisvarday, Z., Kubota, Y., McBain, C., Oberlaender, M., Rossier, J., Rudy, B., Staiger, J.F., Somogyi, P., Tamas, G., Yuste, R. Comment on "Principles of connectivity among morphologically defined cell types in adult neocortex". (2016) Science. 353(6304):1108. DOI: 10.1126/science.aaf5663

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Smith, J.B., Klug, J.R., Ross, D.L., Howard, C.D., Hollon, N.G., Ko, V.I., Hoffman, H., Callaway, E.M., Gerfen, C.R., Jin, X. Genetic-Based Dissection Unveils the Inputs and Outputs of Striatal Patch and Matrix Compartments. (2016) Neuron. 91(5):1069-1084. DOI: 10.1016/j.neuron.2016.07.046

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Nauhaus, I., Nielsen, K.J., Callaway, E.M. Efficient Receptive Field Tiling in Primate V1. (2016) Neuron. 91(4):893-904. DOI: 10.1016/j.neuron.2016.07.015

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Padmanabhan, K., Osakada, F., Tarabrina, A., Kizer, E., Callaway, E.M., Gage, F.H., Sejnowski, T.J. Diverse Representations of Olfactory Information in Centrifugal Feedback Projections. (2016) Journal of Neuroscience. 36(28):7535-45. DOI: 10.1523/JNEUROSCI.3358-15.2016

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Faget, L., Osakada, F., Duan, J., Ressler, R., Johnson, A.B., Proudfoot, J.A., Yoo, J.H., Callaway, E.M., Hnasko, T.S. Afferent Inputs to Neurotransmitter-Defined Cell Types in the Ventral Tegmental Area. (2016) Cell Reports. 15(12):2796-2808. DOI: 10.1016/j.celrep.2016.05.057

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Kim, E.J., Jacobs, M.W., Ito-Cole, T., Callaway, E.M. Improved Monosynaptic Neural Circuit Tracing Using Engineered Rabies Virus Glycoproteins. (2016) Cell Reports. 15(4):692-699. DOI: 10.1016/j.celrep.2016.03.067

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Wall, N.R., De La Parra, M., Sorokin, J.M., Taniguchi, H., Huang, Z.J., Callaway, E.M. Brain-Wide Maps of Synaptic Input to Cortical Interneurons. (2016) Journal of Neuroscience. 36(14):4000-4009. DOI: 10.1523/JNEUROSCI.3967-15.2016

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Briggs, F., Kiley, C.W., Callaway, E.M., Usrey, W.M. Morphological Substrates for Parallel Streams of Corticogeniculate Feedback Originating in Both V1 and V2 of the Macaque Monkey. (2016) Neuron. 90(2):388-399. DOI: 10.1016/j.neuron.2016.02.038

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Zarrinpar, A., Callaway, E.M. Functional Local Input to Layer 5 Pyramidal Neurons in the Rat Visual Cortex. (2016) Cereb. Cortex. 26(3):991-1003. DOI: 10.1093/cercor/bhu268

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Tuncdemir, S.N., Wamsley, B., Stam, F.J., Osakada, F., Goulding, M., Callaway, E.M., Rudy, B., Fishell, G. Early Somatostatin Interneuron Connectivity Mediates the Maturation of Deep Layer Cortical Circuits. (2016) Neuron. 89(3):521-35. DOI: 10.1016/j.neuron.2015.11.020

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Hasenstaub, A., Otte, S., Callaway, E. Cell Type-Specific Control of Spike Timing by Gamma-Band Oscillatory Inhibition. (2016) Cereb. Cortex. 26(2):797-806. DOI: 10.1093/cercor/bhv044

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Kim, E.J., Juavinett, A.L., Kyubwa, E.M., Jacobs, M.W., Callaway, E.M. Three Types of Cortical Layer 5 Neurons That Differ in Brain-wide Connectivity and Function. (2015) Neuron. 88(6):1253-1267. DOI: 10.1016/j.neuron.2015.11.002

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Callaway, E.M., Luo, L. Monosynaptic Circuit Tracing with Glycoprotein-Deleted Rabies Viruses. (2015) Journal of Neuroscience. 35(24):8979-8985. DOI: 10.1523/JNEUROSCI.0409-15.2015

Juavinett, A.L., Callaway, E.M. Pattern and Component Motion Responses in Mouse Visual Cortical Areas. (2015) Current Biology. 25(13):1759-1764. DOI: 10.1016/j.cub.2015.05.028

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Izpisua Belmonte, J.C., Callaway, E.M., Caddick, S.J., Churchland, P., Feng, G., Homanics, G.E., Lee, K.F., Leopold, D.A., Miller, C.T., Mitchell, J.F., Mitalipov, S., Moutri, A.R., Movshon, J.A., Okano, H., Reynolds, J.H., Ringach, D., Sejnowski, T.J., Silva, A.C., Strick, P.L., Wu, J., Zhang, F. Brains, genes, and primates. (2015) Neuron. 86(3):617-31. DOI: 10.1016/j.neuron.2015.03.021

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Li, P.H., Gauthier, J.L., Schiff, M., Sher, A., Ahn, D., Field, G.D., Greschner, M., Callaway, E.M., Litke, A.M., Chichilnisky, E.J. Anatomical identification of extracellularly recorded cells in large-scale multielectrode recordings. (2015) Journal of Neuroscience. 35(11):4663-4675. DOI: 10.1523/JNEUROSCI.3675-14.2015

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Garrett, M.E., Nauhaus, I., Marshel, J.H., Callaway, E.M. Topography and areal organization of mouse visual cortex. (2014) Journal of Neuroscience. 34(37):12587-12600. DOI: 10.1523/JNEUROSCI.1124-14.2014

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Ni, Y., Nawabi, H., Liu, X., Yang, L., Miyamichi, K., Tedeschi, A., Xu, B., Wall, N.R., Callaway, E.M., He, Z. Characterization of long descending premotor propriospinal neurons in the spinal cord. (2014) Journal of Neuroscience. 34(28):9404-9417. DOI: 10.1523/JNEUROSCI.1771-14.2014

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Cetin, A., Callaway, E.M. Optical control of retrogradely infected neurons using drug-regulated "TLoop" lentiviral vectors. (2014) Journal of Neurophysiology. 111(10):2150-2159. DOI: 10.1152/jn.00495.2013

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Sun, Y., Nguyen, A.Q., Nguyen, J.P., Le, L., Saur, D., Choi, J., Callaway, E.M., Xu, X. Cell-type-specific circuit connectivity of hippocampal CA1 revealed through Cre-dependent rabies tracing. (2014) Cell Reports. 7(1):269-280. DOI: 10.1016/j.celrep.2014.02.030

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Cruz-Martín, A., El-Danaf, R.N., Osakada, F., Sriram, B., Dhande, O.S., Nguyen, P.L., Callaway, E.M., Ghosh, A., Huberman, A.D. A dedicated circuit links direction-selective retinal ganglion cells to the primary visual cortex. (2014) Nature. 507(7492):358-361. DOI: 10.1038/nature12989

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Ruiz, O., Lustig, B.R., Nassi, J.J., Cetin, A., Reynolds, J.H., Albright, T.D., Callaway, E.M., Stoner, G.R., Roe, A.W. Optogenetics through windows on the brain in the nonhuman primate. (2013) Journal of Neurophysiology. 110(6):1455-67. DOI: 10.1152/jn.00153.2013

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Osakada, F., Callaway, E.M. Design and generation of recombinant rabies virus vectors. (2013) Nature Protocols. 8(8):1583-1601. DOI: 10.1038/nprot.2013.094

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Nienborg, H., Hasenstaub, A., Nauhaus, I., Taniguchi, H., Huang, Z.J., Callaway, E.M. Contrast dependence and differential contributions from somatostatin- and parvalbumin-expressing neurons to spatial integration in mouse V1. (2013) Journal of Neuroscience. 33(27):11145-11154. DOI: 10.1523/JNEUROSCI.5320-12.2013

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Wall, N.R., De La Parra, M., Callaway, E.M., Kreitzer, A.C. Differential innervation of direct- and indirect-pathway striatal projection neurons. (2013) Neuron. 79(2):347-360. DOI: 10.1016/j.neuron.2013.05.014

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Li, Y., Stam, F.J., Aimone, J.B., Goulding, M., Callaway, E.M., Gage, F.H. Molecular layer perforant path-associated cells contribute to feed-forward inhibition in the adult dentate gyrus. (2013) Proceedings of the National Academy of Sciences of the United States of America. 110(22):9106-11. DOI: 10.1073/pnas.1306912110

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Yin, L., Geng, Y., Osakada, F., Sharma, R., Cetin, A.H., Callaway, E.M., Williams, D.R., Merigan, W.H. Imaging light responses of retinal ganglion cells in the living mouse eye. (2013) Journal of Neurophysiology. 109(9):2415-2421. DOI: 10.1152/jn.01043.2012

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Nauhaus, I., Nielsen, K.J., Disney, A.A., Callaway, E.M. Orthogonal micro-organization of orientation and spatial frequency in primate primary visual cortex. (2012) Nature Neuroscience. 15(12):1683-1690. DOI: 10.1038/nn.3255

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Marshel, J.H., Kaye, A.P., Nauhaus, I., Callaway, E.M. Anterior-posterior direction opponency in the superficial mouse lateral geniculate nucleus. (2012) Neuron. 76(4):713-720. DOI: 10.1016/j.neuron.2012.09.021

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Callaway, E.M., Marder, E. Common features of diverse circuits. (2012) Current Opinion in Neurobiology. 22(4):565-567. DOI: 10.1016/j.conb.2012.07.003

Nielsen, K.J., Callaway, E.M., Krauzlis, R.J. Viral vector-based reversible neuronal inactivation and behavioral manipulation in the macaque monkey. (2012) Frontiers in Systems Neuroscience. 6:48. DOI: 10.3389/fnsys.2012.00048

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Li, Y., Aimone, J.B., Xu, X., Callaway, E.M., Gage, F.H. Development of GABAergic inputs controls the contribution of maturing neurons to the adult hippocampal network. (2012) Proceedings of the National Academy of Sciences of the United States of America. 109(11):4290-5. DOI: 10.1073/pnas.1120754109

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Nauhaus, I., Nielsen, K.J., Callaway, E.M. Nonlinearity of two-photon Ca2+ imaging yields distorted measurements of tuning for V1 neuronal populations. (2012) Journal of Neurophysiology. 107(3):923-936. DOI: 10.1152/jn.00725.2011

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Vivar, C., Potter, M.C., Choi, J., Lee, J.Y., Stringer, T.P., Callaway, E.M., Gage, F.H., Suh, H., van Praag, H. Monosynaptic inputs to new neurons in the dentate gyrus. (2012) Nature Communications. 3:1107. DOI: 10.1038/ncomms2101

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Nhan, H.L., Callaway, E.M. Morphology of superior colliculus- and middle temporal area-projecting neurons in primate primary visual cortex. (2012) Journal of Comparative Neurology. 520(1):52-80. DOI: 10.1002/cne.22685

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Marshel, J.H., Garrett, M.E., Nauhaus, I., Callaway, E.M. Functional specialization of seven mouse visual cortical areas. (2011) Neuron. 72(6):1040-1054. DOI: 10.1016/j.neuron.2011.12.004

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Choi, J., Callaway, E.M. Monosynaptic inputs to ErbB4-expressing inhibitory neurons in mouse primary somatosensory cortex. (2011) Journal of Comparative Neurology. 519(17):3402-3414. DOI: 10.1002/cne.22680

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Osakada, F., Mori, T., Cetin, A.H., Marshel, J.H., Virgen, B., Callaway, E.M. New rabies virus variants for monitoring and manipulating activity and gene expression in defined neural circuits. (2011) Neuron. 71(4):617-631. DOI: 10.1016/j.neuron.2011.07.005

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Callaway, E.M., Borrell, V. Developmental sculpting of dendritic morphology of layer 4 neurons in visual cortex: influence of retinal input. (2011) Journal of Neuroscience. 31(20):7456-7470. DOI: 10.1523/JNEUROSCI.5222-10.2011

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Miyamichi, K., Amat, F., Moussavi, F., Wang, C., Wickersham, I., Wall, N.R., Taniguchi, H., Tasic, B., Huang, Z.J., He, Z., Callaway, E.M., Horowitz, M.A., Luo, L. Cortical representations of olfactory input by trans-synaptic tracing. (2011) Nature. 472(7342):191-196. DOI: 10.1038/nature09714

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Wall, N.R., Wickersham, I.R., Cetin, A., De La Parra, M., Callaway, E.M. Monosynaptic circuit tracing in vivo through Cre-dependent targeting and complementation of modified rabies virus. (2010) Proceedings of the National Academy of Sciences of the United States of America. 107(50):21848-21853. DOI: 10.1073/pnas.1011756107

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Weible, A.P., Schwarcz, L., Wickersham, I.R., Deblander, L., Wu, H., Callaway, E.M., Seung, H.S., Kentros, C.G. Transgenic targeting of recombinant rabies virus reveals monosynaptic connectivity of specific neurons. (2010) Journal of Neuroscience. 30(49):16509-16513. DOI: 10.1523/JNEUROSCI.2442-10.2010

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Heider, B., Nathanson, J.L., Isacoff, E.Y., Callaway, E.M., Siegel, R.M. Two-photon imaging of calcium in virally transfected striate cortical neurons of behaving monkey. (2010) PLOS One. 5(11). DOI: 10.1371/journal.pone.0013829

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Haubensak, W., Kunwar, P.S., Cai, H., Ciocchi, S., Wall, N.R., Ponnusamy, R., Biag, J., Dong, H.W., Deisseroth, K., Callaway, E.M., Fanselow, M.S., Lüthi, A., Anderson, D.J. Genetic dissection of an amygdala microcircuit that gates conditioned fear. (2010) Nature. 468(7321):270-276. DOI: 10.1038/nature09553

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Hasenstaub, A.R., Callaway, E.M. Paint it black (or red, or green): optical and genetic tools illuminate inhibitory contributions to cortical circuit function. (2010) Neuron. 67(5):681-684. DOI: 10.1016/j.neuron.2010.08.039

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Choi, J., Young, J.A., Callaway, E.M. Selective viral vector transduction of ErbB4 expressing cortical interneurons in vivo with a viral receptor-ligand bridge protein. (2010) Proceedings of the National Academy of Sciences of the United States of America. 107(38):16703-16708. DOI: 10.1073/pnas.1006233107

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Marshel, J.H., Mori, T., Nielsen, K.J., Callaway, E.M. Targeting single neuronal networks for gene expression and cell labeling in vivo. (2010) Neuron. 67(4):562-574. DOI: 10.1016/j.neuron.2010.08.001

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Hasenstaub, A., Otte, S., Callaway, E., Sejnowski, T.J. Metabolic cost as a unifying principle governing neuronal biophysics. (2010) Proceedings of the National Academy of Sciences of the United States of America. 107(27):12329-34. DOI: 10.1073/pnas.0914886107

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Otte, S., Hasenstaub, A., Callaway, E.M. Cell type-specific control of neuronal responsiveness by gamma-band oscillatory inhibition. (2010) Journal of Neuroscience. 30(6):2150-2159. DOI: 10.1523/JNEUROSCI.4818-09.2010

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Xu, X., Roby, K.D., Callaway, E.M. Immunochemical characterization of inhibitory mouse cortical neurons: three chemically distinct classes of inhibitory cells. (2010) Journal of Comparative Neurology. 518(3):389-404. DOI: 10.1002/cne.22229

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Lyon, D.C., Nassi, J.J., Callaway, E.M. A disynaptic relay from superior colliculus to dorsal stream visual cortex in macaque monkey. (2010) Neuron. 65(2):270-279. DOI: 10.1016/j.neuron.2010.01.003

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Nathanson, J.L., Jappelli, R., Scheeff, E.D., Manning, G., Obata, K., Brenner, S., Callaway, E.M. Short Promoters in Viral Vectors Drive Selective Expression in Mammalian Inhibitory Neurons, but do not Restrict Activity to Specific Inhibitory Cell-Types. (2009) Front Neural Circuits. 3:19. DOI: 10.3389/neuro.04.019.2009

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Wehr, M., Hostick, U., Kyweriga, M., Tan, A., Weible, A.P., Wu, H., Wu, W., Callaway, E.M., Kentros, C. Transgenic silencing of neurons in the mammalian brain by expression of the allatostatin receptor (AlstR). (2009) Journal of Neurophysiology. 102(4):2554-2562. DOI: 10.1152/jn.00480.2009

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Nathanson, J.L., Yanagawa, Y., Obata, K., Callaway, E.M. Preferential labeling of inhibitory and excitatory cortical neurons by endogenous tropism of adeno-associated virus and lentivirus vectors. (2009) Neuroscience. 161(2):441-450. DOI: 10.1016/j.neuroscience.2009.03.032

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Nassi, J.J., Callaway, E.M. Parallel processing strategies of the primate visual system. (2009) Nature Reviews Neuroscience. 10(5):360-372. DOI: 10.1038/nrn2619

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Xu, X., Callaway, E.M. Laminar specificity of functional input to distinct types of inhibitory cortical neurons. (2009) Journal of Neuroscience. 29(1):70-85. DOI: 10.1523/JNEUROSCI.4104-08.2009

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Callaway, E.M. Transneuronal circuit tracing with neurotropic viruses. (2008) Current Opinion in Neurobiology. 18(6):617-623. DOI: 10.1016/j.conb.2009.03.007

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Barbour, D.L., Callaway, E.M. Excitatory local connections of superficial neurons in rat auditory cortex. (2008) Journal of Neuroscience. 28(44):11174-11185. DOI: 10.1523/JNEUROSCI.2093-08.2008

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Tan, W., Janczewski, W.A., Yang, P., Shao, X.M., Callaway, E.M., Feldman, J.L. Silencing preBötzinger complex somatostatin-expressing neurons induces persistent apnea in awake rat. (2008) Nature Neuroscience. 11(5):538-540. DOI: 10.1038/nn.2104

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Larsen, D.D., Wickersham, I.R., Callaway, E.M. Retrograde tracing with recombinant rabies virus reveals correlations between projection targets and dendritic architecture in layer 5 of mouse barrel cortex. (2008) Front Neural Circuits. 1:5. DOI: 10.3389/neuro.04.005.2007

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Luo, L., Callaway, E.M., Svoboda, K. Genetic dissection of neural circuits. (2008) Neuron. 57(5):634-660. DOI: 10.1016/j.neuron.2008.01.002

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Nielsen, K.J., Callaway, E.M. More than a feeling: sensation from cortical stimulation. (2008) Nature Neuroscience. 11(1):10-11. DOI: 10.1038/nn0108-10

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Nassi, J.J., Callaway, E.M. Specialized circuits from primary visual cortex to V2 and area MT. (2007) Neuron. 55(5):799-808. DOI: 10.1016/j.neuron.2007.07.037

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Wickersham, I.R., Lyon, D.C., Barnard, R.J., Mori, T., Finke, S., Conzelmann, K.K., Young, J.A., Callaway, E.M. Monosynaptic restriction of transsynaptic tracing from single, genetically targeted neurons. (2007) Neuron. 53(5):639-647. DOI: 10.1016/j.neuron.2007.01.033

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Wickersham, I.R., Finke, S., Conzelmann, K.K., Callaway, E.M. Retrograde neuronal tracing with a deletion-mutant rabies virus. (2007) Nature Methods. 4(1):47-49. DOI: 10.1038/nmeth999

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Nassi, J.J., Callaway, E.M. Multiple circuits relaying primate parallel visual pathways to the middle temporal area. (2006) Journal of Neuroscience. 26(49):12789-12798. DOI: 10.1523/JNEUROSCI.4044-06.2006

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Sceniak, M.P., Chatterjee, S., Callaway, E.M. Visual spatial summation in macaque geniculocortical afferents. (2006) Journal of Neurophysiology. 96(6):3474-3484. DOI: 10.1152/jn.00734.2006

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Xu, X., Roby, K.D., Callaway, E.M. Mouse cortical inhibitory neuron type that coexpresses somatostatin and calretinin. (2006) Journal of Comparative Neurology. 499(1):144-160. DOI: 10.1002/cne.21101

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Borrell, V., Kaspar, B.K., Gage, F.H., Callaway, E.M. In vivo evidence for radial migration of neurons by long-distance somal translocation in the developing ferret visual cortex. (2006) Cereb. Cortex. 16(11):1571-83. DOI: 10.1093/cercor/bhj094

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Callaway, E.M., Sanes, J.R. New technologies. (2006) Current Opinion in Neurobiology. 16(5):540-542. DOI: 10.1016/j.conb.2006.08.014

Tan, E.M., Yamaguchi, Y., Horwitz, G.D., Gosgnach, S., Lein, E.S., Goulding, M., Albright, T.D., Callaway, E.M. Selective and quickly reversible inactivation of mammalian neurons in vivo using the Drosophila allatostatin receptor. (2006) Neuron. 51(2):157-70. DOI: 10.1016/j.neuron.2006.06.018

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Nassi, J.J., Lyon, D.C., Callaway, E.M. The parvocellular LGN provides a robust disynaptic input to the visual motion area MT. (2006) Neuron. 50(2):319-327. DOI: 10.1016/j.neuron.2006.03.019

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Callaway, E.M. Should I stay or should I go? Presynaptic boutons in the adult cortex still haven't made up their minds. (2006) Neuron. 49(6):780-783. DOI: 10.1016/j.neuron.2006.03.007

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Gosgnach, S., Lanuza, G.M., Butt, S.J., Saueressig, H., Zhang, Y., Velasquez, T., Riethmacher, D., Callaway, E.M., Kiehn, O., Goulding, M. V1 spinal neurons regulate the speed of vertebrate locomotor outputs. (2006) Nature. 440(7081):215-9. DOI: 10.1038/nature04545

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Zarrinpar, A., Callaway, E.M. Local connections to specific types of layer 6 neurons in the rat visual cortex. (2006) Journal of Neurophysiology. 95(3):1751-1761. DOI: 10.1152/jn.00974.2005

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Larsen, D.D., Callaway, E.M. Development of layer-specific axonal arborizations in mouse primary somatosensory cortex. (2006) Journal of Comparative Neurology. 494(3):398-414. DOI: 10.1002/cne.20754

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Yoshimura, Y., Callaway, E.M. Fine-scale specificity of cortical networks depends on inhibitory cell type and connectivity. (2005) Nature Neuroscience. 8(11):1552-1559. DOI: 10.1038/nn1565

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Callaway, E.M. Structure and function of parallel pathways in the primate early visual system. (2005) Journal of Physiology. 566(Pt 1):13-19. DOI: 10.1113/jphysiol.2005.088047

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Briggs, F., Callaway, E.M. Laminar patterns of local excitatory input to layer 5 neurons in macaque primary visual cortex. (2005) Cereb. Cortex. 15(5):479-488. DOI: 10.1093/cercor/bhh154

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Borrell, V., Yoshimura, Y., Callaway, E.M. Targeted gene delivery to telencephalic inhibitory neurons by directional in utero electroporation. (2005) Journal of Neuroscience Methods. 143(2):151-158. DOI: 10.1016/j.jneumeth.2004.09.027

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Callaway, E.M. A molecular and genetic arsenal for systems neuroscience. (2005) Trends in Neurosciences. 28(4):196-201. DOI: 10.1016/j.tins.2005.01.007

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Lein, E.S., Callaway, E.M., Albright, T.D., Gage, F.H. Redefining the boundaries of the hippocampal CA2 subfield in the mouse using gene expression and 3-dimensional reconstruction. (2005) Journal of Comparative Neurology. 485(1):1-10. DOI: 10.1002/cne.20426

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Yoshimura, Y., Dantzker, J.L., Callaway, E.M. Excitatory cortical neurons form fine-scale functional networks. (2005) Nature. 433(7028):868-873. DOI: 10.1038/nature03252

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Callaway, E.M. Neural substrates within primary visual cortex for interactions between parallel visual pathways. (2005) Progress in Brain Research. 149:59-64. DOI: 10.1016/S0079-6123(05)49005-6

Siegel, R.M., Callaway, E.M. Francis Crick's legacy for neuroscience: between the alpha and the Omega. (2004) PLOS Biology. 2(12). DOI: 10.1371/journal.pbio.0020419

Horwitz, G.D., Callaway, E.M. Antisense inhibition of reward learning. (2004) Nature Neuroscience. 7(10):1023-1024. DOI: 10.1038/nn1004-1023

Callaway, E.M. Close encounters: how cortical neurons find and connect to their correct synaptic partners depends on the cell type. (2004) Neuron. 43(2):156-158. DOI: 10.1016/j.neuron.2004.07.006

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Callaway, E.M. Feedforward, feedback and inhibitory connections in primate visual cortex. (2004) Neural Networks. 17(5-6):625-632. DOI: 10.1016/j.neunet.2004.04.004

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Brivanlou, I.H., Dantzker, J.L., Stevens, C.F., Callaway, E.M. Topographic specificity of functional connections from hippocampal CA3 to CA1. (2004) Proceedings of the National Academy of Sciences of the United States of America. 101(8):2560-2565.

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Chatterjee, S., Callaway, E.M. Parallel colour-opponent pathways to primary visual cortex. (2003) Nature. 426(6967):668-671. DOI: 10.1038/nature02167

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Callaway, E.M. Orientation tuning--a crooked path to the straight and narrow. (2002) Neuron. 36(5):783-785.

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Callaway, E.M., Yuste, R. Stimulating neurons with light. (2002) Current Opinion in Neurobiology. 12(5):587-592.

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Chatterjee, S., Callaway, E.M. S cone contributions to the magnocellular visual pathway in macaque monkey. (2002) Neuron. 35(6):1135-1146.

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Borrell, V., Callaway, E.M. Reorganization of exuberant axonal arbors contributes to the development of laminar specificity in ferret visual cortex. (2002) Journal of Neuroscience. 22(15):6682-6695. DOI: 20026663

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Lechner, H.A., Lein, E.S., Callaway, E.M. A genetic method for selective and quickly reversible silencing of Mammalian neurons. (2002) Journal of Neuroscience. 22(13):5287-5290. DOI: 20026527

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Callaway, E.M. Cell type specificity of local cortical connections. (2002) Journal of Neurocytology. 31(3-5):231-237.

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Callaway, E.M. Neural mechanisms for the generation of visual complex cells. (2001) Neuron. 32(3):378-380.

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Briggs, F., Callaway, E.M. Layer-specific input to distinct cell types in layer 6 of monkey primary visual cortex. (2001) Journal of Neuroscience. 21(10):3600-3608.

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Yabuta, N.H., Sawatari, A., Callaway, E.M. Two functional channels from primary visual cortex to dorsal visual cortical areas. (2001) Science. 292(5515):297-300. DOI: 10.1126/science.1057916

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Butler, A.K., Dantzker, J.L., Shah, R.B., Callaway, E.M. Development of visual cortical axons: layer-specific effects of extrinsic influences and activity blockade. (2001) Journal of Comparative Neurology. 430(3):321-331.

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Yabuta, N.H., Butler, A.K., Callaway, E.M. Laminar specificity of local circuits in barrel cortex of ephrin-A5 knockout mice. (2000) Journal of Neuroscience. 20(15):RC88.

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Dantzker, J.L., Callaway, E.M. Laminar sources of synaptic input to cortical inhibitory interneurons and pyramidal neurons. (2000) Nature Neuroscience. 3(7):701-707. DOI: 10.1038/76656

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Sawatari, A., Callaway, E.M. Diversity and cell type specificity of local excitatory connections to neurons in layer 3B of monkey primary visual cortex. (2000) Neuron. 25(2):459-471.

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Furuta, T., Wang, S.S., Dantzker, J.L., Dore, T.M., Bybee, W.J., Callaway, E.M., Denk, W., Tsien, R.Y. Brominated 7-hydroxycoumarin-4-ylmethyls: photolabile protecting groups with biologically useful cross-sections for two photon photolysis. (1999) Proceedings of the National Academy of Sciences of the United States of America. 96(4):1193-1200.

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Yabuta, N.H., Callaway, E.M. Cytochrome-oxidase blobs and intrinsic horizontal connections of layer 2/3 pyramidal neurons in primate V1. (1998) Visual Neuroscience. 15(6):1007-1027.

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Pyramidal neurons in superficial layers of cerebral cortex have extensive horizontal axons that provide a substrate for lateral interactions across cortical columns. These connections are believed to link functionally similar regions, as suggested by the observation that cytochrome-oxidase blobs in the monkey primary visual cortex (V1) are preferentially connected to blobs and interblobs to interblobs. To better understand the precise relationship between horizontal connections and blobs, we intracellularly labeled 20 layer 2/3 pyramidal neurons in tangential living brain slices from V1 of macaque monkeys. The locations of each cell body and the cell's synaptic boutons relative to blobs were quantitatively analyzed. We found evidence for two cell types located at characteristic distances from blob centers: (1) neurons lacking long-distance, clustered axons (somata 130-200 microm from blob centers) and (2) cells with clustered, long-distance axon collaterals (somata < 130 microm or >200 microm from blob centers). For all cells, synaptic boutons close to the cell body were located at similar distances from blob centers as the cell body. The majority of boutons from cells lacking distal axon clusters were close to their cell bodies. Cells located more than 200 microm from blob centers were in interblobs and had long-distance clustered axon collaterals selectively targeting distant interblob regions. Cells located less than 130 microm from blob centers were found within both blobs and interblobs, but many were close to traditionally defined borders. The distant synaptic boutons from these cells were generally located relatively near to blob centers, but the neurons closest to blob centers had synaptic boutons closer to blob centers than those farther away. There was not a sharp transition that would suggest specificity for blobs and interblobs as discrete, binary entities. Instead they appear to be extremes along a continuum. These observations have important implications for the function of lateral interactions within V1.

Yabuta, N.H., Callaway, E.M. Functional streams and local connections of layer 4C neurons in primary visual cortex of the macaque monkey. (1998) Journal of Neuroscience. 18(22):9489-9499.

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The primate visual system is composed of multiple, functionally specialized cortical areas. The functional diversity among areas is thought to reflect different contributions from early parallel visual pathways to the area V1 neurons providing input to "higher" cortical areas. The M pathway is believed to provide information about motion and contrast, via layer 4B of V1, to dorsal visual areas. The P pathway is believed to provide information about shape and color, via layer 2/3 of V1, to ventral visual areas, with specialized contributions from cytochrome-oxidase (CO) blob versus interblob neurons. However, the detailed anatomical relationships between the M and P pathways and the neurons in V1 that provide input to higher extrastriate cortical areas are poorly understood. To study these relationships, spiny stellate neurons in the M- and P-recipient layers of V1, 4Calpha and 4Cbeta, respectively, were intracellularly labeled, and their axonal and dendritic arbors were reconstructed. We find that neurons with dendrites in upper layer 4Calpha project axons to layer 4B and CO blobs in layer 2/3, thus relaying M input to these regions. Other neurons in lower layer 4Calpha provide M input to interblobs. These cells have either (1) dendrites restricted to lower layer 4Calpha and axons specifically targeting layer 2/3 interblobs, or (2) dendrites in lower 4Calpha and 4Cbeta and axons targeting blobs and interblobs. P-recipient layer 4Cbeta neurons have dense axonal arbors in both blobs and interblobs but not layer 4B. Quantitative analyses reveal that 4Calpha cells provide approximately five times more synapses than 4Cbeta cells to layer 4B, whereas 4Cbeta cells provide five times more synapses than 4Calpha cells to layer 2/3. These observations imply that M input is dominant in layer 4B. In layer 2/3, both blobs and interblobs receive M and P input, but the P input is dominant, and M input to interblobs derives exclusively from a subpopulation of M afferents that targets lower 4Calpha, not from afferents targeting only upper 4Calpha (cf. Blasdel and Lund, 1983). We speculate that the M and P pathways to interblobs are "X-like" linear systems, whereas blobs also receive nonlinear "Y-like" M input.

Dantzker, J.L., Callaway, E.M. The development of local, layer-specific visual cortical axons in the absence of extrinsic influences and intrinsic activity. (1998) Journal of Neuroscience. 18(11):4145-4154.

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Callaway, E.M. Visual scenes and cortical neurons: what you see is what you get. (1998) Proceedings of the National Academy of Sciences of the United States of America. 95(7):3344-3345.

Callaway, E.M. Prenatal development of layer-specific local circuits in primary visual cortex of the macaque monkey. (1998) Journal of Neuroscience. 18(4):1505-1527.

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Previous studies have demonstrated that axonal arbors specific for the four main cortical layers - 2/3, 4, 5, and 6 - develop precisely from the outset using activity-independent cues. In macaque primary visual cortex (V1), layer 2/3 is subdivided into layers named 2/3A, 3B, 4A, and 4B, and layer 4 is subdivided into 4Calpha and 4Cbeta. Individual neurons in V1 of mature macaques have axonal arbors that are highly specific for these sublayers. We have studied the prenatal development of laminar and sublaminar specificity of local circuits in macaque V1. Two-hundred thirty-eight neurons were labeled intracellularly in living brain slices prepared from V1 of five prenatal macaque monkeys aged 100 to 145 d postconception (E100-E145). Axonal and dendritic arbors of labeled neurons were reconstructed to assess their relationships to the cortical layers. We find that developing spiny neurons in layers 2-4B and layer 5 specifically target superficial and deep layers without forming "incorrect" branches in layer 4C. Similarly, layer 6 pyramidal neurons that target layer 4C do not form "incorrect" branches in layer 5. These results indicate that specific projections to the main cortical layers develop with a high degree of selectivity, as in other species. However, the development of sublayer-specific projections was not always precise from the outset. Unlike postnatal animals, axons of some prenatal layer 4Cbeta spiny neurons branch in layer 4B. At similar ages, many pyramidal neurons in the upper half of layer 6 have axonal branches in layer 4Calpha as well as 4Cbeta; these projections are specific for 4Cbeta in more mature animals. Also, there is similar "exuberance" in axonal arbors of other layer 6 cell types. Transient projections were also observed in the subplate and to the white matter for cells from all layers, except 4Cbeta. These observations indicate that at least some sublayer-specific projections emerge by elimination of exuberant axonal branches and suggest that they may use activity-dependent mechanisms to identify "correct" target layers. Such cues could be provided by laminar differences in the patterns of spontaneous prenatal activity in the retino-geniculo-cortical network.

Callaway, E.M. Local circuits in primary visual cortex of the macaque monkey. (1998) Annual Review of Neuroscience. 21:47-74. DOI: 10.1146/annurev.neuro.21.1.47

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Wiser, A.K., Callaway, E.M. Ocular dominance columns and local projections of layer 6 pyramidal neurons in macaque primary visual cortex. (1997) Developmental Biology. 14(2):241-251.

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Callaway, E.M., Lieber, J.L. Development of axonal arbors of layer 6 pyramidal neurons in ferret primary visual cortex. (1996) Journal of Comparative Neurology. 376(2):295-305. DOI: 10.1002/(SICI)1096-9861(19961209)376:2<295::AID

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Callaway, E.M., Wiser, A.K. Contributions of individual layer 2-5 spiny neurons to local circuits in macaque primary visual cortex. (1996) Visual Neuroscience. 13(5):907-922.

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Sawatari, A., Callaway, E.M. Convergence of magno- and parvocellular pathways in layer 4B of macaque primary visual cortex. (1996) Nature. 380(6573):442-446. DOI: 10.1038/380442a0

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Wiser, A.K., Callaway, E.M. Contributions of individual layer 6 pyramidal neurons to local circuitry in macaque primary visual cortex. (1996) Journal of Neuroscience. 16(8):2724-2739.

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Callaway, E.M. Caged neurotransmitters. Shedding light on neural circuits. (1994) Current Biology. 4(11):1010-1012.

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Callaway, E.M., Katz, L.C. Photostimulation using caged glutamate reveals functional circuitry in living brain slices. (1993) Proceedings of the National Academy of Sciences of the United States of America. 90(16):7661-7665.

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Katz, L.C., Callaway, E.M. Development of local circuits in mammalian visual cortex. (1992) Annual Review of Neuroscience. 15:31-56. DOI: 10.1146/annurev.ne.15.030192.000335

Callaway, E.M., Katz, L.C. Development of axonal arbors of layer 4 spiny neurons in cat striate cortex. (1992) Journal of Neuroscience. 12(2):570-582.

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Spiny neurons in layer 4 of cat striate cortex are the primary recipients of geniculocortical afferents and provide crucial links to other cortical layers for processing visual information. Using intracellular staining, we examined the development of the local axonal projections of these neurons to determine (1) whether the laminar specificity of their projections emerged specifically or was sculpted from transient exuberant projections and (2) whether the emergence of excitatory connections from layer 4 to layer 2/3 could contribute to the activity-dependent development of clustered horizontal connections of layer 2/3 pyramidal neurons. Differences in the extent of projections to infragranular (layers 5 and 6, which receive sparse projections) versus superficial layers (layers 2/3 and 4, which receive extensive projections) developed specifically from the outset. By postnatal day 15 (P15) projections to infragranular layers matured and were indistinguishable from those in the oldest animal studied (P33). In contrast, projections to superficial layers continued to increase in complexity after P15. Projections within layer 4, which were the most elaborate at all ages studied, reached maturity at about P20, while those to layer 2/3 continued to increase in complexity through P33. No evidence for exuberant projections to any of these cortical layers was observed. At very early postnatal ages (P5) projections to the subplate region were evident. These disappeared by P8-P11, suggesting the presence of transient connections from layer 4 spiny neurons to subplate neurons. Binocular deprivation did not prevent the emergence of projections from layer 4 spiny neurons into layer 2/3 or development of normal laminar differences in projection density. Connections from layer 4 to layer 2/3 emerged after horizontal connections in layer 2/3 were crudely clustered, but in synchrony with the later refinement of clusters. Collaterals from layer 4 cells first crossed into layer 3 at P11, but were extremely short (extending only 50-200 microns beyond the laminar boundary) and uncommon (only 4 of 19 cells). Since by P8 horizontal projections of layer 2/3 pyramidal neurons are already crudely clustered, the emergence of crude clustering is probably independent of layer 4 to layer 2/3 excitatory projections. The proportion of cells projecting to layer 2/3 and the complexity of their arbors both increased in the subsequent weeks, closely matching the timing of both the refinement of crudely clustered horizontal connections and the emergence of visual responsiveness in layer 2/3.(ABSTRACT TRUNCATED AT 400 WORDS)

Callaway, E.M., Katz, L.C. Emergence and refinement of clustered horizontal connections in cat striate cortex. (1990) Journal of Neuroscience. 10(4):1134-1153.

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Pyramidal cells in layer 2/3 of adult cat striate cortex have long, intrinsic horizontal axon collaterals within both layer 2/3 and layer 5. These collaterals form periodic "clusters" of finer axon branches that link columns of similar orientation selectivity. We have investigated the sequence of events and possible mechanisms underlying the development of these clustered intrinsic horizontal connections using a combination of neuronal tracers and intracellular staining. Small injections of fluorescent latex microspheres made during the first postnatal week (at P4-6), when examined in tangential sections, produced an even, unclustered distribution of retrogradely labeled cells up to 2 mm from the injection site. At P8, retrograde labeling extended over a larger area and clustering was discernible, primarily among the most distant labeled cells. At both P6 and P8, labeling was similar in layers 2/3 and 5, indicating that the transition from clustered to unclustered connections occurred simultaneously for cells in superficial and deep laminae. By the end of the second postnatal week (P12-15), retrogradely labeled cells were far more clustered both within and beyond the extent of P6 label; the density of labeled cells was high throughout the labeled region, but much higher within clusters. The periodicity of these nascent clusters was similar to that in the adult. Despite obvious clustering, the pattern of retrograde label observed following injections at 2-3 weeks (P12-21) differed markedly from the adult, in that the regions between clusters contained many labeled cells. Over the next 3 weeks, the connections were refined, so that by the sixth postnatal week (P36-38), regions between clusters contained very few retrogradely labeled cells and the overall pattern of retrograde label was indistinguishable from that in adults. Despite differences in postmigratory ages of neurons from the superficial and deep laminae, clustering of retrogradely labeled cells from these 2 populations was similar at all ages. Experiments in which 2-3 weeks elapsed between the time microsphere injections were made and animals were killed demonstrated that neither the initial formation of crude clusters nor their refinement was due to cell death. Instead, cluster refinement resulted from specific process elimination. When a red microsphere injection at P15 was followed by a green microsphere injection at exactly the same location on P29, the earlier injection resulted in crude clustering, as expected. Virtually all of the cells double-labeled by the later injection were within the densest clusters of label from the early injection.(ABSTRACT TRUNCATED AT 400 WORDS)

Callaway, E.M., Soha, J.M., Van Essen, D.C. Differential loss of neuromuscular connections according to activity level and spinal position of neonatal rabbit soleus motor neurons. (1989) Journal of Neuroscience. 9(5):1806-1824.

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We have tested whether the ability of synapses to compete for occupancy of endplates during neuromuscular synapse elimination is affected by differences in the spinal position or in the activity level of the parent motor neuron. To test the role of spinal position, the relative sizes of motor units for motor neurons from middle and extreme (rostral/caudal) positions in the rabbit soleus motor pool were determined at 3 postnatal ages: 4-5 d ("early" ages, when the soleus is heavily polyinnervated), 8-9 d ("intermediate"), and 11-15 d ("late," when the soleus has just reached singly innervated state). Average motor unit sizes from extreme ventral roots were similar to those from middle ventral roots in early-aged soleus muscles but were significantly smaller (by 18-27%) for both intermediate and late muscles. Thus, motor neurons from extreme positions evidently compete less effectively for retention of synapses than those from middle positions. To test the role of differential activity, inactive and active synapses were pitted directly against one another by implanting Silastic plugs laden with tetrodotoxin (TTX) into one of the spinal nerves containing a minority of the soleus motor axons. Differential activity was maintained during a period of extensive synapse loss, from the time of the implant at day 4 or 5 until the intermediate age (day 8-9). Motor unit twitch tensions were subsequently measured to determine the relative number of synapses retained by individual active and inactive motor neurons. The inactivated motor units were on average significantly larger (by more than 50%) than the corresponding group from normal and control-implanted animals. The abnormally large size of inactivated motor units persisted in animals allowed to recover from the TTX block and examined after multiple innervation had disappeared. Hence, the effect of the TTX block cannot be attributed to a simple slowing of synapse elimination specifically among the inactive motor neurons. We conclude that complete presynaptic inactivity improves the chances of survival relative to that for normal activity during synapse elimination in the neonatal rabbit soleus muscle. This difference in competitive ability may contribute to the development of an important characteristic of adult muscles, the correlation between motor unit size and recruitment threshold.

Callaway, E.M., Van Essen, D.C. Slowing of synapse elimination by alpha-bungarotoxin superfusion of the neonatal rabbit soleus muscle. (1989) Developmental Biology. 131(2):356-365.

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Soha, J.M., Callaway, E.M., Van Essen, D.C. Lack of fiber type selectivity during reinnervation of neonatal rabbit soleus muscle. (1989) Developmental Biology. 131(2):401-414.

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Callaway, E.M., Soha, J.M., Van Essen, D.C. Competition favouring inactive over active motor neurons during synapse elimination. (1987) Nature. 328(6129):422-426. DOI: 10.1038/328422a0

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Edward Callaway, PhD

Salk Institute for Biological Studies - Publications

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