Publications - Salk Institute for Biological Studies

Todas las publicaciones

Klug, J.R., Yan, X., Hoffman, H., Engelhardt, M.D., Osakada, F., Callaway, E.M., Jin, X. Asymmetric cortical projections to striatal direct and indirect pathways distinctly control actions. (2025) Elife. 12. DOI: 10.7554/eLife.92992

+ expandir resumen

Cassidy, R.M., Macias, A.V., Lagos, W.N., Ugorji, C., Callaway, E.M. Complementary Organization of Mouse Driver and Modulator Cortico-Thalamo-Cortical Circuits. (2025) Journal of Neuroscience. DOI: 10.1523/JNEUROSCI.1167-24.2024

+ expandir resumen

Corticocortical (CC) projections in the visual system facilitate hierarchical processing of sensory information. In addition to direct CC connections, indirect cortico-thalamo-cortical (CTC) pathways through the pulvinar nucleus of the thalamus can relay sensory signals and mediate cortical interactions according to behavioral demands. While the pulvinar connects extensively to the entire visual cortex, it is unknown whether transthalamic pathways link all cortical areas or whether they follow systematic organizational rules. Because mouse pulvinar neurons projecting to different areas are spatially intermingled, their input/output relationships have been difficult to characterize using traditional anatomical methods. To determine the organization of CTC circuits, we mapped the higher visual areas (HVAs) of male and female mice with intrinsic signal imaging and targeted five pulvinar→HVA pathways for projection-specific rabies tracing. We aligned post-mortem cortical tissue to in vivo maps for precise quantification of the areas and cell types projecting to each pulvinar→HVA population. Layer 5 corticothalamic (L5CT) "driver" inputs to the pulvinar originate predominantly from primary visual cortex (V1), consistent with the CC hierarchy. L5CT inputs from lateral HVAs specifically avoid driving reciprocal connections, consistent with the "no-strong-loops" hypothesis. Conversely, layer 6 corticothalamic (L6CT) "modulator" inputs are distributed across areas and are biased toward reciprocal connections. Unlike previous studies in primates, we find that every HVA receives disynaptic input from the superior colliculus. CTC circuits in the pulvinar thus depend on both target HVA and input cell type, such that driving and modulating higher-order pathways follow complementary connection rules similar to those governing first-order CT circuits. Understanding the function of the pulvinar will require knowledge of its anatomical connections. Using state-of-the-art rabies tracing, we establish a map of brain-wide and CTC pulvinar connections. While the primate tectopulvinar pathway selectively targets dorsal visual areas, we find ubiquitous SC input in the mouse. This extrageniculate projection supports unconscious visually-guided behavior, suggesting that all visual cortical areas contribute to such functions in mice. Our results also unify longstanding anatomical hypotheses. Namely, "driver" CTC inputs are feedforward relays and adhere to the "no-strong-loops" hypothesis. "Modulator" L6CT inputs are overrepresented in the target HVA, reflecting the reciprocal connectivity described in previous bulk tracing studies. Together, these findings constitute a comprehensive map to guide future experimental and theoretical studies of pulvinar function.

Patiño, M., Rossa, M.A., Lagos, W.N., Patne, N.S., Callaway, E.M. Transcriptomic cell-type specificity of local cortical circuits. (2024) Neuron. DOI: 10.1016/j.neuron.2024.09.003

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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) Naturaleza. 624(7991):355-365. DOI: 10.1038/s41586-023-06823-w

+ expandir resumen

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) Naturaleza. 624(7991):390-402. DOI: 10.1038/s41586-023-06819-6

+ expandir resumen

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

+ expandir resumen

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) Ciencia. 382(6667):eadf6812. DOI: 10.1126/science.adf6812

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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) Naturaleza. DOI: 10.1038/s41586-022-04806-x

+ expandir resumen

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) Actas de la Academia Nacional de Ciencias de los Estados Unidos de América. 119(22):e2203677119. DOI: 10.1073/pnas.2203677119

+ expandir resumen

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

+ expandir resumen

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) Naturaleza. 598(7879):120-128. DOI: 10.1038/s41586-020-03182-8

+ expandir resumen

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) Naturaleza. 598(7879):167-173. DOI: 10.1038/s41586-021-03223-w

+ expandir resumen

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) Biología Actual. DOI: 10.1016/j.cub.2021.09.025

+ expandir resumen

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

+ expandir resumen

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) Móvil. 182(6):1372-1376. DOI: 10.1016/j.cell.2020.08.010

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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) Actas de la Academia Nacional de Ciencias de los Estados Unidos de América. DOI: 10.1073/pnas.2002080117

+ expandir resumen

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) Actas de la Academia Nacional de Ciencias de los Estados Unidos de América. 116(52):27001–27010. DOI: 10.1073/pnas.1915974116

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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) Ciencia. 364(6447):1275-1279. DOI: 10.1126/science.aaw5868

+ expandir resumen

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) Biología Actual. 29(10):1592-1605. DOI: 10.1016/j.cub.2019.03.065

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

Callaway, E.M., Garg, A.K. Brain technology: Neurons recorded en masse. (2017) Naturaleza. 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

+ expandir resumen

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) Naturaleza. 540(7631):144-149. DOI: 10.1038/nature20565

+ expandir resumen

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

+ expandir resumen

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) Móvil. 167(4):961-972. DOI: 10.1016/j.cell.2016.09.051

+ expandir resumen

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

+ expandir resumen

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) Ciencia. 353(6304):1108. DOI: 10.1126/science.aaf5663

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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) Biología Actual. 25(13):1759-1764. DOI: 10.1016/j.cub.2015.05.028

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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) Naturaleza. 507(7492):358-361. DOI: 10.1038/nature12989

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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) Actas de la Academia Nacional de Ciencias de los Estados Unidos de América. 110(22):9106-11. DOI: 10.1073/pnas.1306912110

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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) Actas de la Academia Nacional de Ciencias de los Estados Unidos de América. 109(11):4290-5. DOI: 10.1073/pnas.1120754109

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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) Naturaleza. 472(7342):191-196. DOI: 10.1038/nature09714

+ expandir resumen

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) Actas de la Academia Nacional de Ciencias de los Estados Unidos de América. 107(50):21848-21853. DOI: 10.1073/pnas.1011756107

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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) Naturaleza. 468(7321):270-276. DOI: 10.1038/nature09553

+ expandir resumen

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

+ expandir resumen

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) Actas de la Academia Nacional de Ciencias de los Estados Unidos de América. 107(38):16703-16708. DOI: 10.1073/pnas.1006233107

+ expandir resumen

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

+ expandir resumen

Hasenstaub, A., Otte, S., Callaway, E., Sejnowski, T.J. Metabolic cost as a unifying principle governing neuronal biophysics. (2010) Actas de la Academia Nacional de Ciencias de los Estados Unidos de América. 107(27):12329-34. DOI: 10.1073/pnas.0914886107

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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) Naturaleza. 440(7081):215-9. DOI: 10.1038/nature04545

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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 Biología. 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

+ expandir resumen

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

+ expandir resumen

Brivanlou, I.H., Dantzker, J.L., Stevens, C.F., Callaway, E.M. Topographic specificity of functional connections from hippocampal CA3 to CA1. (2004) Actas de la Academia Nacional de Ciencias de los Estados Unidos de América. 101(8):2560-2565.

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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

+ expandir resumen

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.

+ expandir resumen

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

+ expandir resumen

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.

+ expandir resumen

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.

+ expandir resumen

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

+ expandir resumen

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.

+ expandir resumen

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) Actas de la Academia Nacional de Ciencias de los Estados Unidos de América. 96(4):1193-1200.

+ expandir resumen

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.

+ expandir resumen

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.

+ expandir resumen

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.

+ expandir resumen

Callaway, E.M. Visual scenes and cortical neurons: what you see is what you get. (1998) Actas de la Academia Nacional de Ciencias de los Estados Unidos de América. 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.

+ expandir resumen

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

+ expandir resumen

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.

+ expandir resumen

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

+ expandir resumen

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.

+ expandir resumen

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

+ expandir resumen

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.

+ expandir resumen

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

+ expandir resumen

Callaway, E.M., Katz, L.C. Photostimulation using caged glutamate reveals functional circuitry in living brain slices. (1993) Actas de la Academia Nacional de Ciencias de los Estados Unidos de América. 90(16):7661-7665.

+ expandir resumen

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.

+ expandir resumen

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.

+ expandir resumen

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.

+ expandir resumen

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.

+ expandir resumen

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.

+ expandir resumen

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

+ expandir resumen

Dr. Edward Callaway

Instituto Salk de Estudios Biológicos - Publicaciones

Todas las publicaciones

Apoya la Investigación Salk

Educación

Afiliaciones

Premios y distinciones

Perfil

Características

Sitio web

Contacto