Publications - Salk Institute for Biological Studies

2013 PUBLICATIONS

Alle Veröffentlichungen

Lainscsek, C., Weyhenmeyer, J., Hernandez, M.E., Poizner, H., Sejnowski, T.J. Non-linear dynamical classification of short time series of the rössler system in high noise regimes. (2013) Frontiers in Neurology. 4:182. DOI: 10.3389/fneur.2013.00182

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Time series analysis with delay differential equations (DDEs) reveals non-linear properties of the underlying dynamical system and can serve as a non-linear time-domain classification tool. Here global DDE models were used to analyze short segments of simulated time series from a known dynamical system, the Rössler system, in high noise regimes. In a companion paper, we apply the DDE model developed here to classify short segments of encephalographic (EEG) data recorded from patients with Parkinson's disease and healthy subjects. Nine simulated subjects in each of two distinct classes were generated by varying the bifurcation parameter b and keeping the other two parameters (a and c) of the Rössler system fixed. All choices of b were in the chaotic parameter range. We diluted the simulated data using white noise ranging from 10 to -30 dB signal-to-noise ratios (SNR). Structure selection was supervised by selecting the number of terms, delays, and order of non-linearity of the model DDE model that best linearly separated the two classes of data. The distances d from the linear dividing hyperplane was then used to assess the classification performance by computing the area A' under the ROC curve. The selected model was tested on untrained data using repeated random sub-sampling validation. DDEs were able to accurately distinguish the two dynamical conditions, and moreover, to quantify the changes in the dynamics. There was a significant correlation between the dynamical bifurcation parameter b of the simulated data and the classification parameter d from our analysis. This correlation still held for new simulated subjects with new dynamical parameters selected from each of the two dynamical regimes. Furthermore, the correlation was robust to added noise, being significant even when the noise was greater than the signal. We conclude that DDE models may be used as a generalizable and reliable classification tool for even small segments of noisy data.

Lainscsek, C., Hernandez, M.E., Weyhenmeyer, J., Sejnowski, T.J., Poizner, H. Non-linear dynamical analysis of EEG time series distinguishes patients with Parkinson's disease from healthy individuals. (2013) Frontiers in Neurology. 4:200. DOI: 10.3389/fneur.2013.00200

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The pathophysiology of Parkinson's disease (PD) is known to involve altered patterns of neuronal firing and synchronization in cortical-basal ganglia circuits. One window into the nature of the aberrant temporal dynamics in the cerebral cortex of PD patients can come from analysis of the patients electroencephalography (EEG). Rather than using spectral-based methods, we used data models based on delay differential equations (DDE) as non-linear time-domain classification tools to analyze EEG recordings from PD patients on and off dopaminergic therapy and healthy individuals. Two sets of 50 1-s segments of 64-channel EEG activity were recorded from nine PD patients on and off medication and nine age-matched controls. The 64 EEG channels were grouped into 10 clusters covering frontal, central, parietal, and occipital brain regions for analysis. DDE models were fitted to individual trials, and model coefficients and error were used as features for classification. The best models were selected using repeated random sub-sampling validation and classification performance was measured using the area under the ROC curve A'. In a companion paper, we show that DDEs can uncover hidden dynamical structure from short segments of simulated time series of known dynamical systems in high noise regimes. Using the same method for finding the best models, we found here that even short segments of EEG data in PD patients and controls contained dynamical structure, and moreover, that PD patients exhibited a greater dynamic range than controls. DDE model output on the means from one set of 50 trials provided nearly complete separation of PD patients off medication from controls: across brain regions, the area under the receiver-operating characteristic curves, A', varied from 0.95 to 1.0. For distinguishing PD patients on vs. off medication, classification performance A' ranged from 0.86 to 1.0 across brain regions. Moreover, the generalizability of the model to the second set of 50 trials was excellent, with A' ranging from 0.81 to 0.94 across brain regions for controls vs. PD off medication, and from 0.62 to 0.82 for PD on medication vs. off. Finally, model features significantly predicted individual patients' motor severity, as assessed with standard clinical rating scales.

Pfaff, S., Shaham, S. Development of neurons and glia. (2013) Aktuelle Meinungen in der Neurobiologie. 23(6):901-2.

Grindberg, R.V., Yee-Greenbaum, J.L., McConnell, M.J., Novotny, M., O'Shaughnessy, A.L., Lambert, G.M., Araúzo-Bravo, M.J., Lee, J., Fishman, M., Robbins, G.E., Lin, X., Venepally, P., Badger, J.H., Galbraith, D.W., Gage, F.H., Lasken, R.S. RNA-sequencing from single nuclei. (2013) Verhandlungen der Nationalen Akademie der Wissenschaften der Vereinigten Staaten von Amerika. 110(49):19802-7. DOI: 10.1073/pnas.1319700110

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Borowska, J., Jones, C.T., Zhang, H., Blacklaws, J., Goulding, M., Zhang, Y. Functional subpopulations of V3 interneurons in the mature mouse spinal cord. (2013) Journal of Neuroscience. 33(47):18553-65. DOI: 10.1523/JNEUROSCI.2005-13.2013

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Del Barrio, M.G., Bourane, S., Grossmann, K., Schüle, R., Britsch, S., O'Leary, D.D., Goulding, M. A transcription factor code defines nine sensory interneuron subtypes in the mechanosensory area of the spinal cord. (2013) PLOS One. 8(11):e77928. DOI: 10.1371/journal.pone.0077928

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Reilly, M.T., Faulkner, G.J., Dubnau, J., Ponomarev, I., Gage, F.H. The role of transposable elements in health and diseases of the central nervous system. (2013) Journal of Neuroscience. 33(45):17577-86. DOI: 10.1523/JNEUROSCI.3369-13.2013

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McConnell, M.J., Lindberg, M.R., Brennand, K.J., Piper, J.C., Voet, T., Cowing-Zitron, C., Shumilina, S., Lasken, R.S., Vermeesch, J.R., Hall, I.M., Gage, F.H. Mosaic copy number variation in human neurons. (2013) Wissenschaft. 342(6158):632-7. DOI: 10.1126/science.1243472

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Marchetto, M.C.N., Narvaiza, I., Denli, A.M., Benner, C., Lazzarini, T.A., Nathanson, J.L., Paquola, A.C.M., Desai, K.N., Herai, R.H., Weitzman, M.D., Yeo, G.W., Muotri, A.R., Gage, F.H. Differential L1 regulation in pluripotent stem cells of humans and apes. (2013) Natur. 503(7477):525-529. DOI: 10.1038/nature12686

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Identifying cellular and molecular differences between human and non-human primates (NHPs) is essential to the basic understanding of the evolution and diversity of our own species. Until now, preserved tissues have been the main source for most comparative studies between humans, chimpanzees (Pan troglodytes) and bonobos (Pan paniscus). However, these tissue samples do not fairly represent the distinctive traits of live cell behaviour and are not amenable to genetic manipulation. We propose that induced pluripotent stem (iPS) cells could be a unique biological resource to determine relevant phenotypical differences between human and NHPs, and that those differences could have potential adaptation and speciation value. Here we describe the generation and initial characterization of iPS cells from chimpanzees and bonobos as new tools to explore factors that may have contributed to great ape evolution. Comparative gene expression analysis of human and NHP iPS cells revealed differences in the regulation of long interspersed element-1 (L1, also known as LINE-1) transposons. A force of change in mammalian evolution, L1 elements are retrotransposons that have remained active during primate evolution. Decreased levels of L1-restricting factors APOBEC3B (also known as A3B) and PIWIL2 (ref. 7) in NHP iPS cells correlated with increased L1 mobility and endogenous L1 messenger RNA levels. Moreover, results from the manipulation of A3B and PIWIL2 levels in iPS cells supported a causal inverse relationship between levels of these proteins and L1 retrotransposition. Finally, we found increased copy numbers of species-specific L1 elements in the genome of chimpanzees compared to humans, supporting the idea that increased L1 mobility in NHPs is not limited to iPS cells in culture and may have also occurred in the germ line or embryonic cells developmentally upstream to germline specification during primate evolution. We propose that differences in L1 mobility may have differentially shaped the genomes of humans and NHPs and could have continuing adaptive significance.

Bekinschtein, P., Kent, B.A., Oomen, C.A., Clemenson, G.D., Gage, F.H., Saksida, L.M., Bussey, T.J. BDNF in the dentate gyrus is required for consolidation of "pattern-separated" memories. (2013) Cell Reports. 5(3):759-68. DOI: 10.1016/j.celrep.2013.09.027

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Miller, J.A., Nathanson, J., Franjic, D., Shim, S., Dalley, R.A., Shapouri, S., Smith, K.A., Sunkin, S.M., Bernard, A., Bennett, J.L., Lee, C.K., Hawrylycz, M.J., Jones, A.R., Amaral, D.G., Šestan, N., Gage, F.H., Lein, E.S. Conserved molecular signatures of neurogenesis in the hippocampal subgranular zone of rodents and primates. (2013) Entwicklung. 140(22):4633-44. DOI: 10.1242/dev.097212

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Gage, F.H., Temple, S. Neural stem cells: generating and regenerating the brain. (2013) Neuron. 80(3):588-601. DOI: 10.1016/j.neuron.2013.10.037

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Deshmukh, V.A., Tardif, V., Lyssiotis, C.A., Green, C.C., Kerman, B., Kim, H.J., Padmanabhan, K., Swoboda, J.G., Ahmad, I., Kondo, T., Gage, F.H., Theofilopoulos, A.N., Lawson, B.R., Schultz, P.G., Lairson, L.L. A regenerative approach to the treatment of multiple sclerosis. (2013) Natur. 502(7471):327-332. DOI: 10.1038/nature12647

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Devor, A., Bandettini, P.A., Boas, D.A., Bower, J.M., Buxton, R.B., Cohen, L.B., Dale, A.M., Einevoll, G.T., Fox, P.T., Franceschini, M.A., Friston, K.J., Fujimoto, J.G., Geyer, M.A., Greenberg, J.H., Halgren, E., Hämäläinen, M.S., Helmchen, F., Hyman, B.T., Jasanoff, A., Jernigan, T.L., Judd, L.L., Kim, S.G., Kleinfeld, D., Kopell, N.J., Kutas, M., Kwong, K.K., Larkum, M.E., Lo, E.H., Magistretti, P.J., Mandeville, J.B., Masliah, E., Mitra, P.P., Mobley, W.C., Moskowitz, M.A., Nimmerjahn, A., Reynolds, J.H., Rosen, B.R., Salzberg, B.M., Schaffer, C.B., Silva, G.A., So, P.T., Spitzer, N.C., Tootell, R.B., Van Essen, D.C., Vanduffel, W., Vinogradov, S.A., Wald, L.L., Wang, L.V., Weber, B., Yodh, A.G. Die Herausforderung, die Punkte im B.R.A.I.N. zu verbinden. (2013) Neuron. 80(2):270-4. DOI: 10.1016/j.neuron.2013.09.008

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Cortes, J.M., Desroches, M., Rodrigues, S., Veltz, R., Muñoz, M.A., Sejnowski, T.J. Short-term synaptic plasticity in the deterministic Tsodyks-Markram model leads to unpredictable network dynamics. (2013) Verhandlungen der Nationalen Akademie der Wissenschaften der Vereinigten Staaten von Amerika. 110(41):16610-5. DOI: 10.1073/pnas.1316071110

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Herzog, C.D., Brown, L., Kruegel, B.R., Wilson, A., Tansey, M.G., Gage, F.H., Johnson, E.M., Bartus, R.T. Enhanced neurotrophic distribution, cell signaling and neuroprotection following substantia nigral versus striatal delivery of AAV2-NRTN (CERE-120). (2013) Neurobiol. Dis. 58:38-48. DOI: 10.1016/j.nbd.2013.04.011

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This paper reassesses the currently accepted viewpoint that targeting the terminal fields (i.e. striatum) of degenerating nigrostriatal dopamine neurons with neurotrophic factors in Parkinson's disease (PD) is sufficient for achieving an optimal neurotrophic response. Recent insight indicating that PD is an axonopathy characterized by axonal transport deficits prompted this effort. We tested whether a significantly greater neurotrophic response might be induced in SN neurons when the neurotrophic factor neurturin (NRTN) is also targeted to the substantia nigra (SN), compared to the more conventional, striatum-only target. While recognizing the importance of maintaining the integrity of nigrostriatal fibers and terminals (especially for achieving optimal function), we refocused attention to the fate of SN neurons. Under conditions of axonal degeneration and neuronal transport deficits, this component of the nigrostriatal system is most vulnerable to the lack of neurotrophic exposure following striatal-only delivery. Given the location of repair genes induced by neurotrophic factors, achieving adequate neurotrophic exposure to the SN neurons is essential for an optimal neurotrophic response, while the survival of these neurons is essential to the very survival of the fibers. Two separate studies were performed using the 6-OHDA model of nigrostriatal degeneration, in conjunction with delivery of the viral vector AAV2-NRTN (CERE-120) to continuously express NRTN to either striatum or nigra alone or combined striatal/nigral exposure, including conditions of ongoing axonopathy. These studies provide additional insight for reinterpreting past animal neurotrophic/6-OHDA studies conducted under conditions where axon transport deficiencies were generally not accounted for, which suggested that targeting the striatum was both necessary and sufficient. The current data demonstrate that delivering NRTN directly to the SN produces 1) expanded NRTN distribution within the terminal field and cell bodies of targeted nigrostriatal neurons, 2) enhanced intracellular neurotrophic factor signaling in the nigrostriatal neurons, and 3) produced greater numbers of surviving dopamine neurons against 6-OHDA-induced toxicity, particularly under the conditions of active axonopathy. Thus, these data provide empirical support that targeting the SN with neurotrophic factors (in addition to striatum) may help enhance the neurotrophic response in midbrain neurons, particularly under conditions of active neurodegeneration which occurs in PD patients.

Aljadeff, J., Segev, R., Berry, M.J., Sharpee, T.O. Spike triggered covariance in strongly correlated gaussian stimuli. (2013) PLOS Computational Biology. 9(9):e1003206. DOI: 10.1371/journal.pcbi.1003206

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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. Optogenetik durch Fenster ins Gehirn beim nichtmenschlichen Primaten. (2013) Journal für Neurophysiologie. 110(6):1455-67. DOI: 10.1152/jn.00153.2013

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Die Optogenetik kombiniert Optik und Genetik, um die neuronale Aktivität zelltypspezifisch und zeitlich präzise im Millisekundenbereich zu steuern. Ihre Anwendung in Modellorganismen wie Nagetieren, Drosophila und Caenorhabditis elegans ist inzwischen gut etabliert. Die Anwendung dieser Technologie bei nichtmenschlichen Primaten (NHPs) hat sich jedoch nur langsam entwickelt. Eine der größten Herausforderungen besteht darin, Viren und Licht durch die dicke Hirnhaut von NHPs zu transportieren, die nur mit Geräten von großem Durchmesser durchdrungen werden kann, die das Gehirn beschädigen. Die Undurchsichtigkeit der Dura des NHP verhindert die Sichtbarkeit des darunter liegenden Kortex, was die räumliche Präzision von Virusinjektionen, elektrophysiologischen Aufzeichnungen und Photostimulationen einschränkt. Hier beschreiben wir einen neuen optogenetischen Ansatz, bei dem die native Dura durch eine optisch transparente künstliche Dura ersetzt wird. Diese künstliche Dura kann mit feinen Glasmikropipetten durchdrungen werden und ermöglicht so die gezielte Injektion von Viren in das Hirngewebe bei minimaler Schädigung der Hirnrinde. Die Expression optogenetischer Wirkstoffe kann im Laufe der Zeit visuell verfolgt werden. Besonders wichtig ist, dass dieses optische Fenster eine gezielte, nicht-invasive Photostimulation und gleichzeitige Messungen der neuronalen Aktivität mittels intrinsischer Signalbildgebung und elektrophysiologischer Ableitungen ermöglicht. Wir präsentieren Ergebnisse sowohl von betäubten und paralysierten (optische Bildgebung) als auch von wachen NHPs (Elektrophysiologie). Die Verbesserungen gegenüber den derzeitigen Methoden, die durch die künstliche Dura möglich sind, sollten einen weit verbreiteten Einsatz optogenetischer Instrumente in der NHP-Forschung ermöglichen - ein wichtiger Schritt zur Entwicklung von Therapien für neuropsychiatrische und neurologische Erkrankungen beim Menschen.

Hsu, C.C., White, N.M., Hayashi, M., Lin, E.C., Poon, T., Banerjee, I., Chen, J., Pfaff, S.L., Macagno, E.R., Dorrestein, P.C. Microscopy ambient ionization top-down mass spectrometry reveals developmental patterning. (2013) Verhandlungen der Nationalen Akademie der Wissenschaften der Vereinigten Staaten von Amerika. 110(37):14855-60. DOI: 10.1073/pnas.1310618110

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Timofeev, I., Sejnowski, T.J., Bazhenov, M., Chauvette, S., Grand, L.B. Age dependency of trauma-induced neocortical epileptogenesis. (2013) Frontiers in Cellular Neuroscience. 7:154. DOI: 10.3389/fncel.2013.00154

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Tang, X., Zhou, L., Wagner, A.M., Marchetto, M.C., Muotri, A.R., Gage, F.H., Chen, G. Astroglial cells regulate the developmental timeline of human neurons differentiated from induced pluripotent stem cells. (2013) Stem Cell Research. 11(2):743-57. DOI: 10.1016/j.scr.2013.05.002

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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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Lister, R.*, Mukamel, E.A., Nery, J.R., Urich, M., Puddifoot, C.A., Johnson, N.D., Lucero, J., Huang, Y., Dwork, A.J., Schultz, M.D., Yu, M., Tonti-Filippini, J., Heyn, H., Hu, S., Wu, J.C., Rao, A., Esteller, M., He, C., Haghighi, F.G., Sejnowski, T.J., Behrens, M.M.*, Ecker, J.R.* Global epigenomic reconfiguration during mammalian brain development. (2013) Wissenschaft. 341(6146):1237905. DOI: 10.1126/science.1237905

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Francius, C., Harris, A., Rucchin, V., Hendricks, T.J., Stam, F.J., Barber, M., Kurek, D., Grosveld, F.G., Pierani, A., Goulding, M., Clotman, F. Identification of multiple subsets of ventral interneurons and differential distribution along the rostrocaudal axis of the developing spinal cord. (2013) PLOS One. 8(8):e70325. DOI: 10.1371/journal.pone.0070325

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Sung, T.C., Chen, Z., Thuret, S., Vilar, M., Gage, F.H., Riek, R., Lee, K.F. P45 forms a complex with FADD and promotes neuronal cell survival following spinal cord injury. (2013) PLOS One. 8(7):e69286. DOI: 10.1371/journal.pone.0069286

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Sharpee, T.O. Computational identification of receptive fields. (2013) Jahresrückblick Neurowissenschaften. 36:103-20. DOI: 10.1146/annurev-neuro-062012-170253

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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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Sharpee, T.O., Kouh, M., Reynolds, J.H. Trade-off zwischen Krümmungsabstimmung und Positionsinvarianz im visuellen Areal V4. (2013) Verhandlungen der Nationalen Akademie der Wissenschaften der Vereinigten Staaten von Amerika. 110(28):11618-23. DOI: 10.1073/pnas.1217479110

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Der Mensch kann eine Vielzahl von Objekten trotz ihrer unterschiedlichen Erscheinung schnell erkennen. Die neuronalen Mechanismen, die den sensorischen Neuronen auf hoher Ebene sowohl eine Selektivität für komplexe Stimulusmerkmale als auch eine "Toleranz" oder Invarianz gegenüber identitätserhaltenden Transformationen, wie z. B. der räumlichen Translation, verleihen, sind nach wie vor kaum verstanden. Frühere Studien haben gezeigt, dass sowohl die Toleranz als auch die Selektivität gegenüber Merkmalskombinationen in aufeinanderfolgenden Phasen des ventralen Sehstroms, der die visuelle Erkennung vermittelt, erhöht sind. Innerhalb eines bestimmten Areals, wie z. B. dem visuellen Areal V4 oder dem inferotemporalen Kortex, wurde festgestellt, dass die Toleranz in umgekehrtem Verhältnis zur Spärlichkeit der neuronalen Antworten steht, die wiederum positiv mit der Selektivität von Konjunktionen korreliert ist. Die direkte Beziehung zwischen Toleranz und Konjunktionsselektivität ist jedoch schwer nachzuweisen, da in verschiedenen Studien entweder eine umgekehrte oder keine signifikante Beziehung festgestellt wurde. Um dies zu klären, haben wir die Reaktionen von V4 auf natürliche Szenen gemessen und mit Hilfe neu entwickelter statistischer Verfahren sowohl die relevanten Stimulusmerkmale als auch den Bereich der Translationsinvarianz für jedes Neuron geschätzt. Die Analyse konzentrierte sich auf die Abstimmung auf Krümmung, ein nachvollziehbares Beispiel für Konjunktionsselektivität, und wir fanden heraus, dass Neuronen, die auf stärker gekrümmte Konturen abgestimmt waren, kleinere Bereiche der Positionsinvarianz aufwiesen und spärlichere Reaktionen auf natürliche Reize produzierten. Diese Kompromisse bieten empirische Unterstützung für neuere Theorien darüber, wie das visuelle System 3D-Formen aus Schattierungs- und Texturflüssen schätzt, sowie für die Kachelhypothese des visuellen Raums für verschiedene Krümmungswerte.

Kaardal, J., Fitzgerald, J.D., Berry, M.J., Sharpee, T.O. Identifying functional bases for multidimensional neural computations. (2013) Neural Computation. 25(7):1870-90. DOI: 10.1162/NECO_a_00465

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Current dimensionality-reduction methods can identify relevant subspaces for neural computations but do not favor one basis over the other within the relevant subspace. Finding the appropriate basis can simplify the description of the nonlinear computation with respect to the relevant variables, making it easier to elucidate the underlying neural computation and make hypotheses about the neural circuitry, giving rise to the observed responses. Part of the problem is that although some of the dimensionality reduction methods can identify many of the relevant dimensions, it is usually difficult to map out or interpret the nonlinear transformation with respect to more than a few relevant dimensions simultaneously without some simplifying assumptions. While recent approaches make it possible to create predictive models based on many relevant dimensions simultaneously, there still remains the need to relate such predictive models to the mechanistic descriptions of the operation of underlying neural circuitry. Here we demonstrate that transforming to a basis within the relevant subspace where the neural computation is best described by a given nonlinear function often makes it easier to interpret the computation and describe it with a small number of parameters. We refer to the corresponding basis as the functional basis, and illustrate the utility of such transformation in the context of logical OR and logical AND functions. We show that although dimensionality-reduction methods such as spike-triggered covariance are able to find a relevant subspace, they often produce dimensions that are difficult to interpret and do not correspond to a functional basis. The functional features can be found using a maximum likelihood approach. The results are illustrated using simulated neurons and recordings from retinal ganglion cells. The resulting features are uniquely defined and nonorthogonal, and they make it easier to relate computational and mechanistic models to each other.

Golomb, B.A., Brenner, S., Chalfie, M., Glashow, S.L., Glauber, R.J., Hubel, D.H., Maskin, E.S., Greengard, P., Gross, D.J., Roberts, R., Tonegawa, S., Wilczek, F.A., Brown, E.M., Sejnowski, T.J. Chocolate habits of Nobel prizewinners. (2013) Natur. 499(7459):409. DOI: 10.1038/499409a

Lainscsek, C., Sejnowski, T.J. Electrocardiogram classification using delay differential equations. (2013) Chaos. 23(2):023132. DOI: 10.1063/1.4811544

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Nandy, A.S., Sharpee, T.O., Reynolds, J.H., Mitchell, J.F. Die Feinstruktur der Formabstimmung im Areal V4. (2013) Neuron. 78(6):1102-15. DOI: 10.1016/j.neuron.2013.04.016

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Yu, D.X., Marchetto, M.C., Gage, F.H. Therapeutic translation of iPSCs for treating neurological disease. (2013) Cell Stem Cell. 12(6):678-88. DOI: 10.1016/j.stem.2013.05.018

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Vilchez, D., Boyer, L., Lutz, M., Merkwirth, C., Morantte, I., Tse, C., Spencer, B., Page, L., Masliah, E., Berggren, W.T., Gage, F.H., Dillin, A. FOXO4 is necessary for neural differentiation of human embryonic stem cells. (2013) Alternde Zelle. 12(3):518-22. DOI: 10.1111/acel.12067

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Ji, B., Wang, X., Pinto-Duarte, A., Kim, M., Caldwell, S., Young, J.W., Behrens, M.M., Sejnowski, T.J., Geyer, M.A., Zhou, X. Prolonged Ketamine Effects in Sp4 Hypomorphic Mice: Mimicking Phenotypes of Schizophrenia. (2013) PLOS One. 8(6):e66327. DOI: 10.1371/journal.pone.0066327

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Chukoskie, L., Snider, J., Mozer, M.C., Krauzlis, R.J., Sejnowski, T.J. Learning where to look for a hidden target. (2013) Verhandlungen der Nationalen Akademie der Wissenschaften der Vereinigten Staaten von Amerika. 110 Suppl :10438-10445. DOI: 10.1073/pnas.1301216110

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Egawa, N., Kitaoka, S., Tsukita, K., Naitoh, M., Takahashi, K., Yamamoto, T., Adachi, F., Kondo, T., Okita, K., Asaka, I., Aoi, T., Watanabe, A., Yamada, Y., Morizane, A., Takahashi, J., Ayaki, T., Ito, H., Yoshikawa, K., Yamawaki, S., Suzuki, S., Watanabe, D., Hioki, H., Kaneko, T., Makioka, K., Okamoto, K., Takuma, H., Tamaoka, A., Hasegawa, K., Nonaka, T., Hasegawa, M., Kawata, A., Yoshida, M., Nakahata, T., Takahashi, R., Marchetto, M.C., Gage, F.H., Yamanaka, S., Inoue, H. Response to comment on "Drug screening for ALS using patient-specific induced pluripotent stem cells". (2013) Science Translational Medicine. 5(188):188lr2. DOI: 10.1126/scitranslmed.3005697

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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) Verhandlungen der Nationalen Akademie der Wissenschaften der Vereinigten Staaten von Amerika. 110(22):9106-11. DOI: 10.1073/pnas.1306912110

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Stiefel, K.M., Englitz, B., Sejnowski, T.J. Origin of intrinsic irregular firing in cortical interneurons. (2013) Verhandlungen der Nationalen Akademie der Wissenschaften der Vereinigten Staaten von Amerika. 110(19):7886-7891. DOI: 10.1073/pnas.1305219110

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Gifford, W.D., Pfaff, S.L., Macfarlan, T.S. Transposable elements as genetic regulatory substrates in early development. (2013) Trends in der Zellbiologie. 23(5):218-26. DOI: 10.1016/j.tcb.2013.01.001

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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 für Neurophysiologie. 109(9):2415-2421. DOI: 10.1152/jn.01043.2012

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Gire, D.H., Restrepo, D., Sejnowski, T.J., Greer, C., De Carlos, J.A., Lopez-Mascaraque, L. Temporal processing in the olfactory system: can we see a smell? (2013) Neuron. 78(3):416-432. DOI: 10.1016/j.neuron.2013.04.033

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Rangel, L.M., Quinn, L.K., Chiba, A.A., Gage, F.H., Aimone, J.B. A hypothesis for temporal coding of young and mature granule cells. (2013) Frontiers in Neuroscience. 7:75. DOI: 10.3389/fnins.2013.00075

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Saremi, S., Sejnowski, T.J., Sharpee, T.O. Double-gabor filters are independent components of small translation-invariant image patches. (2013) Neural Computation. 25(4):922-39. DOI: 10.1162/NECO_a_00418

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Wang, X., Pinto-Duarte, A., Sejnowski, T.J., Behrens, M.M. How Nox2-containing NADPH oxidase affects cortical circuits in the NMDA receptor antagonist model of schizophrenia. (2013) Antioxidants & Redox Signaling. 18(12):1444-62. DOI: 10.1089/ars.2012.4907

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Jeanne, J.M., Sharpee, T.O., Gentner, T.Q. Associative learning enhances population coding by inverting interneuronal correlation patterns. (2013) Neuron. 78(2):352-63. DOI: 10.1016/j.neuron.2013.02.023

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Regner, B.M., Vučinić, D., Domnisoru, C., Bartol, T.M., Hetzer, M.W., Tartakovsky, D.M., Sejnowski, T.J. Anomalous diffusion of single particles in cytoplasm. (2013) Biophysical Journal. 104(8):1652-60. DOI: 10.1016/j.bpj.2013.01.049

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Wang, X., Zhao, Y., Zhang, X., Badie, H., Zhou, Y., Mu, Y., Loo, L.S., Cai, L., Thompson, R.C., Yang, B., Chen, Y., Johnson, P.F., Wu, C., Bu, G., Mobley, W.C., Zhang, D., Gage, F.H., Ranscht, B., Zhang, Y.W., Lipton, S.A., Hong, W., Xu, H. Loss of sorting nexin 27 contributes to excitatory synaptic dysfunction by modulating glutamate receptor recycling in Down's syndrome. (2013) Nature Medicine. 19(4):473-80. DOI: 10.1038/nm.3117

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Deng, W., Mayford, M., Gage, F.H. Selection of distinct populations of dentate granule cells in response to inputs as a mechanism for pattern separation in mice. (2013) Elife. 2:e00312. DOI: 10.7554/eLife.00312

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Hinckley, C.A., Pfaff, S.L. Imaging spinal neuron ensembles active during locomotion with genetically encoded calcium indicators. (2013) Ann. N. Y. Acad. Sci. 1279:71-9. DOI: 10.1111/nyas.12092

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Rowe, H.M., Kapopoulou, A., Corsinotti, A., Fasching, L., Macfarlan, T.S., Tarabay, Y., Viville, S., Jakobsson, J., Pfaff, S.L., Trono, D. TRIM28 repression of retrotransposon-based enhancers is necessary to preserve transcriptional dynamics in embryonic stem cells. (2013) Genomforschung. 23(3):452-61. DOI: 10.1101/gr.147678.112

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Alivisatos, A.P., Andrews, A.M., Boyden, E.S., Chun, M., Church, G.M., Deisseroth, K., Donoghue, J.P., Fraser, S.E., Lippincott-Schwartz, J., Looger, L.L., Masmanidis, S., McEuen, P.L., Nurmikko, A.V., Park, H., Peterka, D.S., Reid, C., Roukes, M.L., Scherer, A., Schnitzer, M., Sejnowski, T.J., Shepard, K.L., Tsao, D., Turrigiano, G., Weiss, P.S., Xu, C., Yuste, R., Zhuang, X. Nanotools for neuroscience and brain activity mapping. (2013) ACS Nano. 7(3):1850-66. DOI: 10.1021/nn4012847

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Alivisatos, A.P., Chun, M., Church, G.M., Deisseroth, K., Donoghue, J.P., Greenspan, R.J., McEuen, P.L., Roukes, M.L., Sejnowski, T.J., Weiss, P.S., Yuste, R. Neuroscience. The brain activity map. (2013) Wissenschaft. 339(6125):1284-5. DOI: 10.1126/science.1236939

Liang, Y., Franks, T.M., Marchetto, M.C., Gage, F.H., Hetzer, M.W. Dynamic association of NUP98 with the human genome. (2013) PLOS Genetics. 9(2):e1003308. DOI: 10.1371/journal.pgen.1003308

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Saremi, S., Sejnowski, T.J. Hierarchical model of natural images and the origin of scale invariance. (2013) Verhandlungen der Nationalen Akademie der Wissenschaften der Vereinigten Staaten von Amerika. 110(8):3071-3076. DOI: 10.1073/pnas.1222618110

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Tanaka, H., Sejnowski, T.J. Computing reaching dynamics in motor cortex with Cartesian spatial coordinates. (2013) Journal für Neurophysiologie. 109(4):1182-1201. DOI: 10.1152/jn.00279.2012

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Kinney, J.P., Spacek, J., Bartol, T.M., Bajaj, C.L., Harris, K.M., Sejnowski, T.J. Extracellular sheets and tunnels modulate glutamate diffusion in hippocampal neuropil. (2013) Journal of Vergleichende Neurologie. 521(2):448-464. DOI: 10.1002/cne.23181

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Srinivasan, L., Asaad, W.F., Ginat, D.T., Gale, J.T., Dougherty, D.D., Williams, Z.M., Sejnowski, T.J., Eskandar, E.N. Action initiation in the human dorsal anterior cingulate cortex. (2013) PLOS One. 8(2):e55247. DOI: 10.1371/journal.pone.0055247

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Shimozaki, K., Clemenson, G.D., Gage, F.H. Paired related homeobox protein 1 is a regulator of stemness in adult neural stem/progenitor cells. (2013) Journal of Neuroscience. 33(9):4066-75. DOI: 10.1523/JNEUROSCI.4586-12.2013

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Volman, V., Bazhenov, M., Sejnowski, T.J. Divide and conquer: functional segregation of synaptic inputs by astrocytic microdomains could alleviate paroxysmal activity following brain trauma. (2013) PLOS Computational Biology. 9(1):e1002856. DOI: 10.1371/journal.pcbi.1002856

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Kurian, L., Sancho-Martinez, I., Nivet, E., Aguirre, A., Moon, K., Pendaries, C., Volle-Challier, C., Bono, F., Herbert, J.M., Pulecio, J., Xia, Y., Li, M., Montserrat, N., Ruiz, S., Dubova, I., Rodriguez, C., Denli, A.M., Boscolo, F.S., Thiagarajan, R.D., Gage, F.H., Loring, J.F., Laurent, L.C., Izpisua Belmonte, J.C. Conversion of human fibroblasts to angioblast-like progenitor cells. (2013) Nature Methods. 10(1):77-83. DOI: 10.1038/nmeth.2255

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Salk Institute for Biological Studies - Waitt Advanced Biophotonics Center - Research

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