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Published in: Brain Structure and Function 4/2015

01-07-2015 | Original Article

Whole-brain mapping of behaviourally induced neural activation in mice

Authors: Dulcie A. Vousden, Jonathan Epp, Hiroyuki Okuno, Brian J. Nieman, Matthijs van Eede, Jun Dazai, Timothy Ragan, Haruhiko Bito, Paul W. Frankland, Jason P. Lerch, R. Mark Henkelman

Published in: Brain Structure and Function | Issue 4/2015

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Abstract

The ability to visualize behaviourally evoked neural activity patterns across the rodent brain is essential for understanding the distributed brain networks mediating particular behaviours. However, current imaging methods are limited in their spatial resolution and/or ability to obtain brain-wide coverage of functional activity. Here, we describe a new automated method for obtaining cellular-level, whole-brain maps of behaviourally induced neural activity in the mouse. This method combines the use of transgenic immediate-early gene reporter mice to visualize neural activity; serial two-photon tomography to image the entire brain at cellular resolution; advanced image processing algorithms to count the activated neurons and align the datasets to the Allen Mouse Brain Atlas; and statistical analysis to identify the network of activated brain regions evoked by behaviour. We demonstrate the use of this approach to determine the whole-brain networks activated during the retrieval of fear memories. Consistent with previous studies, we identified a large network of amygdalar, hippocampal, and neocortical brain regions implicated in fear memory retrieval. Our proposed methods can thus be used to map cellular networks involved in the expression of normal behaviours as well as to investigate in depth circuit dysfunction in mouse models of neurobiological disease.
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Literature
go back to reference Alivisatos AP, Chun M, Church GM, Greenspan RJ, Roukes ML, Yuste R (2012) The brain activity map project and the challenge of functional connectomics. Neuron 74:970–974PubMedCentralPubMedCrossRef Alivisatos AP, Chun M, Church GM, Greenspan RJ, Roukes ML, Yuste R (2012) The brain activity map project and the challenge of functional connectomics. Neuron 74:970–974PubMedCentralPubMedCrossRef
go back to reference Avants BB, Epstein CL, Grossman M, Gee JC (2008) Symmetric diffeomorphic image registration with cross-correlation: evaluating automated labeling of elderly and neurodegenerative brain. Med Image Anal 12:26–41PubMedCentralPubMedCrossRef Avants BB, Epstein CL, Grossman M, Gee JC (2008) Symmetric diffeomorphic image registration with cross-correlation: evaluating automated labeling of elderly and neurodegenerative brain. Med Image Anal 12:26–41PubMedCentralPubMedCrossRef
go back to reference Bullmore E, Sporns O (2009) Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 10:186–198PubMedCrossRef Bullmore E, Sporns O (2009) Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 10:186–198PubMedCrossRef
go back to reference Campeau S, Davis M (1995) Involvement of subcortical and cortical afferents to the lateral nucleus of the amygdala in fear conditioning measured with fear-potentiated startle in rats trained concurrently with auditory and visual conditioned stimuli. J Neurosci 15:2312–2327PubMed Campeau S, Davis M (1995) Involvement of subcortical and cortical afferents to the lateral nucleus of the amygdala in fear conditioning measured with fear-potentiated startle in rats trained concurrently with auditory and visual conditioned stimuli. J Neurosci 15:2312–2327PubMed
go back to reference Carpenter A, Jones T, Lamprecht M, Clarke C, Kang I, Friman O, Guertin D, Chang J, Lindquist R, Moffat J et al (2006) CellProfiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol 7:R100PubMedCentralPubMedCrossRef Carpenter A, Jones T, Lamprecht M, Clarke C, Kang I, Friman O, Guertin D, Chang J, Lindquist R, Moffat J et al (2006) CellProfiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol 7:R100PubMedCentralPubMedCrossRef
go back to reference Chinwalla AT, Cook LL, Delehaunty KD, Fewell GA, Fulton LA, Fulton RS, Graves TA, Hillier LW, Mardis ER, McPherson JD et al (2002) Initial sequencing and comparative analysis of the mouse genome. Nature 420:520–562PubMedCrossRef Chinwalla AT, Cook LL, Delehaunty KD, Fewell GA, Fulton LA, Fulton RS, Graves TA, Hillier LW, Mardis ER, McPherson JD et al (2002) Initial sequencing and comparative analysis of the mouse genome. Nature 420:520–562PubMedCrossRef
go back to reference Collins DL, Evans C (1997) Animal: validation and applications of nonlinear registration-based segmentation. Int J Pattern Recognit Artif Intell 11:1271–1294CrossRef Collins DL, Evans C (1997) Animal: validation and applications of nonlinear registration-based segmentation. Int J Pattern Recognit Artif Intell 11:1271–1294CrossRef
go back to reference Collins DL, Neelin P, Peters TM, Evans AC (1994) Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space. J Comput Assist Tomogr 18:192–205PubMedCrossRef Collins DL, Neelin P, Peters TM, Evans AC (1994) Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space. J Comput Assist Tomogr 18:192–205PubMedCrossRef
go back to reference Collins DL, Holmes CJ, Peters TM, Evans AC (1995) Automatic 3-D model-based neuroanatomical segmentation. Hum Brain Mapp 3:190–208CrossRef Collins DL, Holmes CJ, Peters TM, Evans AC (1995) Automatic 3-D model-based neuroanatomical segmentation. Hum Brain Mapp 3:190–208CrossRef
go back to reference Corcoran KA, Donnan MD, Tronson NC, Guzmán YF, Gao C, Jovasevic V, Guedea AL, Radulovic J (2011) NMDA receptors in retrosplenial cortex are necessary for retrieval of recent and remote context fear memory. J Neurosci 31:11655–11659PubMedCentralPubMedCrossRef Corcoran KA, Donnan MD, Tronson NC, Guzmán YF, Gao C, Jovasevic V, Guedea AL, Radulovic J (2011) NMDA receptors in retrosplenial cortex are necessary for retrieval of recent and remote context fear memory. J Neurosci 31:11655–11659PubMedCentralPubMedCrossRef
go back to reference Corodimas KP, LeDoux JE (1995) Disruptive effects of posttraining perirhinal cortex lesions on conditioned fear: contributions of contextual cues. Behav Neurosci 109:613–619PubMedCrossRef Corodimas KP, LeDoux JE (1995) Disruptive effects of posttraining perirhinal cortex lesions on conditioned fear: contributions of contextual cues. Behav Neurosci 109:613–619PubMedCrossRef
go back to reference Eguchi M, Yamaguchi S (2009) In vivo and in vitro visualization of gene expression dynamics over extensive areas of the brain. Neuroimage 44:1274–1283PubMedCrossRef Eguchi M, Yamaguchi S (2009) In vivo and in vitro visualization of gene expression dynamics over extensive areas of the brain. Neuroimage 44:1274–1283PubMedCrossRef
go back to reference Ferris CF, Smerkers B, Kulkarni P, Caffrey M, Afacan O, Toddes S, Stolberg T, Febo M (2011) Functional magnetic resonance imaging in awake animals. Rev Neurosci 22:665–674PubMedCrossRef Ferris CF, Smerkers B, Kulkarni P, Caffrey M, Afacan O, Toddes S, Stolberg T, Febo M (2011) Functional magnetic resonance imaging in awake animals. Rev Neurosci 22:665–674PubMedCrossRef
go back to reference Frankland PW, Bontempi B, Talton LE, Kaczmarek L, Silva AJ (2004) The involvement of the anterior cingulate cortex in remote contextual fear memory. Science 304:881–883PubMedCrossRef Frankland PW, Bontempi B, Talton LE, Kaczmarek L, Silva AJ (2004) The involvement of the anterior cingulate cortex in remote contextual fear memory. Science 304:881–883PubMedCrossRef
go back to reference Genovese CR, Lazar NA, Nichols T (2002) Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 15:870–878PubMedCrossRef Genovese CR, Lazar NA, Nichols T (2002) Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 15:870–878PubMedCrossRef
go back to reference Gusev PA, Cui C, Alkon DL, Gubin AN (2005) Topography of Arc/Arg3.1 mRNA expression in the dorsal and ventral hippocampus induced by recent and remote spatial memory recall: dissociation of CA3 and CA1 activation. J Neurosci 25:9384–9397PubMedCrossRef Gusev PA, Cui C, Alkon DL, Gubin AN (2005) Topography of Arc/Arg3.1 mRNA expression in the dorsal and ventral hippocampus induced by recent and remote spatial memory recall: dissociation of CA3 and CA1 activation. J Neurosci 25:9384–9397PubMedCrossRef
go back to reference Guzowski JF, Timlin JA, Roysam B, McNaughton BL, Worley PF, Barnes CA (2005) Mapping behaviorally relevant neural circuits with immediate-early gene expression. Curr Opin Neurobiol 15:599–606PubMedCrossRef Guzowski JF, Timlin JA, Roysam B, McNaughton BL, Worley PF, Barnes CA (2005) Mapping behaviorally relevant neural circuits with immediate-early gene expression. Curr Opin Neurobiol 15:599–606PubMedCrossRef
go back to reference Henkelman RM (2010) Systems biology through mouse imaging centers: experience and new directions. Annu Rev Biomed Eng 12:143–166PubMedCrossRef Henkelman RM (2010) Systems biology through mouse imaging centers: experience and new directions. Annu Rev Biomed Eng 12:143–166PubMedCrossRef
go back to reference Huff NC, Frank M, Wright-Hardesty K, Sprunger D, Matus-Amat P, Higgins E, Rudy JW (2006) Amygdala regulation of immediate-early gene expression in the hippocampus induced by contextual fear conditioning. J Neurosci 26:1616–1623PubMedCrossRef Huff NC, Frank M, Wright-Hardesty K, Sprunger D, Matus-Amat P, Higgins E, Rudy JW (2006) Amygdala regulation of immediate-early gene expression in the hippocampus induced by contextual fear conditioning. J Neurosci 26:1616–1623PubMedCrossRef
go back to reference Ji J, Maren S (2008) Lesions of the entorhinal cortex or fornix disrupt the context-dependence of fear extinction in rats. Behav Brain Res 194:201–206PubMedCentralPubMedCrossRef Ji J, Maren S (2008) Lesions of the entorhinal cortex or fornix disrupt the context-dependence of fear extinction in rats. Behav Brain Res 194:201–206PubMedCentralPubMedCrossRef
go back to reference Josselyn SA, Shi C, Carlezon WA Jr, Neve RL, Nestler EJ, Davis M (2001) Long-term memory is facilitated by cAMP response element-binding protein overexpression in the amygdala. J Neurosci 21:2404–2412PubMed Josselyn SA, Shi C, Carlezon WA Jr, Neve RL, Nestler EJ, Davis M (2001) Long-term memory is facilitated by cAMP response element-binding protein overexpression in the amygdala. J Neurosci 21:2404–2412PubMed
go back to reference Kawashima T, Okuno H, Nonaka M, Adachi-Morishima A, Kyo N, Okamura M, Takemoto-Kimura S, Worley PF, Bito H (2009) Synaptic activity-responsive element in the Arc/Arg3.1 promoter essential for synapse-to-nucleus signaling in activated neurons. Proc Natl Acad Sci USA 106:316–321PubMedCentralPubMedCrossRef Kawashima T, Okuno H, Nonaka M, Adachi-Morishima A, Kyo N, Okamura M, Takemoto-Kimura S, Worley PF, Bito H (2009) Synaptic activity-responsive element in the Arc/Arg3.1 promoter essential for synapse-to-nucleus signaling in activated neurons. Proc Natl Acad Sci USA 106:316–321PubMedCentralPubMedCrossRef
go back to reference Kawashima T, Kitamura K, Suzuki K, Nonaka M, Kamijo S, Takemoto-Kimura S, Kano M, Okuno H, Ohki K, Bito H (2013) Functional labeling of neurons and their projections using the synthetic activity–dependent promoter E-SARE. Nature Methods 10:889–895PubMedCrossRef Kawashima T, Kitamura K, Suzuki K, Nonaka M, Kamijo S, Takemoto-Kimura S, Kano M, Okuno H, Ohki K, Bito H (2013) Functional labeling of neurons and their projections using the synthetic activity–dependent promoter E-SARE. Nature Methods 10:889–895PubMedCrossRef
go back to reference Kerr JND, Denk W (2008) Imaging in vivo: watching the brain in action. Nat Rev Neurosci 9:195–205PubMedCrossRef Kerr JND, Denk W (2008) Imaging in vivo: watching the brain in action. Nat Rev Neurosci 9:195–205PubMedCrossRef
go back to reference Kovacevic N, Henderson JT, Lifshitz N, Bishop J, Evans AC, Henkelman RM, Chen XJ (2005) A three-dimensional MRI atlas of the mouse brain with estimates of the average and variability. Cereb Cortex 15:639–645PubMedCrossRef Kovacevic N, Henderson JT, Lifshitz N, Bishop J, Evans AC, Henkelman RM, Chen XJ (2005) A three-dimensional MRI atlas of the mouse brain with estimates of the average and variability. Cereb Cortex 15:639–645PubMedCrossRef
go back to reference Lee I, Kesner RP (2004) Differential contributions of dorsal hippocampal subregions to memory acquisition and retrieval in contextual fear-conditioning. Hippocampus 14:301–310PubMedCrossRef Lee I, Kesner RP (2004) Differential contributions of dorsal hippocampal subregions to memory acquisition and retrieval in contextual fear-conditioning. Hippocampus 14:301–310PubMedCrossRef
go back to reference Lein ES, Hawrylycz MJ, Ao N, Ayres M, Bensinger A, Bernard A, Boe AF, Boguski MS, Brockway KS, Byrnes EJ et al (2007) Genome-wide atlas of gene expression in the adult mouse brain. Nature 445:168–176 and Website: 2012. Allen Institute for Brain Science. Allen Mouse Brain Atlas (Internet). Available from http://mouse.brain-map.org/ Lein ES, Hawrylycz MJ, Ao N, Ayres M, Bensinger A, Bernard A, Boe AF, Boguski MS, Brockway KS, Byrnes EJ et al (2007) Genome-wide atlas of gene expression in the adult mouse brain. Nature 445:168–176 and Website: 2012. Allen Institute for Brain Science. Allen Mouse Brain Atlas (Internet). Available from http://​mouse.​brain-map.​org/​
go back to reference Lerch JP, Carrol JB, Spring S, Bertram LN, Schwab C, Hayden MR, Henkelman RM (2008) Automated deformation analysis in the YAC128 Huntington disease mouse model. NeuroImage 39:32–39PubMedCrossRef Lerch JP, Carrol JB, Spring S, Bertram LN, Schwab C, Hayden MR, Henkelman RM (2008) Automated deformation analysis in the YAC128 Huntington disease mouse model. NeuroImage 39:32–39PubMedCrossRef
go back to reference Lerch JP, Sled JG, Henkelman RM (2011) MRI phenotyping of genetically altered mice. Methods Mol Biol 711:349–361PubMedCrossRef Lerch JP, Sled JG, Henkelman RM (2011) MRI phenotyping of genetically altered mice. Methods Mol Biol 711:349–361PubMedCrossRef
go back to reference Li X, Zhao X, Fang Y, Jiang X, Duong T, Fan C, Huang CC, Kain SR (1998) Generation of destabilized green fluorescent protein as a transcription reporter. J Biol Chem 273:34970–34975PubMedCrossRef Li X, Zhao X, Fang Y, Jiang X, Duong T, Fan C, Huang CC, Kain SR (1998) Generation of destabilized green fluorescent protein as a transcription reporter. J Biol Chem 273:34970–34975PubMedCrossRef
go back to reference Mamiya N, Fukushima H, Suzuki A, Matsuyama Z, Homma S, Frankland PW, Kida S (2009) Brain region-specific gene expression activation required for reconsolidation and extinction of contextual fear memory. J Neurosci 29:402–413PubMedCrossRef Mamiya N, Fukushima H, Suzuki A, Matsuyama Z, Homma S, Frankland PW, Kida S (2009) Brain region-specific gene expression activation required for reconsolidation and extinction of contextual fear memory. J Neurosci 29:402–413PubMedCrossRef
go back to reference Mikuni T, Uesaka N, Okuno H, Hirai H, Deisseroth K, Bito H, Kano M (2013) Arc/Arg3.1 is a postsynaptic mediator of activity-dependent synapse elimination in the developing cerebellum. Neuron 78:1024–1035PubMedCentralPubMedCrossRef Mikuni T, Uesaka N, Okuno H, Hirai H, Deisseroth K, Bito H, Kano M (2013) Arc/Arg3.1 is a postsynaptic mediator of activity-dependent synapse elimination in the developing cerebellum. Neuron 78:1024–1035PubMedCentralPubMedCrossRef
go back to reference Nagai T, Ibata K, Park ES, Kubota M, Mikoshiba K, Miyawaki A (2002) A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat Biotechnol 20:87–90PubMedCrossRef Nagai T, Ibata K, Park ES, Kubota M, Mikoshiba K, Miyawaki A (2002) A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat Biotechnol 20:87–90PubMedCrossRef
go back to reference Okuno H (2011) Regulation and function of immediate-early genes in the brain: beyond neuronal activity markers. Neurosci Res 69:175–186PubMedCrossRef Okuno H (2011) Regulation and function of immediate-early genes in the brain: beyond neuronal activity markers. Neurosci Res 69:175–186PubMedCrossRef
go back to reference Okuno H, Akashi K, Ishii Y, Yagishita-Kyo N, Suzuki K, Nonaka M, Kawashima T, Fujii H, Takemoto-Kimura S, Abe M et al (2012) Inverse synaptic tagging of inactive synapses via dynamic interaction of Arc/Arg3.1 with CaMKIIβ. Cell 149:886–898PubMedCrossRef Okuno H, Akashi K, Ishii Y, Yagishita-Kyo N, Suzuki K, Nonaka M, Kawashima T, Fujii H, Takemoto-Kimura S, Abe M et al (2012) Inverse synaptic tagging of inactive synapses via dynamic interaction of Arc/Arg3.1 with CaMKIIβ. Cell 149:886–898PubMedCrossRef
go back to reference Peters LL, Robledo RF, Bult CJ, Churchill GA, Paigen BJ, Svenson KL (2007) The mouse as a model for human biology: a resource guide for complex trait analysis. Nat Rev Genet 8:58–69PubMedCrossRef Peters LL, Robledo RF, Bult CJ, Churchill GA, Paigen BJ, Svenson KL (2007) The mouse as a model for human biology: a resource guide for complex trait analysis. Nat Rev Genet 8:58–69PubMedCrossRef
go back to reference Ploski JE, Pierre VJ, Smucny J, Park K, Monsey MS, Overeem KA, Schafe GE (2008) The activity-regulated cytoskeletal-associated protein (Arc/Arg3.1) is required for memory consolidation of pavlovian fear conditioning in the lateral amygdala. J Neurosci 28:12383–12395PubMedCrossRef Ploski JE, Pierre VJ, Smucny J, Park K, Monsey MS, Overeem KA, Schafe GE (2008) The activity-regulated cytoskeletal-associated protein (Arc/Arg3.1) is required for memory consolidation of pavlovian fear conditioning in the lateral amygdala. J Neurosci 28:12383–12395PubMedCrossRef
go back to reference Ragan T, Kadiri LR, Venkataraju KU, Bahlmann K, Sutin J, Taranda J, Arganda-Carreras I, Kim Y, Seung HS, Osten P (2012) Serial two-photon tomography for automated ex vivo mouse brain imaging. Nat Methods 9:255–258PubMedCentralPubMedCrossRef Ragan T, Kadiri LR, Venkataraju KU, Bahlmann K, Sutin J, Taranda J, Arganda-Carreras I, Kim Y, Seung HS, Osten P (2012) Serial two-photon tomography for automated ex vivo mouse brain imaging. Nat Methods 9:255–258PubMedCentralPubMedCrossRef
go back to reference Reijmers LG, Perkins BL, Matsuo N, Mayford M (2007) Localization of a stable neural correlate of associative memory. Science 317:1230–1233PubMedCrossRef Reijmers LG, Perkins BL, Matsuo N, Mayford M (2007) Localization of a stable neural correlate of associative memory. Science 317:1230–1233PubMedCrossRef
go back to reference Rudinskiy N, Hawkes JM, Betensky RA, Eguchi M, Yamaguchi S, Spires-Jones TL, Hyman BT (2012) Orchestrated experience-driven Arc responses are disrupted in a mouse model of Alzheimer’s disease. Nat Neurosci 15:1422–1429PubMedCentralPubMedCrossRef Rudinskiy N, Hawkes JM, Betensky RA, Eguchi M, Yamaguchi S, Spires-Jones TL, Hyman BT (2012) Orchestrated experience-driven Arc responses are disrupted in a mouse model of Alzheimer’s disease. Nat Neurosci 15:1422–1429PubMedCentralPubMedCrossRef
go back to reference Shepherd JD, Bear MF (2011) New views of Arc, a master regulator of synaptic plasticity. Nat Neurosci 14:279–284PubMedCrossRef Shepherd JD, Bear MF (2011) New views of Arc, a master regulator of synaptic plasticity. Nat Neurosci 14:279–284PubMedCrossRef
go back to reference Tayler KK, Tanaka KZ, Reijmers LG, Wiltgen BJ (2013) Reactivation of neural ensembles during the retrieval of recent and remote memory. Curr Biol 23:99–106PubMedCrossRef Tayler KK, Tanaka KZ, Reijmers LG, Wiltgen BJ (2013) Reactivation of neural ensembles during the retrieval of recent and remote memory. Curr Biol 23:99–106PubMedCrossRef
go back to reference Tzingounis AV, Nicoll RA (2006) Arc/Arg3.1: linking gene expression to synaptic plasticity and memory. Neuron 52:403–407PubMedCrossRef Tzingounis AV, Nicoll RA (2006) Arc/Arg3.1: linking gene expression to synaptic plasticity and memory. Neuron 52:403–407PubMedCrossRef
go back to reference Wei F, Qiu C-S, Liauw J, Robinson DA, Ho N, Chatila T, Zhuo M (2002) Calcium–calmodulin-dependent protein kinase IV is required for fear memory. Nat Neurosci 5:573–579PubMedCrossRef Wei F, Qiu C-S, Liauw J, Robinson DA, Ho N, Chatila T, Zhuo M (2002) Calcium–calmodulin-dependent protein kinase IV is required for fear memory. Nat Neurosci 5:573–579PubMedCrossRef
go back to reference Wheeler AL, Teixeira CM, Wang AH, Xiong X, Kovacevic N, Lerch JP, McIntosh AR, Parkinson J, Frankland PW (2013) Identification of a functional connectome for long-term fear memory in mice. PLoS Comput Biol 9:e1002853PubMedCentralPubMedCrossRef Wheeler AL, Teixeira CM, Wang AH, Xiong X, Kovacevic N, Lerch JP, McIntosh AR, Parkinson J, Frankland PW (2013) Identification of a functional connectome for long-term fear memory in mice. PLoS Comput Biol 9:e1002853PubMedCentralPubMedCrossRef
go back to reference Yamasaki Y, Hashikawa K, Matsuki N, Nomura H (2012) Off-line Arc transcription in active ensembles during fear memory retrieval. Eur J Neurosci Yamasaki Y, Hashikawa K, Matsuki N, Nomura H (2012) Off-line Arc transcription in active ensembles during fear memory retrieval. Eur J Neurosci
go back to reference Zhu XO, Brown MW, McCabe BJ, Aggleton JP (1995) Effects of the novelty or familiarity of visual stimuli on the expression of the immediate early gene c-fos in rat brain. Neuroscience 69:821–829PubMedCrossRef Zhu XO, Brown MW, McCabe BJ, Aggleton JP (1995) Effects of the novelty or familiarity of visual stimuli on the expression of the immediate early gene c-fos in rat brain. Neuroscience 69:821–829PubMedCrossRef
Metadata
Title
Whole-brain mapping of behaviourally induced neural activation in mice
Authors
Dulcie A. Vousden
Jonathan Epp
Hiroyuki Okuno
Brian J. Nieman
Matthijs van Eede
Jun Dazai
Timothy Ragan
Haruhiko Bito
Paul W. Frankland
Jason P. Lerch
R. Mark Henkelman
Publication date
01-07-2015
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 4/2015
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-014-0774-0

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