Abstract
Neurons form neural circuits through functional synapses. Inputs and outputs across these circuits contribute to the brain’s intricate mechanisms of information processing and behavioral responses. By combining acousto-optic deflector-based scanning microscopy with optogenetics, whole cell electrophysiological recordings, and transgenic viral delivery, researchers can now investigate and map relevant neural circuits with high spatial and cell type-specific precision. The goal of this review is to provide the reader with guidelines and methods for using a combinatorial approach toward circuit mapping in rodent brain tissue.
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Katz LC, Shatz CJ (1996) Synaptic activity and the construction of cortical circuits. Science 274(5290):1133
Ko H, Hofer SB, Pichler B, Buchanan KA, Sjöström PJ, Mrsic-Flogel TD (2011) Functional specificity of local synaptic connections in neocortical networks. Nature 473(7345):87–91
Lüscher C, Jan LY, Stoffel M, Malenka RC, Nicoll RA (1997) G protein-coupled inwardly rectifying K+ channels (GIRKs) mediate postsynaptic but not presynaptic transmitter actions in hippocampal neurons. Neuron 19(3):687–695
Crabtree GW, Gogos JA (2014) Synaptic plasticity, neural circuits, and the emerging role of altered short-term information processing in schizophrenia. Front Synaptic Neurosci 6:28
Nagayama S, Homma R, Imamura F (2014) Neuronal organization of olfactory bulb circuits. Front Neural Circuits 8:98
Huang L, Garcia I, Jen HI, Arenkiel BR (2013) Reciprocal connectivity between mitral cells and external plexiform layer interneurons in the mouse olfactory bulb. Front Neural Circuits 7:32
Huang L, Ung K, Garcia I, Quast KB, Cordiner K, Saggau P, Arenkiel BR (2016) Task learning promotes plasticity of interneuron connectivity maps in the olfactory bulb. J Neurosci 36(34):8856–8871
Quast KB, Ung K, Froudarakis E, Huang L, Herman I, Addison AP et al (2017) Developmental broadening of inhibitory sensory maps. Nat Neurosci 20(2):189–199
Garcia I, Quast KB, Huang L, Herman AM, Selever J, Deussing JM et al (2014) Local CRH signaling promotes synaptogenesis and circuit integration of adult-born neurons. Dev Cell 30(6):645–659
Arenkiel BR et al (2011) Activity-induced remodeling of olfactory bulb microcircuits revealed by monosynaptic tracing. PLoS One 6(12):e29423
Imai T (2014) Construction of functional neuronal circuitry in the olfactory bulb. In: Seminars in cell & developmental biology, vol 35. Academic Press, London, pp 180–188
Arenkiel BR, Peca J, Davison IG, Feliciano C, Deisseroth K, Augustine GJ et al (2007) In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2. Neuron 54(2):205–218
Mitsui S, Igarashi KM, Mori K, Yoshihara Y (2011) Genetic visualization of the secondary olfactory pathway in Tbx21 transgenic mice. Neural Syst Circuits 1(1):5
Faedo A, Ficara F, Ghiani M, Aiuti A, Rubenstein JL, Bulfone A (2002) Developmental expression of the T-box transcription factor T-bet/Tbx21 during mouse embryogenesis. Mech Dev 116(1):157–160
Kosaka T, Kosaka K (2008) Tyrosine hydroxylase-positive GABAergic juxtaglomerular neurons are the main source of the interglomerular connections in the mouse main olfactory bulb. Neurosci Res 60(3):349–354
Parrish-Aungst S, Shipley MT, Erdelyi F, Szabo G, Puche AC (2007) Quantitative analysis of neuronal diversity in the mouse olfactory bulb. J Comp Neurol 501(6):825–836
Miyamichi K, Shlomai-Fuchs Y, Shu M, Weissbourd BC, Luo L, Mizrahi A (2013) Dissecting local circuits: parvalbumin interneurons underlie broad feedback control of olfactory bulb output. Neuron 80(5):1232–1245
Nagai Y, Sano H, Yokoi M (2005) Transgenic expression of cre recombinase in mitral/tufted cells of the olfactorybulb, genesis,43.1
Wang H, Peca J, Matsuzaki M, Matsuzaki K, Noguchi J, Qiu L et al (2007) High-speed mapping of synaptic connectivity using photostimulation in Channelrhodopsin-2 transgenic mice. Proc Natl Acad Sci 104(19):8143–8148
Alvarez-Buylla A, Garcıa-Verdugo JM (2002) Neurogenesis in adult subventricular zone. J Neurosci 22(3):629–634
Herman AM, Ortiz-Guzman J, Kochukov M, Herman I, Quast KB, Patel JM et al (2016) A cholinergic basal forebrain feeding circuit modulates appetite suppression. Nature 538(7624):253–256
Atasoy D, Aponte Y, Su HH, Sternson SM (2008) A FLEX switch targets Channelrhodopsin-2 to multiple cell types for imaging and long-range circuit mapping. J Neurosci 28(28):7025–7030
Perez-Costas E, Melendez-Ferro M, Roberts RC (2007) Microscopy techniques and the study of synapses. Modern Res Educat Topics Microsc 1:164–170
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(5):599–606
Sheng M, Greenberg ME (1990) The regulation and function of c-fos and other immediate early genes in the nervous system. Neuron 4(4):477–485
Nagel G, Szellas T, Huhn W, Kateriya S, Adeishvili N, Berthold P et al (2003) Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc Natl Acad Sci 100(24):13940–13945
Baker CA, Elyada YM, Parra A, Bolton MM (2016) Cellular resolution circuit mapping with temporal-focused excitation of soma-targeted channelrhodopsin. elife 5:e14193
Kravitz AV, Kreitzer AC (2011) Optogenetic manipulation of neural circuitry in vivo. Curr Opin Neurobiol 21(3):433–439
Wang K, Liu Y, Li Y, Guo Y, Song P, Zhang X et al (2011) Precise spatiotemporal control of optogenetic activation using an acousto-optic device. PLoS One 6(12):e28468
Holehonnur R, Luong JA, Chaturvedi D, Ho A, Lella SK, Hosek MP, Ploski JE (2014) Adeno-associated viral serotypes produce differing titers and differentially transduce neurons within the rat basal and lateral amygdala. BMC Neurosci 15(1):28
Osten P, Grinevich V, Cetin A (2007) Viral vectors: a wide range of choices and high levels of service. In: Conditional mutagenesis: an approach to disease models. Springer, Berlin, Heidelberg, pp 177–202
Soudais C, Laplace-Builhe C, Kissa K, Kremer EJ (2001) Preferential transduction of neurons by canine adenovirus vectors and their efficient retrograde transport in vivo. FASEB J 15(12):2283–2285
Bru T, Salinas S, Kremer EJ (2010) An update on canine adenovirus type 2 and its vectors. Virus 2(9):2134–2153
Arenkiel BR, Ehlers MD (2009) Molecular genetics and imaging technologies for circuit-based neuroanatomy. Nature 461(7266):900–907
Denk W, Delaney KR, Gelperin A, Kleinfeld D, Strowbridge BW, Tank DW, Yuste R (1994) Anatomical and functional imaging of neurons using 2-photon laser scanning microscopy. J Neurosci Methods 54(2):151–162
Matsuzaki M, Ellis-Davies GC, Kasai H (2008) Three-dimensional mapping of unitary synaptic connections by two-photon macro photolysis of caged glutamate. J Neurophysiol 99(3):1535–1544
Cardin JA, Carlén M, Meletis K, Knoblich U, Zhang F, Deisseroth K et al (2010) Targeted optogenetic stimulation and recording of neurons in vivo using cell-type-specific expression of Channelrhodopsin-2. Nat Protoc 5(2):247–254
Saraiva LR, Ibarra-Soria X, Khan M, Omura M, Scialdone A, Mombaerts P et al (2015) Hierarchical deconstruction of mouse olfactory sensory neurons: from whole mucosa to single-cell RNA-seq. Sci Rep 5:18178
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This research was supported by funding from the McNair Medical Institute and NINDS grant R01NS078294.
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Liu, G. et al. (2018). A Combinatorial Approach to Circuit Mapping in the Mouse Olfactory Bulb. In: Sillitoe, R. (eds) Extracellular Recording Approaches. Neuromethods, vol 134. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-7549-5_7
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DOI: https://doi.org/10.1007/978-1-4939-7549-5_7
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