Interneurons in the mouse visual thalamus maintain a high degree of retinal convergence throughout postnatal development

Neural Development

William Guido¹  Gubbi Govindaiah¹  Thomas E Krahe²  Tania A Seabrook² 

[1] Department of Anatomical Sciences and Neurobiology, University of Louisville, 511 South Floyd Street, Louisville, KY 40202, USA;Department of Anatomy and Neurobiology, Virginia Commonwealth University Medical Center, Richmond, VA 23298, USA

关键词: Retinal convergence;    Retinogeniculate pathway;    Interneuron;    Dorsal lateral geniculate nucleus;   

Others  :  803584
DOI  :  10.1186/1749-8104-8-24

 received in 2013-09-21, accepted in 2013-12-06,  发布年份 2013

【 摘 要 】

Background

The dorsal lateral geniculate nucleus (dLGN) of the mouse thalamus has emerged as a powerful experimental system for understanding the refinement of developing sensory connections. Interestingly, many of the basic tenets for such developmental remodeling (for example, pruning of connections to form precise sensory maps) fail to take into account a fundamental aspect of sensory organization, cell-type specific wiring. To date, studies have focused on thalamocortical relay neurons and little is known about the development of retinal connections onto the other principal cell type of dLGN, intrinsic interneurons. Here, we used a transgenic mouse line in which green fluorescent protein (GFP) is expressed within dLGN interneurons (GAD67-GFP), making it possible to visualize them in acutely prepared thalamic slices in order to examine their morphology and functional patterns of connectivity throughout postnatal life.

Findings

GFP-expressing interneurons were evenly distributed throughout dLGN and had highly complex and widespread dendritic processes that often crossed eye-specific borders. Estimates of retinal convergence derived from excitatory postsynaptic potential (EPSP) amplitude by stimulus intensity plots revealed that unlike relay cells, interneurons recorded throughout the first 5 weeks of life, maintain a large number (approximately eight to ten) of retinal inputs.

Conclusions

The lack of pruning onto interneurons suggests that the activity-dependent refinement of retinal connections in dLGN is cell-type specific. The high degree of retinal convergence onto interneurons may be necessary for these cells to provide both widespread and local forms of inhibition in dLGN.

【 授权许可】

   
2013 Seabrook et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

【 参考文献 】

• [1]Chen C, Regehr WG: Developmental remodeling of the retinogeniculate synapse. Neuron 2000, 28:955-966.
• [2]Jaubert-Miazza L, Green E, Lo FS, Bui K, Mills J, Guido W: Structural and functional composition of the developing retinogeniculate pathway in the mouse. Vis Neurosci 2005, 22:661-676.
• [3]Dilger EK, Shin HS, Guido W: Requirements for synaptically evoked plateau potentials in relay cells of the dorsal lateral geniculate nucleus of the mouse. J Physiol 2011, 589:919-937.
• [4]Guido W: Refinement of the retinogeniculate pathway. J Physiol 2008, 586:4357-4362.
• [5]Sherman SM: Interneurons and triadic circuitry of the thalamus. Trends Neurosci 2004, 27:670-675.
• [6]Wang X, Sommer FT, Hirsch JA: Inhibitory circuits for visual processing in thalamus. Curr Opin Neurobiol 2011, 21:726-733.
• [7]Arcelli P, Frassoni C, Regondi MC, De Biasi S, Spreafico R: GABAergic neurons in mammalian thalamus: A marker of thalamic complexity? Brain Res Bull 1997, 42:27-37.
• [8]Chattopadhyaya B, Di Cristo G, Higashiyama H, Knott GW, Kuhlman SJ, Welker E, Huang XJ: Experience and activity-dependent maturation of perisomatic GABAergic innervation in primary visual cortex during a postnatal critical period. J Neurosci 2004, 24:9598-9611.
• [9]Jurgens CW, Bell KA, McQuiston AR, Guido W: Optogenetic stimulation of the corticothalamic pathway affects relay cells and GABAergic neurons differently in the mouse visual thalamus. PLoS One 2012, 7:e45717.
• [10]Krahe TE, El-Danaf RN, Dilger EK, Henderson SC, Guido W: Morphologically distinct classes of relay cells exhibit regional preferences in the dorsal lateral geniculate nucleus of the mouse. J Neurosci 2011, 31:17437-17448.
• [11]Rafols JA, Valverde F: The structure of the dorsal lateral geniculate nucleus in the mouse. A golgi and electron microscopic study. J Comp Neurol 1973, 150:303-332.
• [12]Parnavelas JG, Mounty EJ, Bradford R, Lieberman AR: The postnatal development of neurons in the dorsal lateral geniculate nucleus of the rat: a Golgi study. J Comp Neurol 1977, 171:481-499.
• [13]Webster MJ, Rowe MH: Morphology of identified relay cells and interneurons in the dorsal lateral geniculate nucleus of the rat. Exp Brain Res 1984, 56:468-474.
• [14]Williams SR, Turner JP, Anderson CM, Crunelli V: Electrophysiological and morphological properties of interneurones in the rat dorsal lateral geniculate nucleus in vitro. J Physiol 1996, 490:129-147.
• [15]Zhu JJ, Uhlrich DJ, Lytton WW: Burst firing in identified rat geniculate interneurons. Neuroscience 1999, 91:1445-1460.
• [16]Zhu JJ, Uhlrich DJ, Lytton WW: Properties of a hyperpolarization-activated cation current in interneurons in the rat lateral geniculate nucleus. Neuroscience 1999, 92:445-457.
• [17]Perreault MC, Qin Y, Heggelund P, Zhu JJ: Postnatal development of GABAergic signalling in the rat lateral geniculate nucleus: presynaptic dendritic mechanisms. J Physiol 2003, 546:137-148.
• [18]Levick WR, Cleland BG, Dubin MW: Lateral geniculate neurons in cat: retinal input and physiology. Invest Ophthalmol 1972, 11:302-311.
• [19]Wróbel A: Inhibitory mechanisms within the receptive fields of the lateral geniculate body of the cat. Acta Neurobiol Exp 1982, 42:93-107.
• [20]Mastronarde DN: Nonlagged relay cells and interneurons in the cat lateral geniculate nucleus: receptive-field properties and retinal inputs. Vis Neurosci 1992, 8:407-441.
• [21]Montero VM: A quantitative study of synaptic contacts on interneurons and relay cells of the cat lateral geniculate nucleus. Exp Brain Res 1991, 86:257-270.
• [22]Van Horn SC, Erisir A, Sherman SM: Relative distribution of synapses in the A-laminae of the lateral geniculate nucleus of the cat. J Comp Neurol 2000, 416:509-520.
• [23]Bickford ME, Slusarczyk A, Dilger EK, Krahe TE, Kucuk C, Guido W: Synaptic development of the mouse dorsal lateral geniculate nucleus. J Comp Neurol 2010, 518:622-635.
• [24]Acuna-Goycolea C, Brenowitz SD, Regehr WG: Active dendritic conductances dynamically regulate GABA release from thalamic interneurons. Neuron 2008, 57:420-431.
• [25]Govindaiah G, Cox CL: Metabotropic glutamate receptors differentially regulate GABAergic inhibition in thalamus. J Neurosci 2006, 26:13443-13453.
• [26]Crandall SR, Cox CL: Local dendrodendritic inhibition regulates fast synaptic transmission in visual thalamus. J Neurosci 2012, 32:2513-2522.
• [27]Torborg CL, Feller MB: Spontaneous patterned retinal activity and the refinement of retinal projections. Prog Neurobiol 2005, 76:213-235.
• [28]Dolmetsch RE, Pajvani U, Fife K, Spotts JM, Greenberg ME: Signaling to the nucleus by an L-type calcium channel-calmodulin complex through the MAP kinase pathway. Science 2001, 294:333-339.
• [29]Pham TA, Rubenstein JL, Silva AJ, Storm DR, Stryker MP: The cre/creb pathway is transiently expressed in thalamic circuit development and contributes to refinement of retinogeniculate axons. Neuron 2001, 31:409-420.