Experience-Dependent, Layer-Specific Development of Divergent Thalamocortical Connectivity

Cerebral Cortex

Volumn 25, Issue 8, 2015, Pages 2255-2266

  Crocker Buque, Alex ^a   Brown, Sarah M ^a   Kind, Peter C ^a   Isaac, John T R ^b,c   Daw, Michael I ^a  

^a Centre for Integrative Physiology   (United Kingdom)

^b NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^c ELI LILLY AND COMPANY   (United States)

Author keywords

barrel cortex; LTP; plasticity; somatosensory

Indexed keywords

ANIMAL CELL; ARTICLE; CONNECTOME; EXCITATORY POSTSYNAPTIC POTENTIAL; EXPERIENCE; LONG TERM POTENTIATION; MOUSE; NERVE CELL PLASTICITY; NERVE FIBER; NEWBORN; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; SENSORY CORTEX; SOMATOSENSORY CORTEX; THALAMOCORTICAL TRACT; ANIMAL; AXON; CYTOLOGY; DRUG EFFECTS; ELECTROSTIMULATION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NERVE TRACT; NEUROANATOMICAL TRACT TRACING; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; SYNAPSE; THALAMUS; TISSUE CULTURE TECHNIQUE; TOUCH; VIBRISSA;

HTR1B PROTEIN, MOUSE; SEROTONIN 1B RECEPTOR;

ANIMALS; AXONS; ELECTRIC STIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; LONG-TERM POTENTIATION; MICE; NEURAL PATHWAYS; NEUROANATOMICAL TRACT-TRACING TECHNIQUES; PATCH-CLAMP TECHNIQUES; RECEPTOR, SEROTONIN, 5-HT1B; SOMATOSENSORY CORTEX; SYNAPSES; THALAMUS; TISSUE CULTURE TECHNIQUES; TOUCH PERCEPTION; VIBRISSAE;

EID: 84938630573     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhu031     Document Type: Article

References (47)

1. Adams P, Cox K. 2002. A new interpretation of thalamocortical circuitry. Philos Trans R Soc Lond B Biol Sci. 357:1767-1779.
2. Agmon A, Connors BW. 1991. Thalamocortical responses of mouse somatosensory (barrel) cortex in vitro. Neuroscience. 41:365-379.
3. Agmon A, Yang LT, O'Dowd DK, Jones EG. 1993. Organized growth of thalamocortical axons from the deep tier of terminations into layer IV of developing mouse barrel cortex. J Neurosci. 13:5365-5382.
4. An S, Yang JW, Sun H, Kilb W, Luhmann HJ. 2012. Long-term potentiation in the neonatal rat barrel cortex in vivo. J Neurosci. 32:9511-9516.
5. Bannister NJ, Benke TA, Mellor J, Scott H, Gurdal E, Crabtree JW, Isaac JT. 2005. Developmental changes in AMPA and kainate receptormediated quantal transmission at thalamocortical synapses in the barrel cortex. J Neurosci. 25:5259-5271.
6. Beierlein M, Connors BW. 2002. Short-term dynamics of thalamocortical and intracortical synapses onto layer 6 neurons in neocortex. J Neurophysiol. 88:1924-1932.
7. Bonnin A, Peng W, Hewlett W, Levitt P. 2006. Expression mapping of 5-HT1 serotonin receptor subtypes during fetal and early postnatal mouse forebrain development. Neuroscience. 141:781-794.
8. Brecht M. 2007. Barrel cortex and whisker-mediated behaviors. Curr Opin Neurobiol. 17:408-416.
9. Bruno RM, Sakmann B. 2006. Cortex is driven by weak but synchronously active thalamocortical synapses. Science. 312:1622-1627.
10. Bruno RM, Simons DJ. 2002. Feedforward mechanisms of excitatory and inhibitory cortical receptive fields. J Neurosci. 22:10966-10975.
11. Bureau I, von Saint Paul F, Svoboda K. 2006. Interdigitated paralemniscal and lemniscal pathways in the mouse barrel cortex. PLoS Biol. 4:e382.
12. Callaway EM, Borrell V. 2011. Developmental sculpting of dendritic morphology of layer 4 neurons in visual cortex: influence of retinal input. J Neurosci. 31:7456-7470.
13. Castro-Alamancos MA. 2004. Dynamics of sensory thalamocortical synaptic networks during information processing states. Prog Neurobiol. 74:213-247.
14. Catalano SM, Robertson RT, Killackey HP. 1996. Individual axon morphology and thalamocortical topography in developing rat somatosensory cortex. J Comp Neurol. 367:36-53.
15. Constantinople CM, Bruno RM. 2013. Deep cortical layers are activated directly by thalamus. Science. 340:1591-1594.
16. Crair MC, Malenka RC. 1995. A critical period for long-term potentiation at thalamocortical synapses. Nature. 375:325-328.
17. Daw MI, Ashby MC, Isaac JT. 2007. Coordinated developmental recruitment of latent fast spiking interneurons in layer IV barrel cortex. Nat Neurosci. 10:453-461.
18. Daw MI, Bannister NV, Isaac JT. 2006. Rapid, activity-dependent plasticity in timing precision in neonatal barrel cortex. J Neurosci. 26:4178-4187.
19. Daw MI, Scott HL, Isaac JT. 2007. Developmental synaptic plasticity at the thalamocortical input to barrel cortex: mechanisms and roles. Mol Cell Neurosci. 34:493-502.
20. De la Rossa A, Bellone C, Golding B, Vitali I, Moss J, Toni N, Luscher C, Jabaudon D. 2013. In vivo reprogramming of circuit connectivity in postmitotic neocortical neurons. Nat Neurosci. 16:193-200.
21. Erzurumlu RS, Jhaveri S. 1992. Trigeminal ganglion cell processes are spatially ordered prior to the differentiation of the vibrissa pad. J Neurosci. 12:3946-3955.
22. Evrard A, Ropert N. 2009. Early development of the thalamic inhibitory feedback loop in the primary somatosensory system of the newborn mice. J Neurosci. 29:9930-9940.
23. Fox K. 1992. A critical period for experience-dependent synaptic plasticity in rat barrel cortex. J Neurosci. 12:1826-1838.
24. Gabernet L, Jadhav SP, Feldman DE, Carandini M, Scanziani M. 2005. Somatosensory integration controlled by dynamic thalamocortical feed-forward inhibition. Neuron. 48:315-327.
25. Gil Z, Connors BW, Amitai Y. 1999. Efficacy of thalamocortical and intracortical synaptic connections: quanta, innervation, and reliability. Neuron. 23:385-397.
26. Hedrick T, Waters J. 2013. Effect of temperature on spiking patterns of neocortical layer 2/3 and layer 6 pyramidal neurons. Front Neural Circuits. 6:28.
27. Inan M, Lu H-C, Albright MJ, She W-C, Crair MC. 2006. Barrel map development relies on protein kinase a regulatory subunit II betamediated cAMP signaling. J Neurosci. 26:4338-4349.
28. Isaac JT, Crair MC, Nicoll RA, Malenka RC. 1997. Silent synapses during development of thalamocortical inputs. Neuron. 18:269-280.
29. Isaac JT, Hjelmstad GO, Nicoll RA, Malenka RC. 1996. Long-term potentiation at single fiber inputs to hippocampal CA1 pyramidal cells. Proc Natl Acad Sci USA. 93:8710-8715.
30. Jensen KF, Killackey HP. 1987. Terminal arbors of axons projecting to the somatosensory cortex of the adult rat. I. The normal morphology of specific thalamocortical afferents. J Neurosci. 7:3529-3543.
31. Kidd FL, Coumis U, Collingridge GL, Crabtree JW, Isaac JT. 2002. A presynaptic kainate receptor is involved in regulating the dynamic properties of thalamocortical synapses during development. Neuron. 34:635-646.
32. Kidd FL, Isaac JT. 1999. Developmental and activity-dependent regulation of kainate receptors at thalamocortical synapses. Nature. 400:569-573.
33. Lamsa K, Heeroma JH, Kullmann DM. 2005. Hebbian LTP in feedforward inhibitory interneurons and the temporal fidelity of input discrimination. Nat Neurosci. 8:916-924.
34. Laurent A, Goaillard JM, Cases O, Lebrand C, Gaspar P, Ropert N. 2002. Activity-dependent presynaptic effect of serotonin 1B receptors on the somatosensory thalamocortical transmission in neonatal mice. J Neurosci. 22:886-900.
35. Lee LJ, Iwasato T, Itohara S, Erzurumlu RS. 2005. Exuberant thalamocortical axon arborization in cortex-specific NMDAR1 knockout mice. J Comp Neurol. 485:280-292.
36. Liao CC, Lee LJ. 2014. Presynaptic 5-HT1B receptor-mediated synaptic suppression to the subplate neurons in the somatosensory cortex of neonatal rats. Neuropharmacology. 77:81-89.
37. Longair MH, Baker DA, Armstrong JD. 2011. Simple Neurite Tracer: open source software for reconstruction, visualization and analysis of neuronal processes. Bioinformatics. 27:2453-2454.
38. Minlebaev M, Colonnese M, Tsintsadze T, Sirota A, Khazipov R. 2011. Early gamma oscillations synchronize developing thalamus and cortex. Science. 334:226-229.
39. Oberlaender M, Ramirez A, Bruno Randyâ M. 2012. Sensory experience restructures thalamocortical axons during adulthood. Neuron. 74:648-655.
40. Olsen SR, Bortone DS, Adesnik H, Scanziani M. 2012. Gain control by layer six in cortical circuits of vision. Nature. 483:47-52.
41. Salami M, Itami C, Tsumoto T, Kimura F. 2003. Change of conduction velocity by regional myelination yields constant latency irrespective of distance between thalamus and cortex. Proc Natl Acad Sci USA. 100:6174-6179.
42. She WC, Quairiaux C, Albright MJ, Wang YC, Sanchez DE, Chang PS, Welker E, Lu HC. 2009. Roles of mGluR5 in synaptic function and plasticity of the mouse thalamocortical pathway. Eur J Neurosci. 29:1379-1396.
43. Thomson AM. 2010. Neocortical layer 6, a review. Front Neuroanat. 4:1-14.
44. Tropea D, Majewska AK, Garcia R, Sur M. 2010. Structural dynamics of synapses in vivo correlate with functional changes during experiencedependent plasticity in visual cortex. J Neurosci. 30:11086-11095.
45. Wang L, Kloc M, Gu Y, Ge S, Maffei A. 2013. Layer-specific experiencedependent rewiring of thalamocortical circuits. J Neurosci. 33:4181-4191.
46. Wimmer VC, Broser PJ, Kuner T, Bruno RM. 2010. Experience-induced plasticity of thalamocortical axons in both juveniles and adults. J Comp Neurol. 518:4629-4648.
47. Yu X, Chung S, Chen DY, Wang S, Dodd SJ,Walters JR, Isaac JT, Koretsky AP. 2012. Thalamocortical inputs show post-critical-period plasticity. Neuron. 74:731-742.