Spatial organization of excitatory synaptic inputs to layer 4 neurons in mouse primary auditory cortex

Frontiers in Neural Circuits

Volumn 9, Issue APR, 2015, Pages

  Kratz, Megan B ^a,b   Manis, Paul B ^a,b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

Brain slice; Glutamate uncaging; Intracortical circuits; Neocortical circuits; Patch clamp; Spectral integration; Thalamocortical recipient neurons

Indexed keywords

GLUTAMATE RECEPTOR; GLUTAMIC ACID;

ANIMAL TISSUE; ARTICLE; BRAIN MAPPING; CONNECTOME; CORTEX LAYER IV; EVOKED RESPONSE; EXCITATORY POSTSYNAPTIC POTENTIAL; MOUSE; NERVE CELL STIMULATION; NONHUMAN; PHOTOSTIMULATION; PRESYNAPTIC POTENTIAL; PRIMARY AUDITORY CORTEX; PROTEIN BINDING; SPIKE WAVE; ALGORITHM; ANIMAL; AUDITORY CORTEX; AUDITORY NERVOUS SYSTEM; NERVE CELL; PATCH CLAMP TECHNIQUE; PHYSIOLOGY;

ALGORITHMS; ANIMALS; AUDITORY CORTEX; AUDITORY PATHWAYS; BRAIN MAPPING; EXCITATORY POSTSYNAPTIC POTENTIALS; MICE; NEURONS; PATCH-CLAMP TECHNIQUES;

EID: 84930506885     PISSN: 16625110     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncir.2015.00017     Document Type: Article

References (51)

1. Atencio, C. A., Sharpee, T. O., and Schreiner, C. E. (2009). Hierarchical computation in the canonical auditory cortical circuit. Proc. Natl. Acad. Sci. U. S. A. 106, 21894-21899. doi: 10. 1073/pnas. 0908383106.
2. Bandyopadhyay, S., Shamma, S. A., and Kanold, P. O. (2010). Dichotomy of functional organization in the mouse auditory cortex. Nat. Neurosci. 13, 361-368. doi: 10. 1038/nn. 2490.
3. Barbour, D. L., and Callaway, E. M. (2008). Excitatory local connections of superficial neurons in rat auditory cortex. J. Neurosci. 28, 11174-11185. doi: 10. 1523/JNEUROSCI. 2093-08. 2008.
4. Bendels, M. H., Beed, P., Schmitz, D., Johenning, F. W., and Leibold, C. (2010). Detection of input sites in scanning photostimulation data based on spatial correlations. J. Neurosci. Methods 192, 286-295. doi: 10. 1016/j. jneumeth. 2010. 08. 006.
5. Boucsein, C., Nawrot, M., Rotter, S., Aertsen, A., and Heck, D. (2005). Controlling synaptic input patterns in vitro by dynamic photo stimulation. J. Neurophysiol. 94, 2948-2958. doi: 10. 1152/jn. 00245. 2005.
6. Broicher, T., Bidmon, H. J., Kamuf, B., Coulon, P., Gorji, A., Pape, H. C., et al. (2010). Thalamic afferent activation of supragranular layers in auditory cortex in vitro: a voltage sensitive dye study. Neuroscience 165, 371-385. doi: 10. 1016/j. neuroscience. 2009. 10. 025.
7. Callaway, E. M., and Katz, L. C. (1993). Photostimulation using caged glutamate reveals functional circuitry in living brain slices. Proc. Natl. Acad. Sci. U. S. A. 90, 7661-7665. doi: 10. 1073/pnas. 90. 16. 7661.
8. Campagnola, L., Kratz, M. B., and Manis, P. B. (2014). ACQ4: an open-source software platform for data acquisition and analysis in neurophysiology research. Front. Neuroinform. 8: 3. doi: 10. 3389/fninf. 2014. 00003.
9. Campagnola, L., and Manis, P. B. (2014). A map of functional synaptic connectivity in the mouse anteroventral cochlear nucleus. J. Neurosci. 34, 2214-2230. doi: 10. 1523/JNEUROSCI. 4669-13. 2014.
10. Chen, X., Leischner, U., Rochefort, N. L., Nelken, I., and Konnerth, A. (2011). Functional mapping of single spines in cortical neurons in vivo. Nature 475, 501-505. doi: 10. 1038/nature10193.
11. Constantinople, C. M., and Bruno, R. M. (2013). Deep cortical layers are activated directly by thalamus. Science 340, 1591-1594. doi: 10. 1126/science. 1236425.
12. Cruikshank, S. J., Rose, H. J., and Metherate, R. (2002). Auditory thalamocortical synaptic transmission in vitro. J. Neurophysiol. 87, 361-384. doi: 10. 1152/jn. 00549. 2001.
13. Douglas, R. J., and Martin, K. A. (2007a). Mapping the matrix: the ways of neocortex. Neuron 56, 226-238. doi: 10. 1016/j. neuron. 2007. 10. 017.
14. Douglas, R. J., and Martin, K. A. (2007b). Recurrent neuronal circuits in the neocortex. Curr. Biol. 17, R496-R500. doi: 10. 1016/j. cub. 2007. 04. 024.
15. Guo, W., Chambers, A. R., Darrow, K. N., Hancock, K. E., Shinn-Cunningham, B. G., and Polley, D. B. (2012). Robustness of cortical topography across fields, laminae, anesthetic states, and neurophysiological signal types. J. Neurosci. 32, 9159-9172. doi: 10. 1523/JNEUROSCI. 0065-12. 2012.
16. Hackett, T. A., Barkat, T. R., O'brien, B. M., Hensch, T. K., and Polley, D. B. (2011). Linking topography to tonotopy in the mouse auditory thalamocortical circuit. J. Neurosci. 31, 2983-2995. doi: 10. 1523/JNEUROSCI. 5333-10. 2011.
17. Happel, M. F., Jeschke, M., and Ohl, F. W. (2010). Spectral integration in primary auditory cortex attributable to temporally precise convergence of thalamocortical and intracortical input. J. Neurosci. 30, 11114-11127. doi: 10. 1523/JNEUROSCI. 0689-10. 2010.
18. Huggenberger, S., Vater, M., and Deisz, R. A. (2009). Interlaminar differences of intrinsic properties of pyramidal neurons in the auditory cortex of mice. Cereb. Cortex19, 1008-1018. doi: 10. 1093/cercor/bhn143.
19. Jin, X., Prince, D. A., and Huguenard, J. R. (2006). Enhanced excitatory synaptic connectivity in layer v pyramidal neurons of chronically injured epileptogenic neocortex in rats. J. Neurosci. 26, 4891-4900. doi: 10. 1523/JNEUROSCI. 4361-05. 2006.
20. Kadia, S. C., and Wang, X. (2003). Spectral integration in A1 of awake primates: neurons with single-and multipeaked tuning characteristics. J. Neurophysiol. 89, 1603-1622. doi: 10. 1152/jn. 00271. 2001.
21. Kalatsky, V. A., Polley, D. B., Merzenich, M. M., Schreiner, C. E., and Stryker, M. P. (2005). Fine functional organization of auditory cortex revealed by Fourier optical imaging. Proc. Natl. Acad. Sci. U. S. A. 102, 13325-13330. doi: 10. 1073/pnas. 0505592102.
22. Kanold, P. O., Nelken, I., and Polley, D. B. (2014). Local versus global scales of organization in auditory cortex. Trends Neurosci. 37, 502-510. doi: 10. 1016/j. tins. 2014. 06. 003.
23. Kaur, S., Lazar, R., and Metherate, R. (2004). Intracortical pathways determine breadth of subthreshold frequency receptive fields in primary auditory cortex. J. Neurophysiol. 91, 2551-2567. doi: 10. 1152/jn. 01121. 2003.
24. Kaur, S., Rose, H. J., Lazar, R., Liang, K., and Metherate, R. (2005). Spectral integration in primary auditory cortex: laminar processing of afferent input, in vivoand in vitro. Neuroscience 134, 1033-1045. doi: 10. 1016/j. neuroscience. 2005. 04. 052.
25. Krause, B. M., Raz, A., Uhlrich, D. J., Smith, P. H., and Banks, M. I. (2014). Spiking in auditory cortex following thalamic stimulation is dominated by cortical network activity. Front. Syst. Neurosci. 8: 170. doi: 10. 3389/fnsys. 2014. 00170.
26. Lee, C. C., and Imaizumi, K. (2013). Functional convergence of thalamic and intrinsic projections to cortical layers 4 and 6. Neurophysiology 45, 396-406. doi: 10. 1007/s11062-013-9385-2.
27. Lee, C. C., Lam, Y. W., and Sherman, S. M. (2012). Intracortical convergence of layer 6 neurons. Neuroreport 23, 736-740. doi: 10. 1097/WNR. 0b013e328356c1aa.
28. Lee, C. C., and Sherman, S. M. (2008). Synaptic properties of thalamic and intracortical inputs to layer 4 of the first-and higher-order cortical areas in the auditory and somatosensory systems. J. Neurophysiol. 100, 317-326. doi: 10. 1152/jn. 90391. 2008.
29. Lee, C. C., and Sherman, S. M. (2009). Modulator property of the intrinsic cortical projection from layer 6 to layer 4. Front. Syst. Neurosci. 3: 3. doi: 10. 3389/neuro. 06. 003. 2009.
30. Lee, C. C., and Sherman, S. M. (2011). On the classification of pathways in the auditory midbrain, thalamus, and cortex. Hear. Res. 276, 79-87. doi: 10. 1016/j. heares. 2010. 12. 012.
31. Lien, A. D., and Scanziani, M. (2013). Tuned thalamic excitation is amplified by visual cortical circuits. Nat. Neurosci. 16, 1315-1323. doi: 10. 1038/nn. 3488.
32. Liu, B. H., Wu, G. K., Arbuckle, R., Tao, H. W., and Zhang, L. I. (2007). Defining cortical frequency tuning with recurrent excitatory circuitry. Nat. Neurosci. 10, 1594-1600. doi: 10. 1038/nn2012.
33. Norena, A. J., Gourevitch, B., Pienkowski, M., Shaw, G., and Eggermont, J. J. (2008). Increasing spectrotemporal sound density reveals an octave-based organization in cat primary auditory cortex. J. Neurosci. 28, 8885-8896. doi: 10. 1523/JNEUROSCI. 2693-08. 2008.
34. Ojima, H., Honda, C. N., and Jones, E. G. (1992). Characteristics of intracellularly injected infragranular pyramidal neurons in cat primary auditory cortex. Cereb. Cortex 2, 197-216. doi: 10. 1093/cercor/2. 3. 197.
35. Olsen, S. R., Bortone, D. S., Adesnik, H., and Scanziani, M. (2012). Gain control by layer six in cortical circuits of vision. Nature 483, 47-52. doi: 10. 1038/nature10835.
36. Oviedo, H. V., Bureau, I., Svoboda, K., and Zador, A. M. (2010). The functional asymmetry of auditory cortex is reflected in the organization of local cortical circuits. Nat. Neurosci. 13, 1413-1420. doi: 10. 1038/nn. 2659.
37. Richardson, M. J., and Silberberg, G. (2008). Measurement and analysis of postsynaptic potentials using a novel voltage-deconvolution method. J. Neurophysiol. 99, 1020-1031. doi: 10. 1152/jn. 00942. 2007.
38. Richardson, R. J., Blundon, J. A., Bayazitov, I. T., and Zakharenko, S. S. (2009). Connectivity patterns revealed by mapping of active inputs on dendrites of thalamorecipient neurons in the auditory cortex. J. Neurosci. 29, 6406-6417. doi: 10. 1523/JNEUROSCI. 0258-09. 2009.
39. Rose, H. J., and Metherate, R. (2005). Auditory thalamocortical transmission is reliable and temporally precise. J. Neurophysiol. 94, 2019-2030. doi: 10. 1152/jn. 00860. 2004.
40. Schnepel, P., Kumar, A., Zohar, M., Aertsen, A., and Boucsein, C. (2014). Physiology and impact of horizontal connections in rat Neocortex. Cereb. Cortex. doi: 10. 1093/cercor/bhu265. [Epub ahead of print].
41. Schubert, D., Staiger, J. F., Cho, N., Kotter, R., Zilles, K., and Luhmann, H. J. (2001). Layer-specific intracolumnar and transcolumnar functional connectivity of layer V pyramidal cells in rat barrel cortex. J. Neurosci. 21, 3580-3592.
42. Shepherd, G. M., Pologruto, T. A., and Svoboda, K. (2003). Circuit analysis of experience-dependent plasticity in the developing rat barrel cortex. Neuron 38, 277-289. doi: 10. 1016/S0896-6273(03)00152-1.
43. Smith, P. H., and Populin, L. C. (2001). Fundamental differences between the thalamocortical recipient layers of the cat auditory and visual cortices. J. Comp. Neurol. 436, 508-519. doi: 10. 1002/cne. 1084.
44. Stiebler, I., Neulist, R., Fichtel, I., and Ehret, G. (1997). The auditory cortex of the house mouse: left-right differences, tonotopic organization and quantitative analysis of frequency representation. J. Comp. Physiol. A 181, 559-571. doi: 10. 1007/s003590050140.
45. Sutter, M. L., and Schreiner, C. E. (1991). Physiology and topography of neurons with multipeaked tuning curves in cat primary auditory cortex. J. Neurophysiol. 65, 1207-1226.
46. Velenovsky, D. S., Cetas, J. S., Price, R. O., Sinex, D. G., and McMullen, N. T. (2003). Functional subregions in primary auditory cortex defined by thalamocortical terminal arbors: an electrophysiological and anterograde labeling study. J. Neurosci. 23, 308-316.
47. Wallace, M. N., Kitzes, L. M., and Jones, E. G. (1991). Intrinsic inter-and intralaminar connections and their relationship to the tonotopic map in cat primary auditory cortex. Exp. Brain Res. 86, 527-544. doi: 10. 1007/BF00230526.
48. Wang, X. (2013). The harmonic organization of auditory cortex. Front. Syst. Neurosci. 7: 114. doi: 10. 3389/fnsys. 2013. 00114.
49. Watkins, P. V., Kao, J. P., and Kanold, P. O. (2014). Spatial pattern of intra-laminar connectivity in supragranular mouse auditory cortex. Front. Neural Circuits 8: 15. doi: 10. 3389/fncir. 2014. 00015.
50. Winkowski, D. E., and Kanold, P. O. (2013). Laminar transformation of frequency organization in auditory cortex. J. Neurosci. 33, 1498-1508. doi: 10. 1523/JNEUROSCI. 3101-12. 2013.
51. Zhou, Y., Liu, B. H., Wu, G. K., Kim, Y. J., Xiao, Z., Tao, H. W., et al. (2010). Preceding inhibition silences layer 6 neurons in auditory cortex. Neuron 65, 706-717. doi: 10. 1016/j. neuron. 2010. 02. 021.