Midbrain local circuits shape sound intensity codes

Frontiers in Neural Circuits

Volumn 7, Issue OCT, 2013, Pages

  Grimsley, Calum Alex ^a   Sanchez, Jason Tait ^a,b   Sivaramakrishnan, Shobhana ^a  

^a Northeast Ohio Medical University   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

High divalents; Inferior colliculus; Local circuits; Monosynaptic; Sound intensity

Indexed keywords

DIVALENT CATION;

ANIMAL EXPERIMENT; ARTICLE; AUDITORY STIMULATION; BRAIN STEM; CONTROLLED STUDY; INFERIOR COLLICULUS; MESENCEPHALON; MOUSE; NERVE CELL; NONHUMAN; POSTSYNAPTIC MEMBRANE; SOUND INTENSITY; SPIKE; STEREOTYPY; SYNAPTIC INHIBITION; ANIMAL; AUDITORY NERVOUS SYSTEM; AUDITORY THRESHOLD; HEARING; HIGH DIVALENTS; LOCAL CIRCUITS; MONOSYNAPTIC; NERVE CELL INHIBITION; PHYSIOLOGY;

HIGH DIVALENTS; INFERIOR COLLICULUS; LOCAL CIRCUITS; MONOSYNAPTIC; SOUND INTENSITY;

ACOUSTIC STIMULATION; ANIMALS; AUDITORY PATHWAYS; AUDITORY PERCEPTION; AUDITORY THRESHOLD; INFERIOR COLLICULI; MICE; NEURAL INHIBITION; NEURONS;

EID: 84886853892     PISSN: 16625110     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2013.00174     Document Type: Article

References (76)

1. Abbott, L. F., and Chance, F. S. (2005). Drivers and modulators from push-pull and balanced synaptic input. Prog. Brain Res. 149, 147-155. doi: 10.1016/S0079-6123(05)49011-1
2. Abbott, L. F., Varela, J. A., Sen, K., and Nelson, S. B. (1997). Synaptic depression and cortical gain control. Science 275, 220-224. doi: 10.1126/science.275.5297.221
3. Albright, T. D., and Stoner, G. R. (2002). Contextual influences on visual processing. Annu. Rev. Neurosci. 25, 339-379. doi: 10.1146/annurev.neuro.25.112701.142900
4. Arnal, L. H., and Giraud, A. L. (2012). Cortical oscillations and sensory predictions. Trends Cogn. Sci. 16, 390-398. doi: 10.1016/j.tics.2012.05.003
5. Barbour, D. L. (2011). Intensity-invariant coding in the auditory system. Neurosci. Biobehav. Rev. 35, 2064-2072. doi: 10.1016/j.neubiorev.2011.04.009
6. Barbour, D. L., and Wang, X. (2003a). Auditory cortical responses elicited in awake primates by random spectrum stimuli. J. Neurosci. 23, 7194-7206.
7. Barbour, D. L., and Wang, X. (2003b). Contrast tuning in auditory cortex. Science 299, 1073-1075. doi: 10.1126/science.1080425
8. Bartlett, E. L., and Wang, X. (2005). Long-lasting modulation by stimulus context in primate auditory cortex. J. Neurophysiol. 94, 83-104. doi: 10.1152/jn.01124.2004
9. Billimoria, C. P., Kraus, B. J., Narayan, R., Maddox, R. K., and Sen, K. (2008). Invariance and sensitivity to intensity in neural discrimination of natural sounds. J. Neurosci. 28, 6304-6308. doi: 10.1523/JNEUROSCI.0961-08.2008
10. Bolzon, D. M., Nordstrom, K., and O'Carroll, D. C. (2009). Local and large-range inhibition in feature detection. J. Neurosci. 29, 14143-14150. doi: 10.1523/JNEUROSCI.2857-09.2009
11. Cant, N. B., and Benson, C. G. (2003). Parallel auditory pathways: projection patterns of the different neuronal populations in the dorsal and ventral cochlear nuclei. Brain Res. Bull. 60, 457-474. doi: 10.1016/S0361-9230(03)00050-9
12. Cardin, J. A., Palmer, L. A., and Contreras, D. (2008). Cellular mechanisms underlying stimulus-dependent gain modulation in primary visual cortex neurons in vivo. Neuron 59, 150-160. doi: 10.1016/j.neuron.2008.05.002
13. Carlyon, R. P., and Moore, B. C. (1984). Intensity discrimination: a severe departure from Weber's law. J. Acoust. Soc. Am. 76, 1369-1376. doi: 10.1121/1.391453
14. Chandrasekaran, L., Xiao, Y., and Sivaramakrishnan, S. (2013). Functional architecture of the inferior colliculus revealed with voltage-sensitive dyes. Front. Neural Circuits 7:41. doi: 10.3389/fncir.2013.00041
15. Chase, S. M., and Young, E. D. (2005). Limited segregation of different types of sound localization information among classes of units in the inferior colliculus. J. Neurosci. 25, 7575-7585. doi: 10.1523/JNEUROSCI.0915-05.2005
16. Davis, K. A., Ramachandran, R., and May, B. J. (2003). Auditory processing of spectral cues for sound localization in the inferior colliculus. J. Assoc. Res. Otolaryngol. 4, 148-163. doi: 10.1007/s10162-002-2002-5
17. Dean, I., Harper, N. S., and McAlpine, D. (2005). Neural population coding of sound level adapts to stimulus statistics. Nat. Neurosci. 8, 1684-1689. doi: 10.1038/nn1541
18. Destexhe, A., Rudolph, M., and Pare, D. (2003). The high-conductance state of neocortical neurons in vivo. Nat. Rev. Neurosci. 4, 739-751. doi: 10.1038/nrn1198
19. Egorova, M., Vartanyan, I., and Ehret, G. (2006). Frequency response areas of mouse inferior colliculus neurons: II. Critical bands. Neuroreport 17, 1783-1786. doi: 10.1097/01.wnr.0000239966.29308.fb
20. Escabi, M. A., Miller, L. M., Read, H. L., and Schreiner, C. E. (2003). Naturalistic auditory contrast improves spectrotemporal coding in the cat inferior colliculus. J. Neurosci. 23, 11489-11504.
21. Ferster, D. (1988). Spatially opponent excitation and inhibition in simple cells of the cat visual cortex. J. Neurosci. 8, 1172-1180.
22. Ferster, D., and Miller, K. D. (2000). Neural mechanisms of orientation selectivity in the visual cortex. Annu. Rev. Neurosci. 23, 441-471. doi: 10.1146/annurev.neuro.23.1.441
23. Frankenhaeuser, B., and Hodgkin, A. L. (1957). The action of calcium on the electrical properties of squid axons. J. Physiol. 137, 218-244.
24. Freiwald, W. A., and Tsao, D. Y. (2010). Functional compartmentalization and viewpoint generalization within the macaque face-processing system. Science 330, 845-851. doi: 10.1126/science.1194908
25. Gibson, D. J., Young, E. D., and Costalupes, J. A. (1985). Similarity of dynamic range adjustment in auditory nerve and cochlear nuclei. J. Neurophysiol. 53, 940-958.
26. Hasenstaub, A., Sachdev, R. N., and McCormick, D. A. (2007). State changes rapidly modulate cortical neuronal responsiveness. J. Neurosci. 27, 9607-9622. doi: 10.1523/JNEUROSCI.2184-07.2007
27. Havey, D. C., and Caspary, D. M. (1980). A simple technique for constructing 'piggy-back' multibarrel microelectrodes. Electroencephalogr. Clin. Neurophysiol. 48, 249-251. doi: 10.1016/0013-4694(80)90313-2
28. Hirsch, J. A., and Martinez, L. M. (2006). Circuits that build visual cortical receptive fields. Trends Neurosci. 29, 30-39. doi: 10.1016/j.tins.2005.11.001
29. Joris, P. X., Schreiner, C. E., and Rees, A. (2004). Neural processing of amplitude-modulated sounds. Physiol. Rev. 84, 541-577. doi: 10.1152/physrev.00029.2003
30. Kandler, K., Clause, A., and Noh, J. (2009). Tonotopic reorganization of developing auditory brainstem circuits. Nat. Neurosci. 12, 711-717. doi: 10.1038/nn.2332
31. King, A. J., Dahmen, J. C., Keating, P., Leach, N. D., Nodal, F. R., and Bajo, V. M. (2011). Neural circuits underlying adaptation and learning in the perception of auditory space. Neurosci. Biobehav. Rev. 35, 2129-2139. doi: 10.1016/j.neubiorev.2011.03.008
32. Kvale, M. N., and Schreiner, C. E. (2004). Short-term adaptation of auditory receptive fields to dynamic stimuli. J. Neurophysiol. 91, 604-612. doi: 10.1152/jn.00484.2003
33. Lee, K. J., Queenan, B. N., Rozeboom, A. M., Bellmore, R., Lim, S. T., Vicini, S., et al. (2013). Mossy fiber-CA3 synapses mediate homeostatic plasticity in mature hippocampal neurons. Neuron 77, 99-114. doi: 10.1016/j.neuron.2012.10.033
34. Lesica, N. A., and Grothe, B. (2008). Dynamic spectrotemporal feature selectivity in the auditory midbrain. J. Neurosci. 28, 5412-5421. doi: 10.1523/JNEUROSCI.0073-08.2008
35. 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
36. McAlpine, D., Jiang, D., Shackleton, T. M., and Palmer, A. R. (1998). Convergent input from brainstem coincidence detectors onto delay-sensitive neurons in the inferior colliculus. J. Neurosci. 18, 6026-6039.
37. Moore, D. R., Kotak, V. C., and Sanes, D. H. (1998). Commissural and lemniscal synaptic input to the gerbil inferior colliculus. J. Neurophysiol. 80, 2229-2236.
38. Murayama, M., Perez-Garci, E., Nevian, T., Bock, T., Senn, W., and Larkum, M. E. (2009). Dendritic encoding of sensory stimuli controlled by deep cortical interneurons. Nature 457, 1137-1141. doi: 10.1038/nature07663
39. Murphy, B. K., and Miller, K. D. (2009). Balanced amplification: a new mechanism of selective amplification of neural activity patterns. Neuron 61, 635-648. doi: 10.1016/j.neuron.2009.02.005
40. Nakamoto, K. T., Mellott, J. G., Killius, J., Storey-Workley, M. E., Sowick, C. S., and Schofield, B. R. (2013). Analysis of excitatory synapses in the guinea pig inferior colliculus: a study using electron microscopy and GABA immunocytochemistry. Neuroscience 237, 170-183. doi: 10.1016/j.neuroscience.2013.01.061
41. Nelken, I., Kim, P. J., and Young, E. D. (1997). Linear and nonlinear spectral integration in type IV neurons of the dorsal cochlear nucleus. II. Predicting responses with the use of nonlinear models. J. Neurophysiol. 78, 800-811.
42. Nelson, P. C., Ewert, S. D., Carney, L. H., and Dau, T. (2007). Comparison of level discrimination, increment detection, and comodulation masking release in the audio-and envelope-frequency domains. J. Acoust. Soc. Am. 121, 2168-2181. doi: 10.1121/1.2535868
43. Ohtsuki, G., Piochon, C., Adelman, J. P., and Hansel, C. (2012). SK2 channel modulation contributes to compartment-specific dendritic plasticity in cerebellar Purkinje cells. Neuron 75, 108-120. doi: 10.1016/j.neuron.2012.05.025
44. Oliver, D. L., Beckius, G. E., Bishop, D. C., and Kuwada, S. (1997). Simultaneous anterograde labeling of axonal layers from lateral superior olive and dorsal cochlear nucleus in the inferior colliculus of cat. J. Comp. Neurol. 382, 215-229. doi: 10.1002/(SICI)1096-9861(19970602)382:2<215::AID-CNE6>3.0.CO;2-6
45. Oliver, D. L., Kuwada, S., Yin, T. C., Haberly, L. B., and Henkel, C. K. (1991). Dendritic and axonal morphology of HRP-injected neurons in the inferior colliculus of the cat. J. Comp. Neurol. 303, 75-100. doi: 10.1002/cne.903030108
46. Olsen, S. R., and Wilson, R. I. (2008). Lateral presynaptic inhibition mediates gain control in an olfactory circuit. Nature 452, 956-960. doi: 10.1038/nature06864
47. Orton, L. D., Poon, P. W., and Rees, A. (2012). Deactivation of the inferior colliculus by cooling demonstrates intercollicular modulation of neuronal activity. Front. Neural Circuits 6:100. doi: 10.3389/fncir.2012.00100
48. Phillips, D. P., and Hall, S. E. (1987). Responses of single neurons in cat auditory cortex to time-varying stimuli: linear amplitude modulations. Exp. Brain Res. 67, 479-492. doi: 10.1007/BF00247281
49. Phillips, D. P., Semple, M. N., Calford, M. B., and Kitzes, L. M. (1994). Level-dependent representation of stimulus frequency in cat primary auditory cortex. Exp. Brain Res. 102, 210-226. doi: 10.1007/BF00227510
50. Polley, D. B., Heiser, M. A., Blake, D. T., Schreiner, C. E., and Merzenich, M. M. (2004). Associative learning shapes the neural code for stimulus magnitude in primary auditory cortex. Proc. Natl. Acad. Sci. U.S.A. 101, 16351-16356. doi: 10.1073/pnas.0407586101
51. Pouille, F., Marin-Burgin, A., Adesnik, H., Atallah, B. V., and Scanziani, M. (2009). Input normalization by global feedforward inhibition expands cortical dynamic range. Nat. Neurosci. 12, 1577-1585. doi: 10.1038/nn.2441
52. Rauschecker, J. P., Tian, B., and Hauser, M. (1995). Processing of complex sounds in the macaque nonprimary auditory cortex. Science 268, 111-114. doi: 10.1126/science.7701330
53. Rees, A., and Palmer, A. R. (1988). Rate-intensity functions and their modification by broadband noise for neurons in the guinea pig inferior colliculus. J. Acoust. Soc. Am. 83, 1488-1498. doi: 10.1121/1.395904
54. Riesenhuber, M., and Poggio, T. (1999). Hierarchical models of object recognition in cortex. Nat. Neurosci. 2, 1019-1025. doi: 10.1038/14819
55. Sachs, M. B., and Abbas, P. J. (1974). Rate versus level functions for auditory-nerve fibers in cats: tone-burst stimuli. J. Acoust. Soc. Am. 56, 1835-1847. doi: 10.1121/1.1903521
56. Sachs, M. B., and Young, E. D. (1979). Encoding of steady-state vowels in the auditory nerve: representation in terms of discharge rate. J. Acoust. Soc. Am. 66, 470-479. doi: 10.1121/1.383098
57. Sadagopan, S., and Wang, X. (2008). Level invariant representation of sounds by populations of neurons in primary auditory cortex. J. Neurosci. 28, 3415-3426. doi: 10.1523/JNEUROSCI.2743-07.2008
58. Sherman, S. M., and Guillery, R. W. (1998). On the actions that one nerve cell can have on another: distinguishing "drivers" from "modulators". Proc. Natl. Acad. Sci. U.S.A. 95, 7121-7126. doi: 10.1073/pnas.95.12.7121
59. Silberberg, G., Gupta, A., and Markram, H. (2002). Stereotypy in neocortical microcircuits. Trends Neurosci. 25, 227-230. doi: 10.1016/S0166-2236(02)02151-3
60. Sivaramakrishnan, S., and Oliver, D. L. (2006). Neuronal responses to lemniscal stimulation in laminar brain slices of the inferior colliculus. J. Assoc. Res. Otolaryngol. 7, 1-14. doi: 10.1007/s10162-005-0017-4
61. Sivaramakrishnan, S., Sanchez, J. T., and Grimsley, C. A. (2013). High concentrations of divalent cations isolate monosynaptic inputs from local circuits in the auditory midbrain. Front. Neural Circuits 7:175. doi: 10.3389/fncir. 2013.00175
62. Sivaramakrishnan, S., Sterbing-D'angelo, S. J., Filipovic, B., D'angelo, W. R., Oliver, D. L., and Kuwada, S. (2004). GABA(A) synapses shape neuronal responses to sound intensity in the inferior colliculus. J. Neurosci. 24, 5031-5043. doi: 10.1523/JNEUROSCI.0357-04.2004
63. Spirou, G. A., Davis, K. A., Nelken, I., and Young, E. D. (1999). Spectral integration by type II interneurons in dorsal cochlear nucleus. J. Neurophysiol. 82, 648-663.
64. Steriade, M. (2001). Impact of network activities on neuronal properties in corticothalamic systems. J. Neurophysiol. 86, 1-39.
65. Sumner, C. J., Scholes, C., and Snyder, R. L. (2009). Retuning of inferior colliculus neurons following spiral ganglion lesions: a single-neuron model of converging inputs. J. Assoc. Res. Otolaryngol. 10, 111-130. doi: 10.1007/s10162-008-0139-6
66. Tan, A. Y., Atencio, C. A., Polley, D. B., Merzenich, M. M., and Schreiner, C. E. (2007). Unbalanced synaptic inhibition can create intensity-tuned auditory cortex neurons. Neuroscience 146, 449-462. doi: 10.1016/j.neuroscience.2007.01.019
67. Wallace, M. N., Shackleton, T. M., and Palmer, A. R. (2012). Morphological and physiological characteristics of laminar cells in the central nucleus of the inferior colliculus. Front. Neural Circuits 6:55. doi: 10.3389/fncir.2012.00055
68. Watkins, P. V., and Barbour, D. L. (2008). Specialized neuronal adaptation for preserving input sensitivity. Nat. Neurosci. 11, 1259-1261. doi: 10.1038/nn.2201
69. Wehr, M., and Zador, A. M. (2003). Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426, 442-446. doi: 10.1038/nature02116
70. Winer, J. A. (2005). Decoding the auditory corticofugal systems. Hear. Res. 207, 1-9. doi: 10.1016/j.heares.2005.06.007
71. Wu, G. K., Li, P., Tao, H. W., and Zhang, L. I. (2006). Nonmonotonic synaptic excitation and imbalanced inhibition underlying cortical intensity tuning. Neuron 52, 705-715. doi: 10.1016/j.neuron.2006.10.009
72. Wu, S. H., Ma, C. L., and Kelly, J. B. (2004). Contribution of AMPA, NMDA, and GABA(A) receptors to temporal pattern of postsynaptic responses in the inferior colliculus of the rat. J. Neurosci. 24, 4625-4634. doi: 10.1523/JNEUROSCI.0318-04.2004
73. Young, E. D., and Sachs, M. B. (2008). Auditory nerve inputs to cochlear nucleus neurons studied with cross-correlation. Neuroscience 154, 127-138. doi: 10.1016/j.neuroscience.2008.01.036
74. Young, E. D., and Voigt, H. F. (1982). Response properties of type II and type III units in dorsal cochlear nucleus. Hear. Res. 6, 153-169. doi: 10.1016/0378-5955(82)90051-X
75. Yu, X. M., and Salter, M. W. (1999). Src, a molecular switch governing gain control of synaptic transmission mediated by N-methyl-D-aspartate receptors. Proc. Natl. Acad. Sci. U.S.A. 96, 7697-7704. doi: 10.1073/pnas.96.14.7697
76. Zelano, C., and Gottfried, J. A. (2012). A taste of what to expect: top-down modulation of neural coding in rodent gustatory cortex. Neuron 74, 217-219. doi: 10.1016/j.neuron.2012.04.008