Differential Receptive Field Properties of Parvalbumin and Somatostatin Inhibitory Neurons in Mouse Auditory Cortex

Cerebral Cortex

Volumn 25, Issue 7, 2015, Pages 1782-1791

  Li, Ling Yun ^a   Xiong, Xiaorui R ^a   Ibrahim, Leena A ^a   Yuan, Wei ^a,b   Tao, Huizhong W ^a   Zhang, Li I ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b THIRD MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

auditory cortex; in vivo patch recording; inhibitory subtype; interneuron; two photon imaging; whole cell recording

Indexed keywords

PARVALBUMIN; SOMATOSTATIN;

ANIMAL CELL; ARTICLE; AUDITORY CORTEX; FREQUENCY; IN VIVO STUDY; LATENT PERIOD; MOUSE; NERVE CELL; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTIVE FIELD; SPIKE; SYNAPSE; ACTION POTENTIAL; ANIMAL; AUDITORY EVOKED POTENTIAL; C57BL MOUSE; CYTOLOGY; FEMALE; FLUORESCENCE IMAGING; HEARING; METABOLISM; NERVE CELL INHIBITION; PATCH CLAMP TECHNIQUE; PHYSIOLOGY;

ACTION POTENTIALS; ANIMALS; AUDITORY CORTEX; AUDITORY PERCEPTION; EVOKED POTENTIALS, AUDITORY; FEMALE; MICE, INBRED C57BL; NEURAL INHIBITION; NEURONS; OPTICAL IMAGING; PARVALBUMINS; PATCH-CLAMP TECHNIQUES; SOMATOSTATIN; SYNAPSES;

EID: 84936767554     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bht417     Document Type: Article

References (52)

1. Adesnik H, Bruns W, Taniguchi H, Huang ZJ, Scanziani M. 2012. A neural circuit for spatial summation in visual cortex. Nature. 490:226-231.
2. Andermann ML, Ritt J, Neimark MA, Moore CI. 2004. Neural correlates of vibrissa resonance; band-pass and somatotopic representation of high frequency stimuli. Neuron. 42:451-463.
3. Atallah BV, Bruns W, Carandini M, Scanziani M. 2012. Parvalbuminexpressing interneurons linearly transform cortical responses to visual stimuli. Neuron. 73:159-170.
4. Atencio CA, Schreiner CE. 2008. Spectrotemporal processing differences between auditory cortical fast-spiking and regular-spiking neurons. J Neurosci. 28:3897-3910.
5. Bandyopadhyay S, Shamma SA, Kanold PO. 2010. Dichotomy of functional organization in the mouse auditory cortex. Nat Neurosci. 13:361-368.
6. Barbour DL, Callaway EM. 2008. Excitatory local connections of superficial neurons in rat auditory cortex. J Neurosci. 28:11174-11185.
7. Barthó P, Hirase H, Monconduit L, Zugaro M, Harris KD, Buzsáki G. 2004. Characterization of neocortical principal cells and interneurons by network interactions and extracellular features. J Neurophysiol. 92:600-608.
8. Bruno RM, Simons DJ. 2002. Feedforward mechanisms of excitatory and inhibitory cortical receptive fields. J Neurosci. 22:10966-10975.
9. Callaway EM. 1998. Local circuits in primary visual cortex of the macaque monkey. Annu Rev Neurosci. 21:47-74.
10. Di Cristo G, Wu C, Chattopadhyaya B, Ango F, Knott G, Welker E, Svoboda K, Huang ZJ. 2004. Subcellular domain-restricted GABAergic innervations in primary visual cortex in the absence of sensory and thalamic inputs. Nat Neurosci. 7:1184-1186.
11. Douglas RJ, Martin KA. 2004. Neuronal circuits of the neocortex. Annu Rev Neurosci. 27:419-451.
12. Gentet LJ, Kremer Y, Taniguchi H, Huang ZJ, Staiger JF, Petersen CC. 2012. Unique functional properties of somatostatin-expressing GABAergic neurons in mouse barrel cortex. Nat Neurosci. 15:607-612.
13. Gray CM, McCormick DA. 1996. Chattering cells: superficial pyramidal neurons contributing to the generation of synchronous oscillations in the visual cortex. Science. 274:109-113.
14. Hofer SB, Ko H, Pichler B, Vogelstein J, Ros H, Zeng H, Lein E, Lesica NA, Mrsic-Flogel TD. 2011. Differential connectivity and response dynamics of excitatory and inhibitory neurons in visual cortex. Nat Neurosci. 14:1045-1052.
15. Kawaguchi Y, Kubota Y. 1997. GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb Cortex. 7:476-486.
16. Kerlin AM, Andermann ML, Berezovskii VK, Reid RC. 2010. Broadly tuned response properties of diverse inhibitory neuron subtypes in mouse visual cortex. Neuron. 67:858-871.
17. Kitamura K, Judkewitz B, Kano M, Denk W, Häusser M. 2008. Targeted patch-clamp recordings and single-cell electroporation of unlabeled neurons in vivo. Nat Methods. 5:61-67.
18. Lee SH, Kwan AC, Zhang S, Phoumthipphavong V, Flannery JG, Masmanidis SC, Taniguchi H, Huang ZJ, Zhang F, Boyden ES et al. 2012. Activation of specific interneurons improves V1 feature selectivity and visual perception. Nature. 488:379-383.
19. Levy RB, Reyes AD. 2012. Spatial profile of excitatory and inhibitory synaptic connectivity in mouse primary auditory cortex. J Neurosci. 32:5609-5619.
20. Li LY, Li YT, Zhou M, Tao HW, Zhang LI. 2013. Intracortical multiplication of thalamocortical signals in mouse auditory cortex. Nat Neurosci. 16:1179-1181.
21. Li YT, Ma WP, Li LY, Ibrahim LA, Wang SZ, Tao HW. 2012. Broadening of inhibitory tuning underlies contrast-dependent sharpening of orientation selectivity in mouse visual cortex. J Neurosci. 32:16466-16477.
22. Liu BH, Li P, Li YT, Sun YJ, Yanagawa Y, Obata K, Zhang LI, Tao HW. 2009. Visual receptive field structure of cortical inhibitory neurons revealed by two-photon imaging guided recording. J Neurosci. 29:10520-10532.
23. Ma WP, Liu BH, Li YT, Huang ZJ, Zhang LI, Tao HW. 2010. Visual representations by cortical somatostatin inhibitory neurons-selective but with weak and delayed responses. J Neurosci. 30:14371-14379.
24. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C. 2004. Interneurons of the neocortical inhibitory system. Nat Rev Neurosci. 5:793-807.
25. Moore AK, Wehr M. 2013. Parvalbumin-expressing inhibitory interneurons in auditory cortex are well-tuned for frequency. J Neurosci. 33:13713-13723.
26. Petreanu L, Mao T, Sternson SM, Svoboda K. 2009. The subcellular organization of neocortical excitatory connections. Nature. 457:1142-1145.
27. Pfeffer CK, Xue M, He M, Huang ZJ, Scanziani M. 2013. Inhibition of inhibition in visual cortex: the logic of connections between molecularly distinct interneurons. Nat Neurosci. 16:1068-1076.
28. Polley DB, Heiser MA, Blake DT, Schreiner CE, Merzenich MM. 2004. Associative learning shapes the neural code for stimulus magnitude in primary auditory cortex. Proc Natl Acad Sci USA. 101:16351-16356.
29. Razak KA, Fuzessery ZM. 2010. GABA shapes a systematic map of binaural sensitivity in the auditory cortex. J Neurophysiol. 104:517-528.
30. Rothschild G, Nelken I, Mizrahi A. 2010. Functional organization and population dynamics in the mouse primary auditory cortex. Nat Neurosci. 13:353-360.
31. Runyan CA, Schummers J, Van Wart A, Kuhlman SJ, Wilson NR, Huang ZJ, Sur M. 2010. Response features of parvalbumin-expressing interneurons suggest precise roles for subtypes of inhibition in visual cortex. Neuron. 67:847-857.
32. Sadagopan S, Wang X. 2010. Contribution of inhibition to stimulus selectivity in primary auditory cortex of awake primates. J Neurosci. 30:7314-7325.
33. Schumacher JW, Schneider DM, Woolley SM. 2011. Anesthetic state modulates excitability but not spectral tuning or neural discrimination in single auditory midbrain neurons. J Neurophysiol. 106:500-514.
34. Sun YJ, Kim YJ, Ibrahim LA, Tao HW, Zhang LI. 2013. Synaptic mechanisms underlying functional dichotomy between intrinsic-bursting and regular-spiking neurons in auditory cortical layer 5. J Neurosci. 33:5326-5339.
35. Sun YJ, Wu GK, Liu BH, Li P, Zhou M, Xiao Z, Tao HW, Zhang LI. 2010. Fine-tuning of pre-balanced excitation and inhibition during auditory cortical development. Nature. 465:927-931.
36. Sutter ML, Schreiner CE. 1991. Physiology and topography of neurons with multipeaked tuning curves in cat primary auditory cortex. J Neurophysiol. 65:1207-1226.
37. Tan AY, Atencio CA, Polley DB, Merzenich MM, Schreiner CE. 2007. Unbalanced synaptic inhibition can create intensity-tuned auditory cortex neurons. Neuroscience. 146:449-462.
38. Tan AY, Zhang LI, Merzenich MM, Schreiner CE. 2004. Tone-evoked excitatory and inhibitory synaptic conductances of primary auditory cortex neurons. J Neurophysiol. 92:630-643.
39. Tan Z, Hu H, Huang ZJ, Agmon A. 2008. Robust but delayed thalamocortical activation of dendritic-targeting inhibitory interneurons. Proc Natl Acad Sci USA. 105:2187-2192.
40. Taniguchi H, He M, Wu P, Kim S, Paik R, Sugino K, Kvitsiani D, Fu Y, Lu J, Lin Y et al. 2011. A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron. 71: 995-1013.
41. Wehr M, Zador AM. 2003. Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature. 426:442-446.
42. Wilson NR, Runyan CA, Wang FL, Sur M. 2012. Division and subtraction by distinct cortical inhibitory networks in vivo. Nature. 488:343-348.
43. Winkowski DE, Kanold PO. 2013. Laminar transformation of frequency organization in auditory cortex. J Neurosci. 33:1498-1508.
44. Wu GK, Arbuckle R, Liu BH, Tao HW, Zhang LI. 2008. Lateral sharpening of cortical frequency tuning by approximately balanced inhibition. Neuron. 58:132-143.
45. Wu GK, Li P, Tao HW, Zhang LI. 2006. Nonmonotonic synaptic excitation and imbalanced inhibition underlying cortical intensity tuning. Neuron. 52:705-715.
46. Wu GK, Tao HW, Zhang LI. 2011. From elementary synaptic circuits to information processing in primary auditory cortex. Neurosci Biobehav Rev. 35:2094-2104.
47. Xiong XR, Liang F, Li H, Mesik L, Zhang KK, Polley DB, Tao HW, Xiao Z, Zhang LI. 2013. Interaural level difference-dependent gain control and synaptic scaling underlying binaural computation. Neuron. 79:738-753.
48. Xu X, Roby KD, Callaway EM. 2006. Mouse cortical inhibitory neuron type that coexpresses somatostatin and calretinin. J Comp Neurol. 499:144-160.
49. Yoshimura Y, Callaway EM. 2005. Fine-scale specificity of cortical networks depends on inhibitory cell type and connectivity. Nat Neurosci. 8:1552-1559.
50. Yoshimura Y, Dantzker JL, Callaway EM. 2005. Excitatory cortical neurons form fine-scale functional networks. Nature. 433:868-873.
51. Zhang LI, Tan AY, Schreiner CE, Merzenich MM. 2003. Topography and synaptic shaping of direction selectivity in primary auditory cortex. Nature. 424:201-205.
52. Zhou Y, Mesik L, Sun YJ, Liang F, Xiao Z, Tao HW, Zhang LI. 2012. Generation of spike latency tuning by thalamocortical circuits in auditory cortex. J Neurosci. 32:9969-9980.