Neuroanatomical identification of crossmodal auditory inputs to interneurons in somatosensory cortex

Experimental Brain Research

Volumn 202, Issue 3, 2010, Pages 725-731

  Keniston, Leslie P ^a   Henderson, Scott C ^a   Meredith, M Alex ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

Auditory; Confocal microscopy; Multisensory; Synapse; Tactile

Indexed keywords

VESICULAR GLUTAMATE TRANSPORTER 1;

ANIMAL CELL; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; AUDITORY CORTEX; BRAIN REGION; CELL CONTACT; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FUNCTIONAL ANATOMY; IMMUNOCHEMISTRY; INTERNEURON; NERVE FIBER; NERVE PROJECTION; NEUROANATOMY; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SOMATOSENSORY CORTEX; SYNAPTIC POTENTIAL;

ANIMALS; AUDITORY CORTEX; AUDITORY PERCEPTION; AXONS; CATS; IMAGE CYTOMETRY; INTERNEURONS; MICROSCOPY, CONFOCAL; NEURAL PATHWAYS; NEUROANATOMICAL TRACT-TRACING TECHNIQUES; SOMATOSENSORY CORTEX; SYNAPSES; SYNAPTIC TRANSMISSION; TOUCH PERCEPTION;

EID: 77951094210     PISSN: 00144819     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00221-010-2163-0     Document Type: Article

References (48)

1. B Allman MA Meredith 2007 Multisensory processing in 'unimodal' neurons: cross-modal subthreshold auditory effects in cat extrastriate visual cortex J Neuorphysiol 98 545 549 10.1152/jn.00173.2007 (Pubitemid 47084844)
2. BL Allman RE Bittencourt-Navarrete LP Keniston A Medina MY Wang MA Meredith 2008 Do cross-modal projections always result in multisensory integration? Cereb Cortex 18 2066 2076 10.1093/cercor/bhm230 18203695
3. BL Allman LP Keniston MA Meredith 2009 Not just for bimodal neurons anymore: the contribution of unimodal neurons to cortical multisensory processing Brain Topogr 21 157 167 10.1007/s10548-009-0088-3 19326204
4. Y Amitai JR Gibson M Beierlein SL Patrick AM Ho BW Connors D Golomb 2002 The spatial dimensions of electrically coupled networks of interneurons in the neocortex J Neurosci 22 4142 4152 1:CAS:528:DC%2BD38XjvVans7s%3D 12019332
5. G Benedek L Fischer-Szatmari G Kovacs J Perenyi YY Katoh 1996 Visual, somatosensory and auditory modality properties along the feline suprageniculate-anterior ectosylvian sulcus/insular pathway Prog Brain Res 112 325 334 10.1016/S0079-6123(08)63339-7 1:STN:280:DyaK2s7jsVCltg%3D%3D 8979839
6. EM Bowman CR Olson 1988 Visual and auditory association areas of the cat's posterior ectosylvian gyrus: cortical afferents J Comp Neurol 272 30 42 10.1002/cne.902720104 1:STN:280:DyaL1c3lslKhsA%3D%3D 2454976
7. BN Carriere DW Royal TJ Perrault SP Morrison JW Vaughan BE Stein MT Wallace 2007 Visual deprivation alters the development of cortical multisensory integration J Neurophysiol 98 2858 2867 10.1152/jn.00587.2007 17728386 (Pubitemid 350127944)
8. SA Chowdhury DD Rasmusson 2002 Comparison of receptive field expansion produced by GABA(B) and GABA(A) receptor antagonists in raccoon primary somatosensory cortex Exp Brain Res 144 114 121 10.1007/s00221-002-1035-7 1:CAS:528:DC%2BD38XjtFymtL4%3D 11976765 (Pubitemid 34439310)
9. JC Clarey DR Irvine 1986 Auditory response properties of neurons in the anterior ectosylvian sulcus of the cat Brain Res 386 12 19 10.1016/0006-8993(86) 90136-8 1:STN:280:DyaL2s%2FltVOksw%3D%3D 3779403 (Pubitemid 17181455)
10. HR Clemo BE Stein 1983 Organization of a fourth somatosensory area of cortex in cat J Neurophysiol 50 910 925 1:STN:280:DyaL2c%2FjsFansg%3D%3D 6631469
11. HR Clemo L Keniston MA Meredith 2003 A comparison of the distribution of GABA-ergic neurons in cortices representing different sensory modalities J Chem Neuroanat 26 51 63 10.1016/S0891-0618(03)00039-5 1:CAS:528:DC%2BD3sXmvVyhsLo%3D 12954530 (Pubitemid 37083552)
12. HR Clemo BL Allman MA Donlan MA Meredith 2007 Sensory and multisensory representations within the cat rostral suprasylvian cortex J Comp Neurol 503 110 127 10.1002/cne.21378 17480013 (Pubitemid 47024421)
13. HR Clemo GK Sharma BL Allman MA Meredith 2008 Auditory projections to extrastriate visual cortex: connectional basis for multisensory processing in 'unimodal' visual neurons Exp Brain Res 191 37 47 10.1007/s00221-008-1493-7 18648784
14. NM Da Costa KAC Martin 2009 Selective targeting of the dendrites of corticothalamic cells by thalamic afferents in area 17 of the cat J Neurosci 29 13919 13928 10.1523/JNEUROSCI.2785-09.2009 19890002
15. J DeFelipe 1993 Neocortical neuronal diversity: chemical heterogeneity revealed by colocalization studies of classic neurotransmitters, neuropeptides, calcium-binding proteins, and cell surface molecules Cereb Cortex 3 273 289 10.1093/cercor/3.4.273 1:STN:280:DyaK2c%2Fgtl2ntA%3D%3D 8104567
16. LR Dehner LP Keniston HR Clemo MA Meredith 2004 Cross-modal circuitry between auditory and somatosensory areas of the cat anterior ectosylvian sulcal cortex: a 'new' inhibitory form of multisensory convergence Cereb Cortex 14 387 403 10.1093/cercor/bhg135 15028643 (Pubitemid 38506970)
17. RT Fremeau Jr MD Troyer I Pahner GO Nygaard CH Tran RJ Reimer EE Bellocchio D Fortin J Storm-Mathisen RH Edwards 2001 The expression of vesicular glutamate transporters defines two classes of excitatory synapse Neuron 31 247 260 10.1016/S0896-6273(01)00344-0 1:CAS:528:DC%2BD3MXlvFelt7s%3D 11502256 (Pubitemid 32762978)
18. ZM Fuzessery JC Hall 1996 Role of GABA I shaping frequency tuning and creating FM sweep selectivity in the inferior colliculus J Neurophysiol 76 1059 1073 1:CAS:528:DyaK28Xls1akur4%3D 8871220
19. A Graziano XB Liu KD Murray EG Jones 2008 Vesicular glutamate transporters define two sets of glutamatergic afferents to the somatosensory thalamus and two thalamocortical projections in the mouse J Comp Neurol 507 1258 1276 10.1002/cne.21592 1:CAS:528:DC%2BD1cXivFygsL8%3D 18181146 (Pubitemid 351288025)
20. A Hagiwara Y Fukazawa M Deguchi-Tawarada T Ohtsuka R Shigemoto 2005 Differential distribution of release-related proteins in the hippocampal CA3 area as revealed by freeze-fracture replica labeling J Comp Neurol 489 195 216 10.1002/cne.20633 1:CAS:528:DC%2BD2MXnvFyhs78%3D 15983999 (Pubitemid 40994626)
21. AJ Hall SG Lomber 2008 Auditory cortex projections target the peripheral field representation of primary visual cortex Exp Brain Res 190 413 430 10.1007/s00221-008-1485-7 18641978
22. JK Harting BV Updyke DP Van Lieshout 1992 Corticotectal projections in the cat: anterograde transport studies of twenty-five cortical areas J Comp Neurol 324 379 414 10.1002/cne.903240308 1:STN:280:DyaK3s%2FhslWhtg%3D%3D 1401268
23. E Herzog S Takamori R Jahn N Brose SM Wojcik 2006 Synaptic and vesicular co-localization of the glutamate transporters VGLUT1 and VGLUT2 in the mouse hippocampus J Neurochem 99 1011 1018 10.1111/j.1471-4159.2006.04144.x 1:CAS:528:DC%2BD28Xht1eju7rK 16942593 (Pubitemid 44583457)
24. H Jiang F Lepore M Ptito JP Guillemot 1994 Sensory modality distribution in the anterior ectosylvian cortex (AEC) of cats Exp Brain Res 97 404 414 10.1007/BF00241534 1:STN:280:DyaK2c3ksVOgtA%3D%3D 8187853 (Pubitemid 24096369)
25. LP Keniston SC Henderson MA Meredith 2006 Confocal identification of multisensory convergence on cortical neurons in cat Soc Neurosci Abstr 137 18
26. LP Keniston BA Allman MA Meredith HR Clemo 2009 Somatosensory and multisensory properties of the medial bank of the ferret rostral suprasylvian sulcus Exp Brain Res 196 239 251 10.1007/s00221-009-1843-0 1:STN:280: DC%2BD1Mvgt1Olsw%3D%3D 19466399
27. P Lakatos CM Chen MN O'Connell A Mills CE Schroeder 2007 Neuronal oscillations and multisensory interaction in primary auditory cortex Neuron 53 279 292 10.1016/j.neuron.2006.12.011 1:CAS:528:DC%2BD2sXhsVWns7g%3D 17224408 (Pubitemid 46074398)
28. CX Li JC Callaway RS Waters 2002 Removal of GABAergic inhibition alters subthreshold input in neurons in forepaw barrel subfield (FBS) in rat first somatosensory cortex (SI) after digit stimulation Exp Brain Res 145 411 428 10.1007/s00221-002-1124-7 1:CAS:528:DC%2BD38Xls12nsLg%3D 12172653 (Pubitemid 34994784)
29. H Markram M Toledo-Rodriguez Y Wang A Gupta G Silberberg C Wu 2004 Interneurons of the neurocortical inhibitory system Nat Neurosci Rev 5 793 807 10.1038/nrn1519 1:CAS:528:DC%2BD2cXns1Kiurc%3D (Pubitemid 39336216)
30. Meredith MA (2004) Cortico-cortical connectivity and the architecture of cross-modal circuits. In: Spence C, Calvert G Stein B (eds) Handbook of multisensory processes, MIT Press, pp 343-355
31. MA Meredith BL Allman 2009 Subthreshold multisensory processing in cat auditory cortex NeuroReport 20 126 131 10.1097/WNR.0b013e32831d7bb6 19057421
32. MA Meredith HR Clemo 1989 Auditory cortical projection from the anterior ectosylvian sulcus (Field AES) to the superior colliculus in the cat: an anatomical and electrophysiological study J Comp Neurol 289 687 707 10.1002/cne.902890412 1:STN:280:DyaK3c%2FnvVOgsw%3D%3D 2592605 (Pubitemid 20001388)
33. MA Meredith LR Keniston LR Dehner HR Clemo 2006 Crossmodal projections from somatosensory area SIV to the auditory field of the anterior ectosylvian sulcus (FAES) in cat: further evidence for subthreshold forms of multisensory processing Exp Brain Res 172 472 484 10.1007/s00221-006-0356-3 16501962 (Pubitemid 43989353)
34. JP Rauschecker M Korte 1993 Auditory compensation for early blindness in cat cerebral cortex J Neurosci 13 4538 4548 1:STN:280:DyaK2c%2FhsFegsA%3D%3D 8410202
35. F Reinoso-Suarez JM Roda 1985 Topographical organization of the cortical afferent connections to the cortex of the anterior ectosylvian sulcus in the cat Exp Brain Res 59 313 324 10.1007/BF00230911 1:STN:280:DyaL2M3osFCgtg%3D%3D 2411583 (Pubitemid 15029809)
36. K Richter A Hess H Scheich 1999 Functional mapping of transsynaptic effects of local manipulation of inhibition in gerbil auditory cortex Brain Res 831 184 199 10.1016/S0006-8993(99)01440-7 1:CAS:528:DyaK1MXjsF2qur0%3D 10411998 (Pubitemid 29336202)
37. SE Shore Z Vass NL Wys RA Altschuler 2000 Trigeminal ganglion innervates the auditory brainstem J Comp Neurol 419 271 285 10.1002/(SICI)1096- 9861(20000410)419:3<271::AID-CNE1>3.0.CO;2-M 1:STN:280: DC%2BD3c7ovFyrug%3D%3D 10723004 (Pubitemid 30134139)
38. SE Shore KH El J Lu 2003 Effects of trigeminal ganglion stimulation on unit activity of ventral cochlear nucleus neurons Neurosci 119 1085 1101 10.1016/S0306-4522(03)00207-0 1:CAS:528:DC%2BD3sXkvVChsLw%3D (Pubitemid 36776457)
39. AM Sillito TE Salt JA Kemp 1985 Modulatory and inhibitory processes in the visual cortex Vision Res 25 375 381 10.1016/0042-6989(85)90062-8 1:STN:280:DyaL2M3nsVeqsA%3D%3D 2862740 (Pubitemid 15094578)
40. CC Stichel U Kagi CW Heizmann 1986 Parvalbumin in cat brain: isolation, characterization and localization J Neurochem 47 46 53 1:CAS:528: DyaL28XkslCmtL8%3D 3711911
41. T Sugihara MD Diltz BB Averbeck LM Romanski 2006 Integration of auditory and visual communication information in the primate ventrolateral prefrontal cortex J Neurosci 26 11138 11147 10.1523/JNEUROSCI.3550-06.2006 1:CAS:528:DC%2BD28XhtFymsLnE 17065454 (Pubitemid 44772202)
42. S Takamori JS Rhee C Rosenmund R Jahn 2000 Identification of a vesicular glutamate transporter that defines a glutamatergic phenotype in neurons Nature 407 189 194 10.1038/35025070 1:CAS:528:DC%2BD3cXmvVSmt7o%3D 11001057
43. WA Teder-Salejarvi TF Munte F Sperlich SA Hillyard 1999 Intra-modal and cross-modal spatial attention to auditory and visual stimuli. An event-related brain potential study Brain Res Cogn Brain Res 8 327 343 10.1016/S0926-6410(99) 00037-3 1:STN:280:DC%2BD3c%2FisFKksQ%3D%3D 10556609 (Pubitemid 29518317)
44. CL Veenman A Reiner MG Honig 1992 Biotinylated dextran amine as an anterograde tracer for single- and double-labeling studies J Neurosci Methods 41 239 254 10.1016/0165-0270(92)90089-V 1:CAS:528:DyaK38XltVOksbs%3D 1381034
45. M Vinkenoog MC van den Oever HB Uylings FG Wouterlood 2005 Random or selective neuroanatomical connectivity. Study of the distribution of fibers over two populations of identified interneurons in cerebral cortex Brain Res Brain Res Protoc 14 67 76 10.1016/j.brainresprot.2004.09.005 1:CAS:528: DC%2BD2MXhsV2jtbY%3D 15721812 (Pubitemid 40249947)
46. MT Wallace R Ramachandran BE Stein 2004 A revised view of sensory cortical parcellation Proc Natl Acad Sci USA 101 2167 2172 10.1073/pnas. 0305697101 1:CAS:528:DC%2BD2cXhs1Srs7c%3D 14766982 (Pubitemid 38229033)
47. J Wang D Caspary RJ Salvi 2000 GABA-A antagonist causes dramatic expansion of tuning in primary auditory cortex NeuroReport 11 1137 1140 1:CAS:528:DC%2BD3cXivFOgtrs%3D 10790896
48. X Wang Y Wei V Vaingankar Q Wang K Koepsell FT Sommer HA Hirsch 2007 Feedforward excitation and inhibition evoke dual modes of firing in the cat's visual thalamus during naturalistic viewing Neuron 55 465 478 10.1016/j.neuron.2007.06.039 1:CAS:528:DC%2BD2sXpsVGlt74%3D 17678858 (Pubitemid 47126264)