The auditory cortex of nonhuman primates is comprised of a constellation of at least twelve interconnected areas distributed across three major regions on the superior temporal gyrus: core, belt, and parabelt. Individual areas are distinguished on the basis of unique profiles comprising architectonic features, thalamic and cortical connections, and neuron response properties. Recent demonstrations of convergent auditory – somatosensory interactions in the caudomedial (CM) and caudolateral (CL) belt areas prompted us to pursue anatomical studies to identify the source(s) of somatic input to auditory cortex. Corticocortical and thalamocortical connections were revealed by injecting neuroanatomical tracers into CM, CL, and adjoining fields of marmoset (Callithrix jacchus jacchus) and macaque (Macaca mulatta) monkeys. In addition to auditory cortex, the cortical connections of CM and CL included somatosensory (retroinsular, Ri; granular insula, Ig) and multisensory areas (temporal parietal occipital, temporal parietal temporal). Thalamic inputs included the medial geniculate complex and several multisensory nuclei (supra- geniculate, posterior, limitans, medial pulvinar), but not the ventroposterior complex. Injections of the core (A1, R) and rostromedial areas of auditory cortex revealed sparse multisensory connections. The results suggest that areas Ri and Ig are the principle sources of somatosensory input to the caudal belt, while multisensory regions of cortex and thalamus may also contribute. The present data add to growing evidence of multisensory convergence in cortical areas previously considered to be ‘unimodal’, and also indicate that auditory cortical areas differ in this respect.
Get full access to this article
View all access options for this article.
References
1.
AitkinL MKudoMIrvineD R, 1988“Connections of the primary auditory cortex in the common marmoset, Callithrix jacchus jacchus”Journal of Comparative Neurology269235–248
2.
AkbarianSGrüsserO JGuldinW O, 1992“Thalamic connections of the vestibular cortical fields in the squirrel monkey (Saimiri sciureus)”Journal of Comparative Neurology326423–441
3.
AkbarianSGrüsserO JGuldinW O, 1994“Corticofugal connections between the cerebral cortex and brainstem vestibular nuclei in the macaque monkey”Journal of Comparative Neurology339421–437
4.
AllmanJ MKaasJ H, 1971“Representation of the visual field in striate and adjoining cortex of the owl monkey (Aotus trivirgatus)”Brain Research3589–106
5.
BarbasH, 1993“Organization of cortical afferent input to orbitofrontal areas in the rhesus monkey”Neuroscience56841–864
6.
BarnesC LPandyaD N, 1992“Efferent cortical connections of multimodal cortex of the superior temporal sulcus in the rhesus monkey”Journal of Comparative Neurology318222–244
7.
BeauchampM S, 2005“See me, hear me, touch me: multisensory integration in lateral occipital-temporal cortex”Current Opinion in Neurobiology15145–153
8.
BieserA, 1998“Processing of twitter-call fundamental frequencies in insula and auditory cortex of squirrel monkeys”Experimental Brain Research122139–148
9.
BieserAMuller-PreussP, 1996“Auditory responsive cortex in the squirrel monkey: neural responses to amplitude-modulated sounds”Experimental Brain Research108273–284
10.
BroschMSeleznevaEScheichH, 2005“Nonauditory events of a behavioral procedure activate auditory cortex of highly trained monkeys”Journal of Neuroscience256797–6806
11.
BurtonHFabriMAllowayK, 1995“Cortical areas within the lateral sulcus connected to cutaneous representations in areas 3b and 1: a revised interpretation of the second somatosensory area in macaque monkeys”Journal of Comparative Neurology355539–562
12.
BurtonHJonesE G, 1976“The posterior thalamic region and its cortical projection in New World and Old World monkeys”Journal of Comparative Neurology168249–301
13.
CaetanoGJousmakiV, 2006“Evidence of vibrotactile input to human auditory cortex”Neuroimage2915–28
14.
CappeCBaroneP, 2005“Heteromodal connections supporting multisensory integration at low levels of cortical processing in the monkey”European Journal of Neuroscience222886–2902
15.
CavadaCCompanyTTejedorJCruz-RizzoloR JReinoso-SuarezF, 2000“The anatomical connections of the macaque monkey orbitofrontal cortex. A review”Cerebral Cortex10220–242
16.
CipolloniP BPandyaD N, 1989“Connectional analysis of the ipsilateral and contralateral afferent neurons of the superior temporal region in the Rhesus monkey”Journal of Comparative Neurology281567–585
17.
CoqJ OQiHCollinsC EKaasJ H, 2004“Anatomical and functional organization of somatosensory areas of the lateral fissure of the New World titi monkey (Callicebus moloch)”Journal of Comparative Neurology476363–387
18.
CusickC GWallJ TFellemanD JKaasJ H, 1989“Somatotopic organization of the lateral sulcus of own monkeys: area 3b, S-II, and a ventral somatosensory area”Journal of Comparative Neurology282169–190
19.
de la MotheL ABlumellSKajikawaYHackettT A, 2006a“Cortical connections of auditory cortex in marmoset monkeys: core and medial belt regions”Journal of Comparative Neurology49627–71
20.
de la MotheL ABlumellSKajikawaYHackettT A, 2006b“Thalamic connections of auditory cortex in marmoset monkeys: core and medial belt regions”Journal of Comparative Neurology49672–96
21.
De VitoJ LSimmonsD M, 1976“Some connections of the posterior thalamus in monkey”Experimental Neurology51347–362
22.
DingS LMorecraftR JVan HoesenG W, 2003“Topography, cytoarchitecture, and cellular phenotypes of cortical areas that form the cingulo-parahippocampal isthmus and adjoining retrocalcarine areas in the monkey”Journal of Comparative Neurology456184–201
23.
DisbrowELitinasERecanzoneG HPadbergJKrubitzerL, 2003“Cortical connections of the second somatosensory area and the parietal ventral area in macaque monkeys”Journal of Comparative Neurology462382–399
24.
von EconomoCHornL, 1930“Uber Windungsrelief, Masse und Rindenarchitektonik der Supratemporalfläche, ihre individuellen und ihre Seitenunterschiede”Zeitschrift für Neurologie und Psychiatrie130678–757
25.
FalchierAClavagnierSBaronePKennedyH, 2002“Anatomical evidence of multimodal integration in primate striate cortex”Journal of Neuroscience225749–5759
26.
FoxeJ JMoroczI AMurrayM MHigginsB AJavittD CSchroederC E, 2000“Multisensory auditory – somatosensory interactions in early cortical processing revealed by high-density electrical mapping”Cognitive Brain Research1077–83
27.
FoxeJ JWylieG RMartinezASchroederC EJavittD CGuilfoyleDRitterWMurrayM M, 2002“Auditory – somatosensory multisensory processing in auditory association cortex: an fMRI study”Journal of Neurophysiology88540–543
28.
FriedmanD PMurrayE A, 1986“Thalamic connectivity of the second somatosensory area and neighboring somatosensory fields of the lateral sulcus of the macaque”Journal of Comparative Neurology252348–373
29.
FriedmanD PMurrayE AO'NeillJ BMishkinM, 1986“Cortical connections of the somatosensory fields of the lateral sulcus of macaques: evidence for a corticolimbic pathway for touch”Journal of Comparative Neurology252323–347
30.
FuK MJohnstonT AShahA SArnoldLSmileyJHackettT AGarraghtyP ESchroederC E, 2003“Auditory cortical neurons respond to somatosensory stimulation”Journal of Neuroscience237510–7515
31.
FuK MShahA SMnO CMcGinnisTEckholdtHLakatosPSmileyJSchroederC E, 2004“Timing and laminar profile of eye position effects on auditory responses in primate auditory cortex”Journal of Neurophysiology923522–3531
32.
GalaburdaA MPandyaD N, 1983“The intrinsic architectonic and connectional organization of the superior temporal region of the rhesus monkey”Journal of Comparative Neurology221169–184
33.
GalaburdaASanidesF, 1980“Cytoarchitectonic organization of the human auditory cortex”Journal of Comparative Neurology190597–610
34.
GattasS RSousaA PMishkinMUngerleiderL G, 1997“Cortical projections of area V2 in the macaque”Cerebral Cortex7110–129
35.
GhazanfarA AMaierJ XHoffmanK LLogothetisN K, 2005“Multisensory integration of dynamic faces and voices in rhesus monkey auditory cortex”Journal of Neuroscience255004–5012
36.
GhanzanfarA ASchroederC E, 2006“Is neocortex essentially multisensory?”Trends in Cognitive Sciences10278–285
37.
GobbeléRSchürmannMForssNJuottonenKBuchnerHHariR, 2003“Activation of the human posterior parietal and temporoparietal cortices during audiotactile interaction”Neuroimage20503–511
38.
GrüsserO JPauseMSchreiterU, 1990a“Localization and responses of neurones in the parieto-insular vestibular cortex of awake monkeys' (Macaca fascicularis)”Journal of Physiology430537–557
39.
GrüsserO JPauseMSchreiterU, 1990b“Vestibular neurones in the parieto-insular cortex of monkeys (Macaca fascicularis): visual and neck receptor responses”Journal of Physiology430559–583
40.
GuldinW OAkbarianSGrusserO J, 1992“Cortico-cortical connections and cytoarchitectonics of the primate vestibular cortex: a study in squirrel monkeys (Saimiri sciureus)”Journal of Comparative Neurology326375–401
41.
HackettT A, 2002“The comparative anatomy of the primate auditory cortex”, in Primate Audition: Behavior and Neurobiology Ed. GhazanfarA (Boca Raton, FL: CRC Press) pp 199–226
42.
HackettT A, 2007“Organization and correspondence of the auditory cortex of humans and non-human primates”, in Evolution of the Nervous System Ed. KaasJ (Oxford: Elsevier) pp 109–119
43.
HackettT Ade la MotheL AUlbertIKarmosGSmileyJ FSchroederC E, 2007“Multisensory convergence in auditory cortex, II. Thalamocortical connections of the caudal superior temporal plane”Journal of Comparative Neurology502924–952
44.
HackettT AKaasJ H, 2004“Auditory cortex in primates: functional subdivisions and processing streams”, in The Cognitive Neurosciences III3rd edition, Ed. GazzanigaM S (Boston, MA: MIT Press) pp 215–231
45.
HackettT AKarmosGSchroederC EUlbertISterbing-D'AngeloS JD'AngeloW RKajikawaYBlumellSde la MotheL A, 2005“Neurosurgical access to cortical areas in the lateral fissure of primates”Journal of Neuroscience Methods141103–113
46.
HackettT APreussT MKaasJ H, 2001“Architectonic identification of the core region in auditory cortex of macaques, chimpanzees, and humans”Journal of Comparative Neurology441197–222
47.
HackettT AStepniewskaIKaasJ H, 1998a“Subdivisions of auditory cortex and ipsilateral cortical connections of the parabelt auditory cortex in macaque monkeys”Journal of Comparative Neurology394475–495
48.
HackettT AStepniewskaIKaasJ H, 1998b“Thalamocortical connections of the parabelt auditory cortex in macaque monkeys”Journal of Comparative Neurology394271–286
49.
JonesE GBurtonH, 1976“Areal differences in the laminar distribution of thalamic afferents in cortical fields of the insular, parietal and temporal regions of primates”Journal of Comparative Neurology168197–247
50.
JonesE GPowellT P, 1969“Connexions of the somatic sensory cortex of the rhesus monkey: I. Ipsilateral cortical connexions”Brain92477–502
51.
KaasJ HHackettT A, 2005“Subdivisions and connections of the auditory cortex in primates: a working model”, in The Auditory Cortex: Towards a Synthesis of Human and Animal Research Eds KonigRHeilPBudingerEScheichH (Mahwah, NJ: Lawrence Erlbaum Associates) pp 7–26
52.
KayserCPetkovC IAugathMLogothetisN K, 2005“Integration of touch and sound in auditory cortex”Neuron48373–384
53.
KitagawaNSpenceC, 2006“Audiotactile multisensory interactions in human information processing”Japanese Psychological Research48158–173
54.
KrubitzerLClareyJTweedaleRElstonGCalfordM, 1995“A redefinition of somatosensory areas in the lateral sulcus of macaque monkeys”Journal of Neuroscience153821–3839
55.
KrubitzerL AKaasJ H, 1990“The organization and connections of somatosensory cortex in marmosets”Journal of Neuroscience10952–974
56.
LakatosPChenC MO'ConnellM NMillsASchroederC E, 2007“Neuronal oscillations and multisensory interaction in primary auditory cortex”Neuron53279–292
57.
LakatosPPinczeZFuK GJavittD CKarmosGSchroederC E, 2005a“Timings of pure tone and noise-evoked responses in macaque auditory cortex”NeuroReport16933–937
58.
LakatosPShahA SKnuthK HUlbertIKarmosGSchroederC E, 2005b“An oscillatory hierarchy controlling neuronal excitability and stimulus processing in the auditory cortex”Journal of Neurophysiology941904–1911
59.
LehmannCHerdenerMEspositoFHublDdi SalleFSchefflerKBachD RFederspielAKretzRDierksTSeifritzE, 2006“Differential patterns of multisensory interactions in core and belt areas of human auditory cortex”Neuroimage31294–300
60.
LeinonenL, 1980a“Functional properties of neurons in the parietal retroinsular cortex in awake monkey”Acta Physiologica Scandinavica108381–384
61.
LeinonenL, 1980b“Functional properties of neurones in the posterior part of area 7 in awake monkey”Acta Physiologica Scandinavica108301–308
62.
LeinonenLHyvärinenJSovijärviR A, 1980“Functional properties of neurons in the temporoparietal association cortex of awake monkey”Experimental Brain Research39203–215
63.
LewisJ WVan EssenD C, 2000“Corticocortical connections of visual, sensorimotor, and multimodal processing areas in the parietal lobe of the macaque monkey”Journal of Comparative Neurology428112–137
64.
LinkeRSchweglerH, 2000“Convergent and complementary projections of the caudal paralaminar thalamic nuclei to rat temporal and insular cortex”Cerebral Cortex10753–771
65.
MacalusoEDriverJ, 2005“Multisensory spatial interactions: a window onto functional integration in the human brain”Trends in Neurosciences28264–271
66.
MesulamM MMufsonE J, 1982“Insula of the Old World monkey. I: Architectonics in the insulo-orbito-temporal component of the paralimbic brain”Journal of Comparative Neurology2121–22
67.
MesulamM MPandyaD N, 1973“The projections of the medial geniculate complex within the Sylvian fissure of the rhesus monkey”Brain Research60315–333
68.
MolinariMDell'AnnaM ERausellELeggioM GHashikawaTJonesE G, 1995“Auditory thalamocortical pathways defined in monkeys by calcium-binding protein immunoreactivity”Journal of Comparative Neurology362171–194
69.
MorecraftR JRocklandK SVan HoesenG W, 2000“Localization of area prostriata and its projection to the cingulated motor cortex in the rhesus monkey”Cerebral Cortex10192–203
70.
MorelAGarraghtyP EKaasJ H, 1993“Tonotopic organization, architectonic fields, and connections of auditory cortex in macaque monkeys”Journal of Comparative Neurology335437–459
71.
MorelAKaasJ H, 1992“Subdivisions and connections of auditory cortex in owl monkeys”Journal of Comparative Neurology31827–63
72.
MurrayM MHolholmSMichelC MHeslenfeldD JRitterWJavittD CSchroederC EFoxeJ J, 2005“Grabbing your ear: rapid auditory – somatosensory multisensory interactions in low-level sensory cortices are not constrained by stimulus alignment”Cerebral Cortex15963–974
73.
PalmerS MRosaM G, 2006“A distinct anatomical network of cortical areas for analysis of motion in far peripheral vision”European Journal of Neuroscience242389–2405
74.
PandyaD NHallettMMukherjeeS K, 1969“Intra- and inter-hemispheric connections of the neocortical auditory system in the rhesus monkey”Brain Research1449–65
75.
PandyaD NRoseneD L, 1993“Laminar termination patterns of thalamic, callosal, and association afferents in the primary auditory area of the rhesus monkey”Experiments in Neurology119220–234
76.
PandyaD NSanidesF, 1973“Architectonic parcellation of the temporal operculum in rhesus monkey and its projection pattern”Zeitschrift für Anatomie und Entwicklungsgeschichte139127–161
77.
PonsT PKaasJ H, 1986“Corticocortical connections of area 2 of somatosensory cortex in macaque monkeys: a correlative anatomical and electrophysiological study”Journal of Comparative Neurology248313–335
78.
QiH-XLyonD CKaasJ H, 2002“Cortical and thalamic connections of the parietal ventral somatosensory area in marmoset monkeys (Callithrix jacchus)”Journal of Comparative Neurology443168–182
79.
RauscheckerJ PTianBPonsTMishkinM, 1997“Serial and parallel processing in rhesus monkey auditory cortex”Journal of Comparative Neurology38289–103
80.
RobinsonC JBurtonH, 1980a“Organization of somatosensory receptive fields in cortical areas 7b, retroinsula, postauditory and granular insula of M. fascicularis”Journal of Comparative Neurology19269–92
81.
RobinsonC JBurtonH, 1980b“Somatic submodality distribution within the second somatosensory (SII), 7b, retroinsular, postauditory, and granular insular cortical areas of M. fascicularis”Journal of Comparative Neurology19293–108
82.
RobinsonC JBurtonH, 1980c“Somatotopographic organization in the second somatosensory area of M. fascicularis”Journal of Comparative Neurology19243–67
83.
RocklandK SOjimaH, 2003“Multisensory convergence in calcarine visual areas in macaque monkey”, international Journal of Psychophysiology50 (1–2) 19–26
84.
RosaM GCasagrandeV APreussTKaasJ H, 1997“Visual field representation in striate and prestriate cortices of a prosimian primate (Galago garnetti)”Journal of Neurophysiology773193–3217
85.
RosaM GSoaresJ GFioraniMJrGattassR, 1993“Cortical afferents of visual area MT in the Cebus monkey: possible homologies between New and Old World monkeys”Visual Neuroscience10827–855
86.
SchneiderR JFriedmanD PMishkinM, 1993“A modality-specific somatosensory area within the insula of the rhesus monkey”Brain Research621116–120
87.
SchroederC EFoxeJ J, 2002“The timing and laminar profile of converging inputs to multisensory areas of the macaque neocortex”Cognitive Brain Research14187–198
88.
SchroederC EFoxeJ J, 2005“Multisensory contributions to low-level, ‘unisensory’ processing”Current Opinion in Neurobiology15454–458
89.
SchroederC ELindsleyR WSpechtCMarcoviciASmileyJ FJavittD C, 2001“Somatosensory input to auditory association cortex in the macaque monkey”Journal of Neurophysiology851322–1327
90.
SchroederC ESmileyJFuK GMcGinnisTO'ConnellM NHackettT A, 2003“Anatomical mechanisms and functional implications of multisensory convergence in early cortical processing”international Journal of Psychophysiology505–17
91.
SchurmannMCaetanoGHlushchukYJousmakiVHariR, 2006“Touch activates human auditory cortex”Neuroimage301325–1331
92.
SeltzerBColaM GGutierrezCMasseeMWeldonCCusickC G, 1996“Overlapping and nonoverlapping cortical projections to cortex of the superior temporal sulcus in the rhesus monkey: double anterograde tracer studies”Journal of Comparative Neurology370173–190
93.
SmileyJ FHackettT AUlbertIKarmosGLakatosPJavittD CSchroederC E, 2007, “Multisensory convergence in auditory cortex, I. Cortical connections of the caudal superior temporal plane”Journal of Comparative Neurology502894–923
94.
SousaA PPinonM CGattassRRosaM G, 1991“Topographic organization of cortical input to striate cortex in the Cebus monkey: a fluorescent tracer study”Journal of Comparative Neurology308665–682
95.
SudakovKMacLeanP DReevesAMarinoR, 1971“Unit study of exteroceptive inputs to claustrocortex in awake, sitting, squirrel monkey”Brain Research2819–34
96.
SweetR ADorph-PetersenK ALewisD A, 2005“Mapping auditory core, lateral belt, and parabelt cortices in the human superior temporal gyrus”Journal of Comparative Neurology491270–289
97.
WallaceM TRamachandranRSteinB E, 2004“A revised view of sensory cortical parcellation”Proceedings of the National Academy of Sciences of the USA1012167–2172
98.
Werner-ReissUKellyK ATrauseA SUnderhillA MGrohJ M, 2003“Eye position affects activity in primary auditory cortex of primates”Current Biology13554–562
