Brain Structure and Function

, Volume 223, Issue 4, pp 1599–1614 | Cite as

Organization of auditory areas in the superior temporal gyrus of marmoset monkeys revealed by real-time optical imaging

  • Masataka Nishimura
  • Makoto Takemoto
  • Wen-Jie Song
Original Article


The prevailing model of the primate auditory cortex proposes a core–belt–parabelt structure. The model proposes three auditory areas in the lateral belt region; however, it may contain more, as this region has been mapped only at a limited spatial resolution. To explore this possibility, we examined the auditory areas in the lateral belt region of the marmoset using a high-resolution optical imaging technique. Based on responses to pure tones, we identified multiple areas in the superior temporal gyrus. The three areas in the core region, the primary area (A1), the rostral area (R), and the rostrotemporal area, were readily identified from their frequency gradients and positions immediately ventral to the lateral sulcus. Three belt areas were identified with frequency gradients and relative positions to A1 and R that were in agreement with previous studies: the caudolateral area, the middle lateral area, and the anterolateral area (AL). Situated between R and AL, however, we identified two additional areas. The first was located caudoventral to R with a frequency gradient in the ventrocaudal direction, which we named the medial anterolateral (MAL) area. The second was a small area with no obvious tonotopy (NT), positioned between the MAL and AL areas. Both the MAL and NT areas responded to a wide range of frequencies (at least 2–24 kHz). Our results suggest that the belt region caudoventral to R is more complex than previously proposed, and we thus call for a refinement of the current primate auditory cortex model.


Frequency gradient Optical imaging Primate auditory cortex Tonotopy 



This work was supported by Grant-in-Aid for Scientific Research on Innovative Areas “Adaptive Circuit Shift” (#15H01442) and “Dynamic Regulation of Brain Function by Scrap & Build System” (#17H05749) of the Ministry of Education, Culture, Sports, Science and Technology of Japan, and JSPS Grants (#25290006).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

429_2017_1574_MOESM1_ESM.eps (1.3 mb)
Figure S1. Correlation between t scores and ΔF/F0. Peak t score values and ΔF/F0 in response to the first 1 kHz tone shown in Fig. 1 were measured and plotted across every 10,000 pixels in the time window from 0 to 50 msec after the stimulus onset. (EPS 1281 KB)


  1. Aitkin LM, Merzenich MM, Irvine DR, Clarey JC, Nelson JE (1986) Frequency representation in auditory cortex of the common marmoset (Callithrix jacchus jacchus). J Comp Neurol 252:175–185CrossRefPubMedGoogle Scholar
  2. Bendor D, Wang X (2005) The neuronal representation of pitch in primate auditory cortex. Nature 436:1161–1165CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bendor D, Wang X (2008) Neural response properties of primary, rostral, and rostrotemporal core fields in the auditory cortex of marmoset monkeys. J Neurophysiol 100(2):888–906CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bieser A, Müller-Preuss P (1996) Auditory responsive cortex in the squirrel monkey: neural responses to amplitude-modulated sounds. Exp Brain Res 108:273–284CrossRefPubMedGoogle Scholar
  5. Brugge JF, Merzenich MM (1973) Responses of neurons in auditory cortex of the macaque monkey to monaural and binaural stimulation. J Neurophysiol 36(6):1138–1158CrossRefPubMedGoogle Scholar
  6. Camalier CR, D’Angelo WR, Sterbing-D’Angelo SJ, de la Mothe LA, Hackett TA (2012) Neural latencies across auditory cortex of macaque support a dorsal stream supramodal timing advantage in primates. Proc Natl Acad Sci USA 109(44):18168–18173CrossRefPubMedPubMedCentralGoogle Scholar
  7. de la Mothe LA, Blumell S, Kajikawa Y, Hackett TA (2006a) Cortical connections of the auditory cortex in marmoset monkeys: core and medial belt regions. J Comp Neurol 496(1):27–71CrossRefPubMedGoogle Scholar
  8. de la Mothe LA, Blumell S, Kajikawa Y, Hackett TA (2006b) Thalamic connections of the auditory cortex in marmoset monkeys: core and medial belt regions. J Comp Neurol 496:72–96CrossRefPubMedPubMedCentralGoogle Scholar
  9. Feng L, Wang X (2017) Harmonic template neurons in primate auditory cortex underlying complex sound processing. Proc Natl Acad Sci USA 114(5):E840–E848CrossRefPubMedPubMedCentralGoogle Scholar
  10. Grinvald A, Lieke EE, Frostig RD, Hildesheim R (1994) Cortical point-spread function and long-range lateral interactions revealed by real-time optical imaging of macaque monkey primary visual cortex. J Neurosci 14:2545–2568PubMedGoogle Scholar
  11. Horikawa J, Hosokawa Y, Kubota M, Nasu M, Taniguchi I (1996) Optical imaging of spatiotemporal patterns of glutamatergic excitation and GABAergic inhibition in the guinea-pig auditory cortex in vivo. J Physiol 497(Pt 3):629–638CrossRefPubMedPubMedCentralGoogle Scholar
  12. Horikawa J, Hess A, Nasu M, Hosokawa Y, Scheich H, Taniguchi I (2001) Optical imaging of neural activity in multiple auditory cortical fields of guinea pigs. Neuroreport 12:3335–3339CrossRefPubMedGoogle Scholar
  13. Imig TJ, Ruggero MA, Kitzes LM, Javel E, Brugge JF (1977) Organization of auditory cortex in the owl monkey (Aotus trivirgatus). J Comp Neurol 171:111–128CrossRefPubMedGoogle Scholar
  14. Inagaki S, Katura T, Kawaguchi H, Song W-J (2003) Isolation of neural activity from respiratory and heartbeat noises for in vivo optical recordings using independent component analysis. Neurosci Lett 352:9–12CrossRefPubMedGoogle Scholar
  15. Kaas JH, Hackett TA (2000) Subdivisions of auditory cortex and processing streams in primates. Proc Natl Acad Sci USA 97:11793–11799CrossRefPubMedPubMedCentralGoogle Scholar
  16. Kajikawa Y, de la Mothe LA, Blumell S, Hackett TA (2005) A comparison of neuron response properties in areas A1 and CM of the marmoset monkey auditory cortex: tones and broad band noise. J Neurophysiol 93:22–34CrossRefPubMedGoogle Scholar
  17. Kosaki H, Hashikawa T, He J, Jones EG (1997) Tonotopic organization of auditory cortical fields delineated by parvalbumin immunoreactivity in macaque monkeys. J Comp Neurol 386:304–316CrossRefPubMedGoogle Scholar
  18. Lu T, Wang X (2004) Information content of auditory cortical responses to time-varying acoustic stimuli. J Neurophysiol 91:301–313CrossRefPubMedGoogle Scholar
  19. Lu T, Liang L, Wang X (2001) Temporal and rate representations of time-varying signals in the auditory cortex of awake primates. Nat Neurosci 4:1131–1138CrossRefPubMedGoogle Scholar
  20. Luethke LE, Krubitzer LA, Kaas JH (1989) Connections of primary auditory cortex in the New World monkey, Saguinus. J Comp Neurol 285(4):487–513Google Scholar
  21. Maeda S, Inagaki S, Kawaguchi H, Song W-J (2001) Separation of signal and noise from in vivo optical recording in guinea pig using independent component analysis. Neurosci Lett 302:137–140CrossRefPubMedGoogle Scholar
  22. Merzenich MM, Brugge JF (1973) Representation of the cochlear partition of the superior temporal plane of the macaque monkey. Brain Res 50:275–296CrossRefPubMedGoogle Scholar
  23. Miller JM, Sutton D, Pfingst B, Ryan A, Beaton R, Gourevitch G (1972) Single cell activity in the auditory cortex of Rhesus monkeys: behavioral dependency. Science 177(4047):449–451CrossRefPubMedGoogle Scholar
  24. Morel A, Kaas JH (1992) Subdivisions and connections of auditory cortex in owl monkeys. J Comp Neurol 318:27–63CrossRefPubMedGoogle Scholar
  25. Morel A, Garraghty PE, Kaas JH (1993) Tonotopic organization, architectonic fields, and connections of auditory cortex in macaque monkeys. J Comp Neurol 335:437–459CrossRefPubMedGoogle Scholar
  26. Nagarajan SS, Cheung SW, Bedenbaugh P, Beitel RE, Schreiner CE, Merzenich MM (2002) Representation of spectral and temporal envelope of twitter vocalizations in common marmoset primary auditory cortex. J Neurophysiol 87:1723–1737CrossRefPubMedGoogle Scholar
  27. Nieto-Diego J, Malmierca MS (2016) Topographic distribution of stimulus-specific adaptation across auditory cortical fields in the anesthetized rat. PLoS Biol 14(3):e1002397CrossRefPubMedPubMedCentralGoogle Scholar
  28. Nishimura M, Song W-J (2014) Greenwood frequency-position relationship in the primary auditory cortex in guinea pigs. NeuroImage 89:181–191CrossRefPubMedGoogle Scholar
  29. Nishimura M, Shirasawa H, Kaizo HH, Song H W-J (2007) New field with tonotopic organization in guinea pig auditory cortex. J Neurophysiol 97:927–932CrossRefPubMedGoogle Scholar
  30. Paxinos G, Watson C, Petrides M, Rosa M, Tokuno H (2012) The marmoset brain in stereotaxic coordinates, 1st edn. Academic Press, New YorkGoogle Scholar
  31. Petkov CI, Kayser C, Augath M, Logothetis NK (2006) Functional imaging reveals numerous fields in the monkey auditory cortex. PLoS Biol 4(7):e215CrossRefPubMedPubMedCentralGoogle Scholar
  32. Petkov CI, Kayser C, Steudel T, Whittingstall K, Augath M, Logothetis NK (2008) A voice region in the monkey brain. Nat Neurosci 11(3):367–374CrossRefPubMedGoogle Scholar
  33. Philibert B, Beitel RE, Nagarajan SS, Bonham BH, Schreiner CE, Cheung SW (2005) Functional organization and hemispheric comparison of primary auditory cortex in the common marmoset (Callithrix jacchus). J Comp Neurol 487:391–406CrossRefPubMedGoogle Scholar
  34. Rauschecker JP, Tian B (2004) Processing of band-passed noise in the lateral auditory belt cortex of the rhesus monkey. J Neurophysiol 91:2578–2589CrossRefPubMedGoogle Scholar
  35. Rauschecker JP, Tian B, Hauser M (1995) Processing of complex sounds in the macaque nonprimary auditory cortex. Science 268:111–114CrossRefPubMedGoogle Scholar
  36. Rauschecker JP, Tian B, Pons T, Mishkin M (1997) Serial and parallel processing in rhesus monkey auditory cortex. J Comp Neurol 382:89–103CrossRefPubMedGoogle Scholar
  37. Recanzone GH, Schreiner CE, Sutter ML, Beitel RE, Merzenich MM (1999) Functional organization of spectral receptive fields in the primary auditory cortex of the owl monkey. J Comp Neurol 415(4):460–481CrossRefPubMedGoogle Scholar
  38. Recanzone GH, Guard DC, Phan ML (2000) Frequency and intensity response properties of single neurons in the auditory cortex of the behaving macaque monkey. J Neurophysiol 83:2315–2331CrossRefPubMedGoogle Scholar
  39. Song W-J, Kawaguchi H, Totoki S, Inoue Y, Katura T, Maeda S, Inagaki S, Shirasawa H, Nishimura M (2006) Cortical intrinsic circuits can support activity propagation through an isofrequency strip of the guinea pig primary auditory cortex. Cereb Cortex 16:718–729CrossRefPubMedGoogle Scholar
  40. Sweet RA, Dorph-Petersen KA, Lewis DA (2005) Mapping auditory core, lateral belt, and parabelt cortices in the human superior temporal gyrus. J Comp Neurol 491:270–289CrossRefPubMedGoogle Scholar
  41. Tian B, Rauschecker JP (2004) Processing of frequency-modulated sounds in the lateral auditory belt cortex of the rhesus monkey. J Neurophysiol 92:2993–3013CrossRefPubMedGoogle Scholar
  42. Tian B, Reser D, Durham A, Kustov A, Rauschecker JP (2001) Functional specialization in rhesus monkey auditory cortex. Science 292:290–293CrossRefPubMedGoogle Scholar
  43. Wang X (2013) The harmonic organization of auditory cortex. Front Syst Neurosci. Google Scholar
  44. Wang X, Kadia SC (2001) Differential representation of species-specific primate vocalizations in the auditory cortices of marmoset and cat. J Neurophysiol 86:2616–2620CrossRefPubMedGoogle Scholar
  45. Wang X, Merzenich MM, Beitel R, Schreiner CE (1995) Representation of a species-specific vocalization in the primary auditory cortex of the common marmoset: temporal and spectral characteristics. J Neurophysiol 74:2685–2706CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  1. 1.Department of Sensory and Cognitive Physiology, Graduate School of Medical SciencesKumamoto UniversityKumamotoJapan
  2. 2.Program for Leading Graduate Schools HIGO ProgramKumamoto UniversityKumamotoJapan

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