Unidirectional monosynaptic connections from auditory areas to the primary visual cortex in the marmoset monkey

Piotr Majka, Marcello G. P. Rosa, Shi Bai, Jonathan M. Chan, Bing-Xing Huo, Natalia Jermakow, Meng K. Lin, Yeonsook S. Takahashi, Ianina H. Wolkowicz, Katrina H. Worthy, Ramesh Rajan, David H. Reser, Daniel K. Wojcik, Hideyuki Okano, Partha Mitra

Research output: Contribution to journalArticleResearchpeer-review

Abstract

Until the late 20th Century, it was believed that different sensory modalities were
processed by largely independent pathways in the primate cortex, with cross-modal integration only occurring in specialized polysensory areas. This model was challenged by the finding that the peripheral representation of the primary visual cortex (V1) receives monosynaptic connections from areas of the auditory cortex in the macaque. However, auditory projections to V1 have not been reported in other primates. We investigated the existence of direct interconnections between V1 and auditory areas in the marmoset, a New World monkey. Labelled neurons in auditory cortex were observed following 4 out of 10 retrograde tracer injections involving V1. These projections to V1 originated in the caudal subdivisions of auditory cortex (primary auditory cortex, caudal belt and parabelt areas), and targeted parts of V1 that represent parafoveal and peripheral vision. Injections near the representation of the vertical meridian of the visual field labelled few or no cells in auditory cortex. We also placed 8 retrograde tracer injections involving core, belt and parabelt auditory areas,
none of which revealed direct projections from V1. These results confirm the existence of a direct, nonreciprocal projection from auditory areas to V1 in a different primate species, which has evolved separately from the macaque for over 30 million years. The essential similarity of these observations between marmoset and macaque indicate that early-stage audiovisual integration is a shared characteristic of primate sensory processing.
Original languageEnglish
Pages (from-to)111-131
Number of pages21
JournalBrain Structure and Function
Volume224
Issue number1
DOIs
Publication statusPublished - Jan 2019

Keywords

  • striate cortex
  • auditory cortex
  • connections
  • primate
  • audiovisual integration

Cite this

Majka, Piotr ; Rosa, Marcello G. P. ; Bai, Shi ; Chan, Jonathan M. ; Huo, Bing-Xing ; Jermakow, Natalia ; Lin, Meng K. ; Takahashi, Yeonsook S. ; Wolkowicz, Ianina H. ; Worthy, Katrina H. ; Rajan, Ramesh ; Reser, David H. ; Wojcik, Daniel K. ; Okano, Hideyuki ; Mitra, Partha. / Unidirectional monosynaptic connections from auditory areas to the primary visual cortex in the marmoset monkey. In: Brain Structure and Function. 2019 ; Vol. 224, No. 1. pp. 111-131.
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title = "Unidirectional monosynaptic connections from auditory areas to the primary visual cortex in the marmoset monkey",
abstract = "Until the late 20th Century, it was believed that different sensory modalities wereprocessed by largely independent pathways in the primate cortex, with cross-modal integration only occurring in specialized polysensory areas. This model was challenged by the finding that the peripheral representation of the primary visual cortex (V1) receives monosynaptic connections from areas of the auditory cortex in the macaque. However, auditory projections to V1 have not been reported in other primates. We investigated the existence of direct interconnections between V1 and auditory areas in the marmoset, a New World monkey. Labelled neurons in auditory cortex were observed following 4 out of 10 retrograde tracer injections involving V1. These projections to V1 originated in the caudal subdivisions of auditory cortex (primary auditory cortex, caudal belt and parabelt areas), and targeted parts of V1 that represent parafoveal and peripheral vision. Injections near the representation of the vertical meridian of the visual field labelled few or no cells in auditory cortex. We also placed 8 retrograde tracer injections involving core, belt and parabelt auditory areas,none of which revealed direct projections from V1. These results confirm the existence of a direct, nonreciprocal projection from auditory areas to V1 in a different primate species, which has evolved separately from the macaque for over 30 million years. The essential similarity of these observations between marmoset and macaque indicate that early-stage audiovisual integration is a shared characteristic of primate sensory processing.",
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author = "Piotr Majka and Rosa, {Marcello G. P.} and Shi Bai and Chan, {Jonathan M.} and Bing-Xing Huo and Natalia Jermakow and Lin, {Meng K.} and Takahashi, {Yeonsook S.} and Wolkowicz, {Ianina H.} and Worthy, {Katrina H.} and Ramesh Rajan and Reser, {David H.} and Wojcik, {Daniel K.} and Hideyuki Okano and Partha Mitra",
year = "2019",
month = "1",
doi = "10.1007/s00429-018-1764-4",
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Majka, P, Rosa, MGP, Bai, S, Chan, JM, Huo, B-X, Jermakow, N, Lin, MK, Takahashi, YS, Wolkowicz, IH, Worthy, KH, Rajan, R, Reser, DH, Wojcik, DK, Okano, H & Mitra, P 2019, 'Unidirectional monosynaptic connections from auditory areas to the primary visual cortex in the marmoset monkey', Brain Structure and Function, vol. 224, no. 1, pp. 111-131. https://doi.org/10.1007/s00429-018-1764-4

Unidirectional monosynaptic connections from auditory areas to the primary visual cortex in the marmoset monkey. / Majka, Piotr; Rosa, Marcello G. P.; Bai, Shi; Chan, Jonathan M.; Huo, Bing-Xing; Jermakow, Natalia; Lin, Meng K.; Takahashi, Yeonsook S.; Wolkowicz, Ianina H.; Worthy, Katrina H.; Rajan, Ramesh; Reser, David H.; Wojcik, Daniel K.; Okano, Hideyuki; Mitra, Partha.

In: Brain Structure and Function, Vol. 224, No. 1, 01.2019, p. 111-131.

Research output: Contribution to journalArticleResearchpeer-review

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T1 - Unidirectional monosynaptic connections from auditory areas to the primary visual cortex in the marmoset monkey

AU - Majka, Piotr

AU - Rosa, Marcello G. P.

AU - Bai, Shi

AU - Chan, Jonathan M.

AU - Huo, Bing-Xing

AU - Jermakow, Natalia

AU - Lin, Meng K.

AU - Takahashi, Yeonsook S.

AU - Wolkowicz, Ianina H.

AU - Worthy, Katrina H.

AU - Rajan, Ramesh

AU - Reser, David H.

AU - Wojcik, Daniel K.

AU - Okano, Hideyuki

AU - Mitra, Partha

PY - 2019/1

Y1 - 2019/1

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AB - Until the late 20th Century, it was believed that different sensory modalities wereprocessed by largely independent pathways in the primate cortex, with cross-modal integration only occurring in specialized polysensory areas. This model was challenged by the finding that the peripheral representation of the primary visual cortex (V1) receives monosynaptic connections from areas of the auditory cortex in the macaque. However, auditory projections to V1 have not been reported in other primates. We investigated the existence of direct interconnections between V1 and auditory areas in the marmoset, a New World monkey. Labelled neurons in auditory cortex were observed following 4 out of 10 retrograde tracer injections involving V1. These projections to V1 originated in the caudal subdivisions of auditory cortex (primary auditory cortex, caudal belt and parabelt areas), and targeted parts of V1 that represent parafoveal and peripheral vision. Injections near the representation of the vertical meridian of the visual field labelled few or no cells in auditory cortex. We also placed 8 retrograde tracer injections involving core, belt and parabelt auditory areas,none of which revealed direct projections from V1. These results confirm the existence of a direct, nonreciprocal projection from auditory areas to V1 in a different primate species, which has evolved separately from the macaque for over 30 million years. The essential similarity of these observations between marmoset and macaque indicate that early-stage audiovisual integration is a shared characteristic of primate sensory processing.

KW - striate cortex

KW - auditory cortex

KW - connections

KW - primate

KW - audiovisual integration

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DO - 10.1007/s00429-018-1764-4

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