3D topology of orientation columns in visual cortex revealed by functional optical coherence tomography

Yu Nakamichi, Valery A. Kalatsky, Hideyuki Watanabe, Takayuki Sato, Rajagopalan Umamaheswari, Manabu Tanifuji

Research output: Contribution to journalArticle

Abstract

Orientation tuning is a canonical neuronal response property of six-layer visual cortex that is encoded in pinwheel structures with center orientation singularities. Optical imaging of intrinsic signals enables us to map these surface two-dimensional (2D) structures, whereas lack of appropriate techniques has not allowed us to visualize depth structures of orientation coding. In the present study, we performed functional optical coherence tomography (fOCT), a technique capable of acquiring a 3D map of the intrinsic signals, to study the topology of orientation coding inside the cat visual cortex. With this technique, for the first time, we visualized columnar assemblies in orientation coding that had been predicted from electrophysiological recordings. In addition, we found that the columnar structures were largely distorted around pinwheel centers: center singularities were not rigid straight lines running perpendicularly to the cortical surface but formed twisted string-like structures inside the cortex that turned and extended horizontally through the cortex. Looping singularities were observed with their respective termini accessing the same cortical surface via clockwise and counterclockwise orientation pinwheels. These results suggest that a 3D topology of orientation coding cannot be fully anticipated from 2D surface measurements. Moreover, the findings demonstrate the utility of fOCT as an in vivo mesoscale imaging method for mapping functional response properties of cortex in the depth axis. NEW & NOTEWORTHY We used functional optical coherence tomography (fOCT) to visualize three-dimensional structure of the orientation columns with millimeter range and micrometer spatial resolution. We validated vertically elongated columnar structure in iso-orientation domains. The columnar structure was distorted around pinwheel centers. An orientation singularity formed a string with tortuous trajectories inside the cortex and connected clockwise and counterclockwise pinwheel centers in the surface orientation map. The results were confirmed by comparisons with conventional optical imaging and electrophysiological recordings.

Original languageEnglish
Pages (from-to)1562-1575
Number of pages14
JournalJournal of neurophysiology
Volume119
Issue number4
DOIs
Publication statusPublished - 2018 Apr 1
Externally publishedYes

Keywords

  • functional architecture
  • functional imaging
  • optical coherence tomography
  • optical imaging
  • orientation column
  • visual cortex

ASJC Scopus subject areas

  • Neuroscience(all)
  • Physiology

Cite this

3D topology of orientation columns in visual cortex revealed by functional optical coherence tomography. / Nakamichi, Yu; Kalatsky, Valery A.; Watanabe, Hideyuki; Sato, Takayuki; Umamaheswari, Rajagopalan; Tanifuji, Manabu.

In: Journal of neurophysiology, Vol. 119, No. 4, 01.04.2018, p. 1562-1575.

Research output: Contribution to journalArticle

Nakamichi, Yu ; Kalatsky, Valery A. ; Watanabe, Hideyuki ; Sato, Takayuki ; Umamaheswari, Rajagopalan ; Tanifuji, Manabu. / 3D topology of orientation columns in visual cortex revealed by functional optical coherence tomography. In: Journal of neurophysiology. 2018 ; Vol. 119, No. 4. pp. 1562-1575.
@article{aef704c7c82549cd8a85a56d6cf2ba7b,
title = "3D topology of orientation columns in visual cortex revealed by functional optical coherence tomography",
abstract = "Orientation tuning is a canonical neuronal response property of six-layer visual cortex that is encoded in pinwheel structures with center orientation singularities. Optical imaging of intrinsic signals enables us to map these surface two-dimensional (2D) structures, whereas lack of appropriate techniques has not allowed us to visualize depth structures of orientation coding. In the present study, we performed functional optical coherence tomography (fOCT), a technique capable of acquiring a 3D map of the intrinsic signals, to study the topology of orientation coding inside the cat visual cortex. With this technique, for the first time, we visualized columnar assemblies in orientation coding that had been predicted from electrophysiological recordings. In addition, we found that the columnar structures were largely distorted around pinwheel centers: center singularities were not rigid straight lines running perpendicularly to the cortical surface but formed twisted string-like structures inside the cortex that turned and extended horizontally through the cortex. Looping singularities were observed with their respective termini accessing the same cortical surface via clockwise and counterclockwise orientation pinwheels. These results suggest that a 3D topology of orientation coding cannot be fully anticipated from 2D surface measurements. Moreover, the findings demonstrate the utility of fOCT as an in vivo mesoscale imaging method for mapping functional response properties of cortex in the depth axis. NEW & NOTEWORTHY We used functional optical coherence tomography (fOCT) to visualize three-dimensional structure of the orientation columns with millimeter range and micrometer spatial resolution. We validated vertically elongated columnar structure in iso-orientation domains. The columnar structure was distorted around pinwheel centers. An orientation singularity formed a string with tortuous trajectories inside the cortex and connected clockwise and counterclockwise pinwheel centers in the surface orientation map. The results were confirmed by comparisons with conventional optical imaging and electrophysiological recordings.",
keywords = "functional architecture, functional imaging, optical coherence tomography, optical imaging, orientation column, visual cortex",
author = "Yu Nakamichi and Kalatsky, {Valery A.} and Hideyuki Watanabe and Takayuki Sato and Rajagopalan Umamaheswari and Manabu Tanifuji",
year = "2018",
month = "4",
day = "1",
doi = "10.1152/jn.00921.2017",
language = "English",
volume = "119",
pages = "1562--1575",
journal = "Journal of Neurophysiology",
issn = "0022-3077",
publisher = "American Physiological Society",
number = "4",

}

TY - JOUR

T1 - 3D topology of orientation columns in visual cortex revealed by functional optical coherence tomography

AU - Nakamichi, Yu

AU - Kalatsky, Valery A.

AU - Watanabe, Hideyuki

AU - Sato, Takayuki

AU - Umamaheswari, Rajagopalan

AU - Tanifuji, Manabu

PY - 2018/4/1

Y1 - 2018/4/1

N2 - Orientation tuning is a canonical neuronal response property of six-layer visual cortex that is encoded in pinwheel structures with center orientation singularities. Optical imaging of intrinsic signals enables us to map these surface two-dimensional (2D) structures, whereas lack of appropriate techniques has not allowed us to visualize depth structures of orientation coding. In the present study, we performed functional optical coherence tomography (fOCT), a technique capable of acquiring a 3D map of the intrinsic signals, to study the topology of orientation coding inside the cat visual cortex. With this technique, for the first time, we visualized columnar assemblies in orientation coding that had been predicted from electrophysiological recordings. In addition, we found that the columnar structures were largely distorted around pinwheel centers: center singularities were not rigid straight lines running perpendicularly to the cortical surface but formed twisted string-like structures inside the cortex that turned and extended horizontally through the cortex. Looping singularities were observed with their respective termini accessing the same cortical surface via clockwise and counterclockwise orientation pinwheels. These results suggest that a 3D topology of orientation coding cannot be fully anticipated from 2D surface measurements. Moreover, the findings demonstrate the utility of fOCT as an in vivo mesoscale imaging method for mapping functional response properties of cortex in the depth axis. NEW & NOTEWORTHY We used functional optical coherence tomography (fOCT) to visualize three-dimensional structure of the orientation columns with millimeter range and micrometer spatial resolution. We validated vertically elongated columnar structure in iso-orientation domains. The columnar structure was distorted around pinwheel centers. An orientation singularity formed a string with tortuous trajectories inside the cortex and connected clockwise and counterclockwise pinwheel centers in the surface orientation map. The results were confirmed by comparisons with conventional optical imaging and electrophysiological recordings.

AB - Orientation tuning is a canonical neuronal response property of six-layer visual cortex that is encoded in pinwheel structures with center orientation singularities. Optical imaging of intrinsic signals enables us to map these surface two-dimensional (2D) structures, whereas lack of appropriate techniques has not allowed us to visualize depth structures of orientation coding. In the present study, we performed functional optical coherence tomography (fOCT), a technique capable of acquiring a 3D map of the intrinsic signals, to study the topology of orientation coding inside the cat visual cortex. With this technique, for the first time, we visualized columnar assemblies in orientation coding that had been predicted from electrophysiological recordings. In addition, we found that the columnar structures were largely distorted around pinwheel centers: center singularities were not rigid straight lines running perpendicularly to the cortical surface but formed twisted string-like structures inside the cortex that turned and extended horizontally through the cortex. Looping singularities were observed with their respective termini accessing the same cortical surface via clockwise and counterclockwise orientation pinwheels. These results suggest that a 3D topology of orientation coding cannot be fully anticipated from 2D surface measurements. Moreover, the findings demonstrate the utility of fOCT as an in vivo mesoscale imaging method for mapping functional response properties of cortex in the depth axis. NEW & NOTEWORTHY We used functional optical coherence tomography (fOCT) to visualize three-dimensional structure of the orientation columns with millimeter range and micrometer spatial resolution. We validated vertically elongated columnar structure in iso-orientation domains. The columnar structure was distorted around pinwheel centers. An orientation singularity formed a string with tortuous trajectories inside the cortex and connected clockwise and counterclockwise pinwheel centers in the surface orientation map. The results were confirmed by comparisons with conventional optical imaging and electrophysiological recordings.

KW - functional architecture

KW - functional imaging

KW - optical coherence tomography

KW - optical imaging

KW - orientation column

KW - visual cortex

UR - http://www.scopus.com/inward/record.url?scp=85061975548&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85061975548&partnerID=8YFLogxK

U2 - 10.1152/jn.00921.2017

DO - 10.1152/jn.00921.2017

M3 - Article

VL - 119

SP - 1562

EP - 1575

JO - Journal of Neurophysiology

JF - Journal of Neurophysiology

SN - 0022-3077

IS - 4

ER -