Cortical layer-specific differences in stimulus selectivity revealed with high-field fMRI and single-vessel resolution optical imaging of the primary visual cortex

Shinho Cho, Arani Roy, Chao J Liu, Djaudat Idiyatullin, Wei Zhu, Yi Zhang, Xiao-Hong Zhu, Phillip O'Herron, Austin Leikvoll, Wei Chen, Prakash Kara, Kâmil Uğurbil

Research output: Contribution to journalArticlepeer-review

Abstract

The mammalian neocortex exhibits a stereotypical laminar organization, with feedforward inputs arriving primarily into layer 4, local computations shaping response selectivity in layers 2/3, and outputs to other brain areas emanating via layers 2/3, 5 and 6. It cannot be assumed a priori that these signatures of laminar differences in neuronal circuitry are reflected in hemodynamic signals that form the basis of functional magnetic resonance imaging (fMRI). Indeed, optical imaging of single-vessel functional responses has highlighted the potential limits of using vascular signals as surrogates for mapping the selectivity of neural responses. Therefore, before fMRI can be employed as an effective tool for studying critical aspects of laminar processing, validation with single-vessel resolution is needed. The primary visual cortex (V1) in cats, with its precise neuronal functional micro-architecture, offers an ideal model system to examine laminar differences in stimulus selectivity across imaging modalities. Here we used cerebral blood volume weighted (wCBV) fMRI to examine if layer-specific orientation-selective responses could be detected in cat V1. We found orientation preference maps organized tangential to the cortical surface that typically extended across depth in a columnar fashion. We then examined arterial dilation and blood velocity responses to identical visual stimuli by using two- and three- photon optical imaging at single-vessel resolution—which provides a measure of the hemodynamic signals with the highest spatial resolution. Both fMRI and optical imaging revealed a consistent laminar response pattern in which orientation selectivity in cortical layer 4 was significantly lower compared to layer 2/3. This systematic change in selectivity across cortical layers has a clear underpinning in neural circuitry, particularly when comparing layer 4 to other cortical layers.

Original languageEnglish (US)
Article number118978
JournalNeuroImage
Volume251
DOIs
StatePublished - May 1 2022

Bibliographical note

Funding Information:
This work was supported by NIH R01 MH111447, R01 MH111413, R01 NS118330, P41 EB027061, U01NS115585 and P30 NS076408; NSF 1707287 and the WM KECK foundation.

Publisher Copyright:
© 2022

Keywords

  • Cerebral blood volume response
  • Functional magnetic resonance imaging
  • Layer-specific orientation selectivity
  • Multi-photon optical imaging
  • Primary visual cortex
  • Vessel dilation

PubMed: MeSH publication types

  • Journal Article
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

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