Literature DB >> 33852803

Compensating for a shifting world: evolving reference frames of visual and auditory signals across three multimodal brain areas.

Valeria C Caruso1,2,3,4,5, Daniel S Pages1,2,3,4, Marc A Sommer1,2,4,6, Jennifer M Groh1,2,3,4,6.   

Abstract

Stimulus locations are detected differently by different sensory systems, but ultimately they yield similar percepts and behavioral responses. How the brain transcends initial differences to compute similar codes is unclear. We quantitatively compared the reference frames of two sensory modalities, vision and audition, across three interconnected brain areas involved in generating saccades, namely the frontal eye fields (FEF), lateral and medial parietal cortex (M/LIP), and superior colliculus (SC). We recorded from single neurons in head-restrained monkeys performing auditory- and visually guided saccades from variable initial fixation locations and evaluated whether their receptive fields were better described as eye-centered, head-centered, or hybrid (i.e. not anchored uniquely to head- or eye-orientation). We found a progression of reference frames across areas and across time, with considerable hybrid-ness and persistent differences between modalities during most epochs/brain regions. For both modalities, the SC was more eye-centered than the FEF, which in turn was more eye-centered than the predominantly hybrid M/LIP. In all three areas and temporal epochs from stimulus onset to movement, visual signals were more eye-centered than auditory signals. In the SC and FEF, auditory signals became more eye-centered at the time of the saccade than they were initially after stimulus onset, but only in the SC at the time of the saccade did the auditory signals become "predominantly" eye-centered. The results indicate that visual and auditory signals both undergo transformations, ultimately reaching the same final reference frame but via different dynamics across brain regions and time.NEW & NOTEWORTHY Models for visual-auditory integration posit that visual signals are eye-centered throughout the brain, whereas auditory signals are converted from head-centered to eye-centered coordinates. We show instead that both modalities largely employ hybrid reference frames: neither fully head- nor eye-centered. Across three hubs of the oculomotor network (intraparietal cortex, frontal eye field, and superior colliculus) visual and auditory signals evolve from hybrid to a common eye-centered format via different dynamics across brain areas and time.

Entities:  

Keywords:  MIP); coordinate transformations; frontal eye field (FEF); intraparietal cortex (LIP; multisensory; superior colliculus (SC)

Mesh:

Year:  2021        PMID: 33852803      PMCID: PMC8325605          DOI: 10.1152/jn.00385.2020

Source DB:  PubMed          Journal:  J Neurophysiol        ISSN: 0022-3077            Impact factor:   2.974


  60 in total

1.  Reach plans in eye-centered coordinates.

Authors:  A P Batista; C A Buneo; L H Snyder; R A Andersen
Journal:  Science       Date:  1999-07-09       Impact factor: 47.728

2.  Idiosyncratic and systematic aspects of spatial representations in the macaque parietal cortex.

Authors:  Steve W C Chang; Lawrence H Snyder
Journal:  Proc Natl Acad Sci U S A       Date:  2010-04-07       Impact factor: 11.205

3.  Dynamic circuitry for updating spatial representations. I. Behavioral evidence for interhemispheric transfer in the split-brain macaque.

Authors:  Rebecca A Berman; Laura M Heiser; Richard C Saunders; Carol L Colby
Journal:  J Neurophysiol       Date:  2005-05-11       Impact factor: 2.714

4.  Saccade-related activity in the lateral intraparietal area. II. Spatial properties.

Authors:  S Barash; R M Bracewell; L Fogassi; J W Gnadt; R A Andersen
Journal:  J Neurophysiol       Date:  1991-09       Impact factor: 2.714

5.  Spatial invariance of visual receptive fields in parietal cortex neurons.

Authors:  J R Duhamel; F Bremmer; S Ben Hamed; W Graf
Journal:  Nature       Date:  1997-10-23       Impact factor: 49.962

6.  Influence of eye position on activity in monkey superior colliculus.

Authors:  A J Van Opstal; K Hepp; Y Suzuki; V Henn
Journal:  J Neurophysiol       Date:  1995-10       Impact factor: 2.714

7.  Neurons of area 7 activated by both visual stimuli and oculomotor behavior.

Authors:  R A Andersen; G K Essick; R M Siegel
Journal:  Exp Brain Res       Date:  1987       Impact factor: 1.972

8.  Eye movement control in primates. The oculomotor system contains specialized subsystems for acquiring and tracking visual targets.

Authors:  D A Robinson
Journal:  Science       Date:  1968-09-20       Impact factor: 47.728

Review 9.  Saccades and shifting receptive fields: anticipating consequences or selecting targets?

Authors:  Marc Zirnsak; Tirin Moore
Journal:  Trends Cogn Sci       Date:  2014-11-11       Impact factor: 20.229

10.  Spatiotopic coding of BOLD signal in human visual cortex depends on spatial attention.

Authors:  Sofia Crespi; Laura Biagi; Giovanni d'Avossa; David C Burr; Michela Tosetti; Maria Concetta Morrone
Journal:  PLoS One       Date:  2011-07-07       Impact factor: 3.240

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  1 in total

1.  Sound Localization of World and Head-Centered Space in Ferrets.

Authors:  Stephen M Town; Jennifer K Bizley
Journal:  J Neurosci       Date:  2022-05-02       Impact factor: 6.709

  1 in total

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