Literature DB >> 34013578

Multisensory enhancement of overt behavior requires multisensory experience.

Scott A Smyre1, Zhengyang Wang1, Barry E Stein1, Benjamin A Rowland1.   

Abstract

The superior colliculus (SC) is richly endowed with neurons that integrate cues from different senses to enhance their physiological responses and the overt behaviors they mediate. However, in the absence of experience with cross-modal combinations (e.g., visual-auditory), they fail to develop this characteristic multisensory capability: Their multisensory responses are no greater than their most effective unisensory responses. Presumably, this impairment in neural development would be reflected as corresponding impairments in SC-mediated behavioral capabilities such as detection and localization performance. Here, we tested that assumption directly in cats raised to adulthood in darkness. They, along with a normally reared cohort, were trained to approach brief visual or auditory stimuli. The animals were then tested with these stimuli individually and in combination under ambient light conditions consistent with their rearing conditions and home environment as well as under the opposite lighting condition. As expected, normally reared animals detected and localized the cross-modal combinations significantly better than their individual component stimuli. However, dark-reared animals showed significant defects in multisensory detection and localization performance. The results indicate that a physiological impairment in single multisensory SC neurons is predictive of an impairment in overt multisensory behaviors.
© 2021 Federation of European Neuroscience Societies and John Wiley & Sons Ltd.

Entities:  

Keywords:  cat; dark rearing; development; multisensory integration; vision

Mesh:

Year:  2021        PMID: 34013578      PMCID: PMC8295226          DOI: 10.1111/ejn.15315

Source DB:  PubMed          Journal:  Eur J Neurosci        ISSN: 0953-816X            Impact factor:   3.698


  63 in total

1.  Incorporating cross-modal statistics in the development and maintenance of multisensory integration.

Authors:  Jinghong Xu; Liping Yu; Benjamin A Rowland; Terrence R Stanford; Barry E Stein
Journal:  J Neurosci       Date:  2012-02-15       Impact factor: 6.167

2.  Multisensory processing in the redundant-target effect: a behavioral and event-related potential study.

Authors:  Matthias Gondan; Birgit Niederhaus; Frank Rösler; Brigitte Röder
Journal:  Percept Psychophys       Date:  2005-05

3.  Bayesian inference with probabilistic population codes.

Authors:  Wei Ji Ma; Jeffrey M Beck; Peter E Latham; Alexandre Pouget
Journal:  Nat Neurosci       Date:  2006-10-22       Impact factor: 24.884

4.  Interactions among converging sensory inputs in the superior colliculus.

Authors:  M A Meredith; B E Stein
Journal:  Science       Date:  1983-07-22       Impact factor: 47.728

5.  Initiating the development of multisensory integration by manipulating sensory experience.

Authors:  Liping Yu; Benjamin A Rowland; Barry E Stein
Journal:  J Neurosci       Date:  2010-04-07       Impact factor: 6.167

6.  Severe multisensory speech integration deficits in high-functioning school-aged children with Autism Spectrum Disorder (ASD) and their resolution during early adolescence.

Authors:  John J Foxe; Sophie Molholm; Victor A Del Bene; Hans-Peter Frey; Natalie N Russo; Daniella Blanco; Dave Saint-Amour; Lars A Ross
Journal:  Cereb Cortex       Date:  2013-08-28       Impact factor: 5.357

Review 7.  Challenges in quantifying multisensory integration: alternative criteria, models, and inverse effectiveness.

Authors:  Barry E Stein; Terrence R Stanford; Ramnarayan Ramachandran; Thomas J Perrault; Benjamin A Rowland
Journal:  Exp Brain Res       Date:  2009-06-24       Impact factor: 1.972

Review 8.  Measuring multisensory integration: from reaction times to spike counts.

Authors:  Hans Colonius; Adele Diederich
Journal:  Sci Rep       Date:  2017-06-08       Impact factor: 4.379

9.  Experience Creates the Multisensory Transform in the Superior Colliculus.

Authors:  Zhengyang Wang; Liping Yu; Jinghong Xu; Barry E Stein; Benjamin A Rowland
Journal:  Front Integr Neurosci       Date:  2020-04-21

10.  Audio-tactile integration in congenitally and late deaf cochlear implant users.

Authors:  Elena Nava; Davide Bottari; Agnes Villwock; Ineke Fengler; Andreas Büchner; Thomas Lenarz; Brigitte Röder
Journal:  PLoS One       Date:  2014-06-11       Impact factor: 3.240

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  3 in total

1.  Typical resting-state activity of the brain requires visual input during an early sensitive period.

Authors:  Katarzyna Rączy; Cordula Hölig; Maria J S Guerreiro; Sunitha Lingareddy; Ramesh Kekunnaya; Brigitte Röder
Journal:  Brain Commun       Date:  2022-06-07

2.  The influence of early audiovisual experience on multisensory integration and causal inference (commentary on Smyre et al., 2021).

Authors:  Uta Noppeney
Journal:  Eur J Neurosci       Date:  2021-12-29       Impact factor: 3.698

3.  Audiovisual spatial recalibration but not integration is shaped by early sensory experience.

Authors:  Patrick Bruns; Lux Li; Maria J S Guerreiro; Idris Shareef; Siddhart S Rajendran; Kabilan Pitchaimuthu; Ramesh Kekunnaya; Brigitte Röder
Journal:  iScience       Date:  2022-05-23
  3 in total

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