Literature DB >> 20371810

Initiating the development of multisensory integration by manipulating sensory experience.

Liping Yu1, Benjamin A Rowland, Barry E Stein.   

Abstract

The multisensory integration capabilities of superior colliculus neurons emerge gradually during early postnatal life as a consequence of experience with cross-modal stimuli. Without such experience neurons become responsive to multiple sensory modalities but are unable to integrate their inputs. The present study demonstrates that neurons retain sensitivity to cross-modal experience well past the normal developmental period for acquiring multisensory integration capabilities. Experience surprisingly late in life was found to rapidly initiate the development of multisensory integration, even more rapidly than expected based on its normal developmental time course. Furthermore, the requisite experience was acquired by the anesthetized brain and in the absence of any of the stimulus-response contingencies generally associated with learning. The key experiential factor was repeated exposure to the relevant stimuli, and this required that the multiple receptive fields of a multisensory neuron encompassed the cross-modal exposure site. Simple exposure to the individual components of a cross-modal stimulus was ineffective in this regard. Furthermore, once a neuron acquired multisensory integration capabilities at the exposure site, it generalized this experience to other locations, albeit with lowered effectiveness. These observations suggest that the prolonged period during which multisensory integration normally appears is due to developmental factors in neural circuitry in addition to those required for incorporating the statistics of cross-modal events; that neurons learn a multisensory principle based on the specifics of experience and can then apply it to other stimulus conditions; and that the incorporation of this multisensory information does not depend on an alert brain.

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Year:  2010        PMID: 20371810      PMCID: PMC2858413          DOI: 10.1523/JNEUROSCI.5575-09.2010

Source DB:  PubMed          Journal:  J Neurosci        ISSN: 0270-6474            Impact factor:   6.167


  38 in total

1.  The influence of visual and auditory receptive field organization on multisensory integration in the superior colliculus.

Authors:  D C Kadunce; J W Vaughan; M T Wallace; B E Stein
Journal:  Exp Brain Res       Date:  2001-08       Impact factor: 1.972

2.  Evaluating the operations underlying multisensory integration in the cat superior colliculus.

Authors:  Terrence R Stanford; Stephan Quessy; Barry E Stein
Journal:  J Neurosci       Date:  2005-07-13       Impact factor: 6.167

3.  Multisensory versus unisensory integration: contrasting modes in the superior colliculus.

Authors:  Juan Carlos Alvarado; J William Vaughan; Terrence R Stanford; Barry E Stein
Journal:  J Neurophysiol       Date:  2007-02-28       Impact factor: 2.714

4.  Multisensory enhancement in the optic tectum of the barn owl: spike count and spike timing.

Authors:  Yael Zahar; Amit Reches; Yoram Gutfreund
Journal:  J Neurophysiol       Date:  2009-03-04       Impact factor: 2.714

5.  Redistribution of synaptic efficacy between neocortical pyramidal neurons.

Authors:  H Markram; M Tsodyks
Journal:  Nature       Date:  1996-08-29       Impact factor: 49.962

6.  The effects of early auditory deprivation on temporal perceptions: a comparison of hearing and hearing-impaired children on temporal pattern matching tasks.

Authors:  L J Anooshian; J M Bryan
Journal:  J Speech Hear Res       Date:  1979-12

7.  Early visual deprivation impairs multisensory interactions in humans.

Authors:  Lisa Putzar; Ines Goerendt; Kathrin Lange; Frank Rösler; Brigitte Röder
Journal:  Nat Neurosci       Date:  2007-09-16       Impact factor: 24.884

8.  Cortex mediates multisensory but not unisensory integration in superior colliculus.

Authors:  Juan Carlos Alvarado; Terrence R Stanford; J William Vaughan; Barry E Stein
Journal:  J Neurosci       Date:  2007-11-21       Impact factor: 6.167

Review 9.  The role of chondroitin sulfate proteoglycans in regeneration and plasticity in the central nervous system.

Authors:  Clare M Galtrey; James W Fawcett
Journal:  Brain Res Rev       Date:  2007-01-11

10.  Multisensory integration produces an initial response enhancement.

Authors:  Benjamin A Rowland; Barry E Stein
Journal:  Front Integr Neurosci       Date:  2007-11-30
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  46 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.  The development of audiovisual multisensory integration across childhood and early adolescence: a high-density electrical mapping study.

Authors:  Alice B Brandwein; John J Foxe; Natalie N Russo; Ted S Altschuler; Hilary Gomes; Sophie Molholm
Journal:  Cereb Cortex       Date:  2010-09-16       Impact factor: 5.357

Review 3.  Development of multisensory integration from the perspective of the individual neuron.

Authors:  Barry E Stein; Terrence R Stanford; Benjamin A Rowland
Journal:  Nat Rev Neurosci       Date:  2014-08       Impact factor: 34.870

Review 4.  Organization and plasticity in multisensory integration: early and late experience affects its governing principles.

Authors:  Barry E Stein; Benjamin A Rowland
Journal:  Prog Brain Res       Date:  2011       Impact factor: 2.453

5.  What does a neuron learn from multisensory experience?

Authors:  Jinghong Xu; Liping Yu; Terrence R Stanford; Benjamin A Rowland; Barry E Stein
Journal:  J Neurophysiol       Date:  2014-11-12       Impact factor: 2.714

6.  Multisensory Plasticity in Superior Colliculus Neurons is Mediated by Association Cortex.

Authors:  Liping Yu; Jinghong Xu; Benjamin A Rowland; Barry E Stein
Journal:  Cereb Cortex       Date:  2014-12-31       Impact factor: 5.357

7.  Relative unisensory strength and timing predict their multisensory product.

Authors:  Ryan L Miller; Scott R Pluta; Barry E Stein; Benjamin A Rowland
Journal:  J Neurosci       Date:  2015-04-01       Impact factor: 6.167

8.  Multisensory Integration Uses a Real-Time Unisensory-Multisensory Transform.

Authors:  Ryan L Miller; Barry E Stein; Benjamin A Rowland
Journal:  J Neurosci       Date:  2017-04-27       Impact factor: 6.167

9.  Cross-Modal Competition: The Default Computation for Multisensory Processing.

Authors:  Liping Yu; Cristiano Cuppini; Jinghong Xu; Benjamin A Rowland; Barry E Stein
Journal:  J Neurosci       Date:  2018-12-20       Impact factor: 6.167

10.  Development of cortical influences on superior colliculus multisensory neurons: effects of dark-rearing.

Authors:  Liping Yu; Jinghong Xu; Benjamin A Rowland; Barry E Stein
Journal:  Eur J Neurosci       Date:  2013-03-27       Impact factor: 3.386

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