Literature DB >> 19458228

Multisensory integration in the superior colliculus requires synergy among corticocollicular inputs.

Juan Carlos Alvarado1, Terrence R Stanford, Benjamin A Rowland, J William Vaughan, Barry E Stein.   

Abstract

Influences from the visual (AEV), auditory (FAES), and somatosensory (SIV) divisions of the cat anterior ectosylvian sulcus (AES) play a critical role in rendering superior colliculus (SC) neurons capable of multisensory integration. However, it is not known whether this is accomplished via their independent sensory-specific action or via some cross-modal cooperative action that emerges as a consequence of their convergence on SC neurons. Using visual-auditory SC neurons as a model, we examined how selective and combined deactivation of FAES and AEV affected SC multisensory (visual-auditory) and unisensory (visual-visual) integration capabilities. As noted earlier, multisensory integration yielded SC responses that were significantly greater than those evoked by the most effective individual component stimulus. This multisensory "response enhancement" was more evident when the component stimuli were weakly effective. Conversely, unisensory integration was dominated by the lack of response enhancement. During cryogenic deactivation of FAES and/or AEV, the unisensory responses of SC neurons were only modestly affected; however, their multisensory response enhancement showed a significant downward shift and was eliminated. The shift was similar in magnitude for deactivation of either AES subregion and, in general, only marginally greater when both were deactivated simultaneously. These data reveal that SC multisensory integration is dependent on the cooperative action of distinct subsets of unisensory corticofugal afferents, afferents whose sensory combination matches the multisensory profile of their midbrain target neurons, and whose functional synergy is specific to rendering SC neurons capable of synthesizing information from those particular senses.

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Year:  2009        PMID: 19458228      PMCID: PMC2805025          DOI: 10.1523/JNEUROSCI.0525-09.2009

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


  59 in total

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Authors:  S Murray Sherman; R W Guillery
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2002-12-29       Impact factor: 6.237

2.  Modeling cross-modal enhancement and modality-specific suppression in multisensory neurons.

Authors:  Paul E Patton; Thomas J Anastasio
Journal:  Neural Comput       Date:  2003-04       Impact factor: 2.026

3.  Neuron-specific response characteristics predict the magnitude of multisensory integration.

Authors:  Thomas J Perrault; J William Vaughan; Barry E Stein; Mark T Wallace
Journal:  J Neurophysiol       Date:  2003-08-20       Impact factor: 2.714

Review 4.  Bayesian multisensory integration and cross-modal spatial links.

Authors:  Sophie Deneve; Alexandre Pouget
Journal:  J Physiol Paris       Date:  2004 Jan-Jun

5.  A chronic headholder minimizing facial obstructions.

Authors:  J G McHaffie; B E Stein
Journal:  Brain Res Bull       Date:  1983-06       Impact factor: 4.077

6.  Sources of subcortical projections to the superior colliculus in the cat.

Authors:  S B Edwards; C L Ginsburgh; C K Henkel; B E Stein
Journal:  J Comp Neurol       Date:  1979-03-15       Impact factor: 3.215

7.  Efferent projections of the neonatal superior colliculus: extraoculomotor-related brain stem structures.

Authors:  B E Stein; R F Spencer; S B Edwards
Journal:  Brain Res       Date:  1982-05-06       Impact factor: 3.252

8.  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

9.  Physiologic and anatomic investigation of a visual cortical area situated in the ventral bank of the anterior ectosylvian sulcus of the cat.

Authors:  L Mucke; M Norita; G Benedek; O Creutzfeldt
Journal:  Exp Brain Res       Date:  1982       Impact factor: 1.972

10.  Superior colliculus lesions preferentially disrupt multisensory orientation.

Authors:  L R Burnett; B E Stein; D Chaponis; M T Wallace
Journal:  Neuroscience       Date:  2004       Impact factor: 3.590

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  33 in total

1.  Alterations to multisensory and unisensory integration by stimulus competition.

Authors:  Scott R Pluta; Benjamin A Rowland; Terrence R Stanford; Barry E Stein
Journal:  J Neurophysiol       Date:  2011-09-28       Impact factor: 2.714

Review 2.  Dissecting neural circuits for multisensory integration and crossmodal processing.

Authors:  Jeffrey M Yau; Gregory C DeAngelis; Dora E Angelaki
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2015-09-19       Impact factor: 6.237

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.  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

6.  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

7.  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

8.  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

9.  An emergent model of multisensory integration in superior colliculus neurons.

Authors:  Cristiano Cuppini; Mauro Ursino; Elisa Magosso; Benjamin A Rowland; Barry E Stein
Journal:  Front Integr Neurosci       Date:  2010-03-22

10.  The non-lemniscal auditory cortex in ferrets: convergence of corticotectal inputs in the superior colliculus.

Authors:  Victoria M Bajo; Fernando R Nodal; Jennifer K Bizley; Andrew J King
Journal:  Front Neuroanat       Date:  2010-05-21       Impact factor: 3.856

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