 |
The Journal of Neuroscience, July 13, 2005, 25(28):6499-6508; doi:10.1523/JNEUROSCI.5095-04.2005
Previous Article | Next Article 
Behavioral/Systems/Cognitive
Evaluating the Operations Underlying Multisensory Integration in the Cat Superior Colliculus
Terrence R. Stanford,1
Stephan Quessy,2 and
Barry E. Stein1
1Department of Neurobiology and Anatomy, Wake Forest University School of Medicine, Winston-Salem, North Carolina 27157, and 2Department of Neurobiology and Anatomy, University of Rochester, Rochester, New York 14642
It is well established that superior colliculus (SC) multisensory neurons integrate cues from different senses; however, the mechanisms responsible for producing multisensory responses are poorly understood. Previous studies have shown that spatially congruent cues from different modalities (e.g., auditory and visual) yield enhanced responses and that the greatest relative enhancements occur for combinations of the least effective modality-specific stimuli. Although these phenomena are well documented, little is known about the mechanisms that underlie them, because no study has systematically examined the operation that multisensory neurons perform on their modality-specific inputs. The goal of this study was to evaluate the computations that multisensory neurons perform in combining the influences of stimuli from two modalities. The extracellular activities of single neurons in the SC of the cat were recorded in response to visual, auditory, and bimodal visual-auditory stimulation. Each neuron was tested across a range of stimulus intensities and multisensory responses evaluated against the null hypothesis of simple summation of unisensory influences. We found that the multisensory response could be superadditive, additive, or subadditive but that the computation was strongly dictated by the efficacies of the modality-specific stimulus components. Superadditivity was most common within a restricted range of near-threshold stimulus efficacies, whereas for the majority of stimuli, response magnitudes were consistent with the linear summation of modality-specific influences. In addition to providing a constraint for developing models of multisensory integration, the relationship between response mode and stimulus efficacy emphasizes the importance of considering stimulus parameters when inducing or interpreting multisensory phenomena.
Key words: superior colliculus; multisensory integration; single-unit electrophysiology; audition; vision; cat
Received Dec 14, 2004;
revised May 29, 2005;
accepted May 29, 2005.
This article has been cited by other articles:

|
 |

|
 |
 
S. R. Pluta and M. Kawasaki
Multisensory enhancement of electromotor responses to a single moving object
J. Exp. Biol.,
September 15, 2008;
211(18):
2919 - 2930.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Kayser, C. I. Petkov, and N. K. Logothetis
Visual Modulation of Neurons in Auditory Cortex
Cereb Cortex,
July 1, 2008;
18(7):
1560 - 1574.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. N. Carriere, D. W. Royal, and M. T. Wallace
Spatial Heterogeneity of Cortical Receptive Fields and Its Impact on Multisensory Interactions
J Neurophysiol,
May 1, 2008;
99(5):
2357 - 2368.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Leo, N. Bolognini, C. Passamonti, B. E. Stein, and E. Ladavas
Cross-modal localization in hemianopia: new insights on multisensory integration
Brain,
March 1, 2008;
131(3):
855 - 865.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. C. Alvarado, T. R. Stanford, J. W. Vaughan, and B. E. Stein
Cortex Mediates Multisensory But Not Unisensory Integration in Superior Colliculus
J. Neurosci.,
November 21, 2007;
27(47):
12775 - 12786.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. F. Reynolds and B. L. Day
Fast visuomotor processing made faster by sound
J. Physiol.,
September 15, 2007;
583(3):
1107 - 1115.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. K. Bizley, F. R. Nodal, V. M. Bajo, I. Nelken, and A. J. King
Physiological and Anatomical Evidence for Multisensory Interactions in Auditory Cortex
Cereb Cortex,
September 1, 2007;
17(9):
2172 - 2189.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. A. Rowland, S. Quessy, T. R. Stanford, and B. E. Stein
Multisensory Integration Shortens Physiological Response Latencies
J. Neurosci.,
May 30, 2007;
27(22):
5879 - 5884.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. C. Alvarado, J. W. Vaughan, T. R. Stanford, and B. E. Stein
Multisensory Versus Unisensory Integration: Contrasting Modes in the Superior Colliculus
J Neurophysiol,
May 1, 2007;
97(5):
3193 - 3205.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. J. Friedlander
Mixing Modalities Is More Than Meets the Eye Alone. Focus on: "Multisensory Versus Unisensory Integration: Contrasting Modes in the Superior Colliculus"
J Neurophysiol,
May 1, 2007;
97(5):
3165 - 3165.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Rouger, S. Lagleyre, B. Fraysse, S. Deneve, O. Deguine, and P. Barone
From the Cover: Evidence that cochlear-implanted deaf patients are better multisensory integrators
PNAS,
April 24, 2007;
104(17):
7295 - 7300.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Avillac, S. Ben Hamed, and J.-R. Duhamel
Multisensory Integration in the Ventral Intraparietal Area of the Macaque Monkey
J. Neurosci.,
February 21, 2007;
27(8):
1922 - 1932.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. Jiang, H. Jiang, B. A. Rowland, and B. E. Stein
Multisensory Orientation Behavior Is Disrupted by Neonatal Cortical Ablation
J Neurophysiol,
January 1, 2007;
97(1):
557 - 562.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Sugihara, M. D. Diltz, B. B. Averbeck, and L. M. Romanski
Integration of Auditory and Visual Communication Information in the Primate Ventrolateral Prefrontal Cortex
J. Neurosci.,
October 25, 2006;
26(43):
11138 - 11147.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. A. Whitchurch and T. T. Takahashi
Combined Auditory and Visual Stimuli Facilitate Head Saccades in the Barn Owl (Tyto alba)
J Neurophysiol,
August 1, 2006;
96(2):
730 - 745.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Molholm, P. Sehatpour, A. D. Mehta, M. Shpaner, M. Gomez-Ramirez, S. Ortigue, J. P. Dyke, T. H. Schwartz, and J. J. Foxe
Audio-Visual Multisensory Integration in Superior Parietal Lobule Revealed by Human Intracranial Recordings
J Neurophysiol,
August 1, 2006;
96(2):
721 - 729.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. Jiang, H. Jiang, and B. E. Stein
Neonatal Cortical Ablation Disrupts Multisensory Development in Superior Colliculus
J Neurophysiol,
March 1, 2006;
95(3):
1380 - 1396.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|