 |
||||
|
||||
|
||||
|
||||
|
||||
Previous Article | Next Article
Volume 17, Number 7, Issue of April 1, 1997 pp. 2429-2444
Copyright ©1997 Society for NeuroscienceDevelopment of Multisensory Neurons and Multisensory Integration in Cat Superior Colliculus
Received Oct. 17, 1996; revised Jan. 9, 1997; accepted Jan. 15, 1997.
Mark T. Wallace and Barry E. Stein Department of Neurobiology and Anatomy, Bowman Gray School of Medicine of Wake Forest University, Winston-Salem, North Carolina 27157
The development of multisensory neurons and multisensory integration was examined in the deep layers of the superior colliculus of kittens ranging in age from 3 to 135 d postnatal (dpn). Despite the high proportion of multisensory neurons in adult animals, no such neurons were found during the first 10 d of postnatal life. Rather, all sensory-responsive neurons were unimodal. The first multisensory neurons (somatosensory-auditory) were found at 12 dpn, and visually responsive multisensory neurons were not found until 20 dpn. Early multisensory neurons responded weakly to sensory stimuli, had long latencies, large receptive fields, and poorly developed response selectivities. Most surprising, however, was their inability to integrate combinations of sensory cues to produce significant response enhancement (or depression), a characteristic feature of the adult. Responses to combinations of sensory cues differed little from responses to their modality-specific components.
At 28 dpn an abrupt physiological change was noted. Some multisensory neurons now integrated combinations of cross-modality cues and exhibited significant response enhancements when these cues were spatially coincident and response depressions when the cues were spatially disparate. During the next 2 months the incidence of multisensory neurons, and the proportion of these neurons capable of adult-like multisensory integration, gradually increased. Once multisensory integration appeared in a given neuron, its properties changed little with development. Even the youngest integrating neurons showed superadditive enhancements and spatial characteristics of multisensory integration that were indistinguishable from the adult. Nevertheless, neonatal and adult multisensory neurons differed in the manner in which they integrated temporally asynchronous stimuli, a distribution that may reflect the very different behavioral requirements at different ages. The possible maturational role of corticotectal projections in the abrupt gating of multisensory integration is discussed.
Key words: visual; auditory; somatosensory; development; neonate; cross-modality
This article has been cited by other articles:
V. Fuentes-Santamaria, J. C. Alvarado, J. G. McHaffie, and B. E. Stein
Axon Morphologies and Convergence Patterns of Projections from Different Sensory-Specific Cortices of the Anterior Ectosylvian Sulcus onto Multisensory Neurons in the Cat Superior Colliculus
Cereb Cortex, April 9, 2009; (2009) bhp060v1.
[Abstract] [Full Text] [PDF]
R. A. A. Campbell, A. J. King, F. R. Nodal, J. W. H. Schnupp, S. Carlile, and T. P. Doubell
Virtual Adult Ears Reveal the Roles of Acoustical Factors and Experience in Auditory Space Map Development
J. Neurosci., November 5, 2008; 28(45): 11557 - 11570.
[Abstract] [Full Text] [PDF]
V. Fuentes-Santamaria, J. C. Alvarado, B. E. Stein, and J. G. McHaffie
Cortex Contacts both Output Neurons and Nitrergic Interneurons in the Superior Colliculus: Direct and Indirect Routes for Multisensory Integration
Cereb Cortex, July 1, 2008; 18(7): 1640 - 1652.
[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]
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]
B. N. Carriere, D. W. Royal, T. J. Perrault, S. P. Morrison, J. W. Vaughan, B. E. Stein, and M. T. Wallace
Visual Deprivation Alters the Development of Cortical Multisensory Integration
J Neurophysiol, November 1, 2007; 98(5): 2858 - 2867.
[Abstract] [Full Text] [PDF]
T. Noesselt, J. W. Rieger, M. A. Schoenfeld, M. Kanowski, H. Hinrichs, H.-J. Heinze, and J. Driver
Audiovisual Temporal Correspondence Modulates Human Multisensory Superior Temporal Sulcus Plus Primary Sensory Cortices
J. Neurosci., October 17, 2007; 27(42): 11431 - 11441.
[Abstract] [Full Text] [PDF]
D. Talsma, T. J. Doty, and M. G. Woldorff
Selective Attention and Audiovisual Integration: Is Attending to Both Modalities a Prerequisite for Early Integration?
Cereb Cortex, March 1, 2007; 17(3): 679 - 690.
[Abstract] [Full Text] [PDF]
M. T. Wallace and B. E. Stein
Early Experience Determines How the Senses Will Interact
J Neurophysiol, January 1, 2007; 97(1): 921 - 926.
[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]
M. T. Wallace, B. N. Carriere, T. J. Perrault Jr, J. W. Vaughan, and B. E. Stein
The Development of Cortical Multisensory Integration.
J. Neurosci., November 15, 2006; 26(46): 11844 - 11849.
[Abstract] [Full Text] [PDF]
D. J. Lewkowicz and A. A. Ghazanfar
From the Cover: The decline of cross-species intersensory perception in human infants
PNAS, April 25, 2006; 103(17): 6771 - 6774.
[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]
A. H. Bell, M. A. Meredith, A. J. Van Opstal, and D. P. Munoz
Crossmodal Integration in the Primate Superior Colliculus Underlying the Preparation and Initiation of Saccadic Eye Movements
J Neurophysiol, June 1, 2005; 93(6): 3659 - 3673.
[Abstract] [Full Text] [PDF]
I. Skaliora, T. P. Doubell, N. P. Holmes, F. R. Nodal, and A. J. King
Functional Topography of Converging Visual and Auditory Inputs to Neurons in the Rat Superior Colliculus
J Neurophysiol, November 1, 2004; 92(5): 2933 - 2946.
[Abstract] [Full Text] [PDF]
M. T. Wallace, T. J. Perrault Jr, W. D. Hairston, and B. E. Stein
Visual Experience Is Necessary for the Development of Multisensory Integration
J. Neurosci., October 27, 2004; 24(43): 9580 - 9584.
[Abstract] [Full Text] [PDF]
M. T. Wallace, R. Ramachandran, and B. E. Stein
A revised view of sensory cortical parcellation
PNAS, February 17, 2004; 101(7): 2167 - 2172.
[Abstract] [Full Text] [PDF]
W. Jiang and B. E. Stein
Cortex Controls Multisensory Depression in Superior Colliculus
J Neurophysiol, October 1, 2003; 90(4): 2123 - 2135.
[Abstract] [Full Text] [PDF]
T. J. Anastasio and P. E. Patton
A Two-Stage Unsupervised Learning Algorithm Reproduces Multisensory Enhancement in a Neural Network Model of the Corticotectal System
J. Neurosci., July 30, 2003; 23(17): 6713 - 6727.
[Abstract] [Full Text] [PDF]
T. P. Doubell, I. Skaliora, J. Baron, and A. J. King
Functional Connectivity between the Superficial and Deeper Layers of the Superior Colliculus: An Anatomical Substrate for Sensorimotor Integration
J. Neurosci., July 23, 2003; 23(16): 6596 - 6607.
[Abstract] [Full Text] [PDF]
B. E. Stein, M. W. Wallace, T. R. Stanford, and W. Jiang
Book Review: Cortex Governs Multisensory Integration in the Midbrain
Neuroscientist, August 1, 2002; 8(4): 306 - 314.
[Abstract] [PDF]
M. T. Wallace and B. E. Stein
Sensory and Multisensory Responses in the Newborn Monkey Superior Colliculus
J. Neurosci., November 15, 2001; 21(22): 8886 - 8894.
[Abstract] [Full Text] [PDF]
W. Jiang, M. T. Wallace, H. Jiang, J. W. Vaughan, and B. E. Stein
Two Cortical Areas Mediate Multisensory Integration in Superior Colliculus Neurons
J Neurophysiol, February 1, 2001; 85(2): 506 - 522.
[Abstract] [Full Text] [PDF]
M. T. Wallace and B. E. Stein
Onset of Cross-Modal Synthesis in the Neonatal Superior Colliculus is Gated by the Development of Cortical Influences
J Neurophysiol, June 1, 2000; 83(6): 3578 - 3582.
[Abstract] [Full Text] [PDF]
T. J. Prescott, P. Redgrave, and K. Gurney
Layered Control Architectures in Robots and Vertebrates
Adaptive Behavior, January 1, 1999; 7(1): 99 - 127.
[Abstract] [PDF]
A. J. King, J. W. H. Schnupp, and I. D. Thompson
Signals from the Superficial Layers of the Superior Colliculus Enable the Development of the Auditory Space Map in the Deeper Layers
J. Neurosci., November 15, 1998; 18(22): 9394 - 9408.
[Abstract] [Full Text] [PDF]
M. T. Wallace, M. A. Meredith, and B. E. Stein
Multisensory Integration in the Superior Colliculus of the Alert Cat
J Neurophysiol, August 1, 1998; 80(2): 1006 - 1010.
[Abstract] [Full Text] [PDF]
|
|
|
|
 |
|