Onset of Cross-Modal Synthesis in the Neonatal Superior Colliculus is Gated by the Development of Cortical Influences

2000 ◽  
Vol 83 (6) ◽  
pp. 3578-3582 ◽  
Author(s):  
M. T. Wallace ◽  
B. E. Stein

Many neurons in the superior colliculus (SC) are able to integrate combinations of visual, auditory, and somatosensory stimuli, thereby markedly affecting the vigor of their responses to external stimuli. However, this capacity for multisensory integration is not inborn. Rather, it appears comparatively late in postnatal development and is not expressed until the SC passes through several distinct developmental stages. As shown here, the final stage in this sequence is one in which a region of association cortex establishes functional control over the SC, thus enabling the multisensory integrative capabilities of its target SC neurons. The first example of this corticotectal input was seen at postnatal day 28. For any individual SC neuron, the onset of corticotectal influences appeared to be abrupt. Because this event occurred at very different times for different SC neurons, a period of 3–4 postnatal months was required before the adult-like condition was achieved. The protracted postnatal period required for the maturation of these corticotectal influences corresponded closely with estimates of the peak period of cortical plasticity, raising the possibility that the genesis of these corticotectal influences, and hence the onset of SC multisensory integration, occurs only after the cortex is capable of exerting experience-dependent control over SC neurons.

1994 ◽  
Vol 71 (1) ◽  
pp. 429-432 ◽  
Author(s):  
M. T. Wallace ◽  
B. E. Stein

1. The synthesis of information from different sensory modalities in the superior colliculus is an important precursor of attentive and orientation behavior. 2. This integration of multisensory information is critically dependent on inputs from a small area of association cortex, the anterior ectosylvian sulcus. Removal of these corticotectal influences can have a remarkably specific effect: it can eliminate multisensory integration in superior colliculus neurons while leaving their responses to unimodal cues intact. 3. Apparently, some of the associative functions of cortex are accomplished via its target neurons in the midbrain.


1998 ◽  
Vol 80 (2) ◽  
pp. 1006-1010 ◽  
Author(s):  
Mark T. Wallace ◽  
M. Alex Meredith ◽  
Barry E. Stein

Wallace, Mark T., M. Alex Meredith, and Barry E. Stein. Multisensory integration in the superior colliculus of the alert cat. J. Neurophysiol. 80: 1006–1010, 1998. The modality convergence patterns, sensory response properties, and principles governing multisensory integration in the superior colliculus (SC) of the alert cat were found to have fundamental similarities to those in anesthetized animals. Of particular interest was the observation that, in a manner indistinguishable from the anesthetized animal, combinations of two different sensory stimuli significantly enhanced the responses of SC neurons above those evoked by either unimodal stimulus. These observations are consistent with the speculation that there is a functional link among multisensory integration in individual SC neurons and cross-modality attentive and orientation behaviors.


2002 ◽  
Vol 88 (1) ◽  
pp. 540-543 ◽  
Author(s):  
John J. Foxe ◽  
Glenn R. Wylie ◽  
Antigona Martinez ◽  
Charles E. Schroeder ◽  
Daniel C. Javitt ◽  
...  

Using high-field (3 Tesla) functional magnetic resonance imaging (fMRI), we demonstrate that auditory and somatosensory inputs converge in a subregion of human auditory cortex along the superior temporal gyrus. Further, simultaneous stimulation in both sensory modalities resulted in activity exceeding that predicted by summing the responses to the unisensory inputs, thereby showing multisensory integration in this convergence region. Recently, intracranial recordings in macaque monkeys have shown similar auditory-somatosensory convergence in a subregion of auditory cortex directly caudomedial to primary auditory cortex (area CM). The multisensory region identified in the present investigation may be the human homologue of CM. Our finding of auditory-somatosensory convergence in early auditory cortices contributes to mounting evidence for multisensory integration early in the cortical processing hierarchy, in brain regions that were previously assumed to be unisensory.


2007 ◽  
Vol 97 (1) ◽  
pp. 921-926 ◽  
Author(s):  
Mark T. Wallace ◽  
Barry E. Stein

Multisensory integration refers to the process by which the brain synthesizes information from different senses to enhance sensitivity to external events. In the present experiments, animals were reared in an altered sensory environment in which visual and auditory stimuli were temporally coupled but originated from different locations. Neurons in the superior colliculus developed a seemingly anomalous form of multisensory integration in which spatially disparate visual-auditory stimuli were integrated in the same way that neurons in normally reared animals integrated visual-auditory stimuli from the same location. The data suggest that the principles governing multisensory integration are highly plastic and that there is no a priori spatial relationship between stimuli from different senses that is required for their integration. Rather, these principles appear to be established early in life based on the specific features of an animal's environment to best adapt it to deal with that environment later in life.


1997 ◽  
Vol 20 (4) ◽  
pp. 629-631 ◽  
Author(s):  
Nestor A. Schmajuk

Shors & Matzel propose that hippocampal LTP increases the effective salience of discrete external stimuli and thereby facilitates the induction of memories at distant places. In line with this suggestion, a neural network model of associative learning and hippocampal function assumes that LTP increases hippocampal error signals to the cortex, thereby facilitating stimulus configuration in association cortex. Computer simulations show that under these assumptions the model correctly describes the effect of LTP induction and blockade in classical discriminations and place learning.


2003 ◽  
Vol 90 (4) ◽  
pp. 2123-2135 ◽  
Author(s):  
Wan Jiang ◽  
Barry E. Stein

Multisensory depression is a fundamental index of multisensory integration in superior colliculus (SC) neurons. It is initiated when one sensory stimulus (auditory) located outside its modality-specific receptive field degrades or eliminates the neuron's responses to another sensory stimulus (visual) presented within its modality-specific receptive field. The present experiments demonstrate that the capacity of SC neurons to engage in multisensory depression is strongly dependent on influences from two cortical areas (the anterior ectosylvian and rostral lateral suprasylvian sulci). When these cortices are deactivated, the ability of SC neurons to synthesize visual-auditory inputs in this way is compromised; multisensory responses are disinhibited, becoming more vigorous and in some cases indistinguishable from responses to the visual stimulus alone. Although obtaining a more robust multisensory SC response when cortex is nonfunctional than when it is functional may seem paradoxical, these data may help explain previous observations that the loss of these cortical influences permits visual orientation behavior in the presence of a normally disruptive auditory stimulus.


2012 ◽  
Vol 108 (11) ◽  
pp. 3073-3086 ◽  
Author(s):  
Arjun K. Bansal ◽  
Jedediah M. Singer ◽  
William S. Anderson ◽  
Alexandra Golby ◽  
Joseph R. Madsen ◽  
...  

The cerebral cortex needs to maintain information for long time periods while at the same time being capable of learning and adapting to changes. The degree of stability of physiological signals in the human brain in response to external stimuli over temporal scales spanning hours to days remains unclear. Here, we quantitatively assessed the stability across sessions of visually selective intracranial field potentials (IFPs) elicited by brief flashes of visual stimuli presented to 27 subjects. The interval between sessions ranged from hours to multiple days. We considered electrodes that showed robust visual selectivity to different shapes; these electrodes were typically located in the inferior occipital gyrus, the inferior temporal cortex, and the fusiform gyrus. We found that IFP responses showed a strong degree of stability across sessions. This stability was evident in averaged responses as well as single-trial decoding analyses, at the image exemplar level as well as at the category level, across different parts of visual cortex, and for three different visual recognition tasks. These results establish a quantitative evaluation of the degree of stationarity of visually selective IFP responses within and across sessions and provide a baseline for studies of cortical plasticity and for the development of brain-machine interfaces.


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