scholarly journals Neonatal Cortical Ablation Disrupts Multisensory Development in Superior Colliculus

2006 ◽  
Vol 95 (3) ◽  
pp. 1380-1396 ◽  
Author(s):  
Wan Jiang ◽  
Huai Jiang ◽  
Barry E. Stein
Keyword(s):  
Superior Colliculus ◽  
Normal Development ◽  
Receptive Fields ◽  
Early Ontogeny ◽  
Neonatal Brain ◽  
Anterior Ectosylvian Sulcus ◽  
Cortical Ablation ◽  
Cat Superior Colliculus ◽  
Multisensory Processes ◽  
Normal Adults

The ability of cat superior colliculus (SC) neurons to synthesize information from different senses depends on influences from two areas of the cortex: the anterior ectosylvian sulcus (AES) and the rostral lateral suprasylvian sulcus (rLS). Reversibly deactivating the inputs to the SC from either of these areas in normal adults severely compromises this ability and the SC-mediated behaviors that depend on it. In this study, we found that removal of these areas in neonatal animals precluded the normal development of multisensory SC processes. At maturity there was a substantial decrease in the incidence of multisensory neurons, and those multisensory neurons that did develop were highly abnormal. Their cross-modal receptive field register was severely compromised, as was their ability to integrate cross-modal stimuli. Apparently, despite the impressive plasticity of the neonatal brain, it cannot compensate for the early loss of these cortices. Surprisingly, however, neonatal removal of either AES or rLS had comparatively minor consequences on these properties. At maturity multisensory SC neurons were quite common: they developed the characteristic spatial register among their unisensory receptive fields and exhibited normal adult-like multisensory integration. These observations suggest that during early ontogeny, when the multisensory properties of SC neurons are being crafted, AES and rLS may have the ability to compensate for the loss of one another's cortico-collicular influences so that normal multisensory processes can develop in the SC.

Ultrastructure of developing visual cortical synapses in the cat superior colliculus

1991 ◽  
Vol 49 ◽  
pp. 156-157
Author(s):  
Caroline A. Miller ◽  
Laura L. Bruce
Keyword(s):  
Superior Colliculus ◽  
Phosphate Buffer ◽  
Receptive Fields ◽  
Visual Cortical Area ◽  
Cortical Synapses ◽  
Visual Cortical ◽  
And Function ◽  
Phosphate Buffered Saline ◽  
The Brain ◽  
Cat Superior Colliculus

The first visual cortical axons arrive in the cat superior colliculus by the time of birth. Adultlike receptive fields develop slowly over several weeks following birth. The developing cortical axons go through a sequence of changes before acquiring their adultlike morphology and function. To determine how these axons interact with neurons in the colliculus, cortico-collicular axons were labeled with biocytin (an anterograde neuronal tracer) and studied with electron microscopy.Deeply anesthetized animals received 200-500 nl injections of biocytin (Sigma; 5% in phosphate buffer) in the lateral suprasylvian visual cortical area. After a 24 hr survival time, the animals were deeply anesthetized and perfused with 0.9% phosphate buffered saline followed by fixation with a solution of 1.25% glutaraldehyde and 1.0% paraformaldehyde in 0.1M phosphate buffer. The brain was sectioned transversely on a vibratome at 50 μm. The tissue was processed immediately to visualize the biocytin.

Mechanisms of Within- and Cross-Modality Suppression in the Superior Colliculus

1997 ◽  
Vol 78 (6) ◽  
pp. 2834-2847 ◽  
Author(s):  
Daniel C. Kadunce ◽  
J. William Vaughan ◽  
Mark T. Wallace ◽  
Gyorgy Benedek ◽  
Barry E. Stein
Keyword(s):  
Superior Colliculus ◽  
Visual Stimulus ◽  
Receptive Fields ◽  
Specific Interest ◽  
Input Channel ◽  
Modality Effects ◽  
Excitatory Stimulus ◽  
Modality Specificity ◽  
Cat Superior Colliculus ◽  
Close Temporal Proximity

Kadunce, Daniel C., J. William Vaughan, Mark T. Wallace, Gyorgy Benedek, and Barry E. Stein. Mechanisms of within- and cross-modality suppression in the superior colliculus. J. Neurophysiol. 78: 2834–2847, 1997. The present studies were initiated to explore the basis for the response suppression that occurs in cat superior colliculus (SC) neurons when two spatially disparate stimuli are presented simultaneously or in close temporal proximity to one another. Of specific interest was examining the possibility that suppressive regions border the receptive fields (RFs) of unimodal and multisensory SC neurons and, when activated, degrade the neuron's responses to excitatory stimuli. Both within- and cross-modality effects were examined. An example of the former is when a response to a visual stimulus within its RF is suppressed by a second visual stimulus outside the RF. An example of the latter is when the response to a visual stimulus within the visual RF is suppressed when a stimulus from a different modality (e.g., auditory) is presented outside its (i.e., auditory) RF. Suppressive regions were found bordering visual, auditory, and somatosensory RFs. Despite significant modality-specific differences in the incidence and effectiveness of these regions, they were generally quite potent regardless of the modality. In the vast majority (85%) of cases, responses to the excitatory stimulus were degraded by ≥50% by simultaneously stimulating the suppressive region. Contrary to expectations and previous speculations, the effects of activating these suppressive regions often were quite specific. Thus powerful within-modality suppression could be demonstrated in many multisensory neurons in which cross-modality suppression could not be generated. However, the converse was not true. If an extra-RF stimulus inhibited center responses to stimuli of a different modality, it also would suppress center responses to stimuli of its own modality. Thus when cross-modality suppression was demonstrated, it was always accompanied by within-modality suppression. These observations suggest that separate mechanisms underlie within- and cross-modality suppression in the SC. Because some modality-specific tectopetal structures contain neurons with suppressive regions bordering their RFs, the within-modality suppression observed in the SC simply may reflect interactions taking place at the level of one input channel. However, the presence of modality-specific suppression at the level of one input channel would have no effect on the excitation initiated via another input channel. Given the modality-specificity of tectopetal inputs, it appears that cross-modality interactions require the convergence of two or more modality-specific inputs onto the same SC neuron and that the expression of these interactions depends on the internal circuitry of the SC. This allows a cross-modality suppressive signal to be nonspecific and to degrade any and all of the neuron's excitatory inputs.

Multisensory Orientation Behavior Is Disrupted by Neonatal Cortical Ablation

2007 ◽  
Vol 97 (1) ◽  
pp. 557-562 ◽  
Author(s):  
Wan Jiang ◽  
Huai Jiang ◽  
Benjamin A. Rowland ◽  
Barry E. Stein
Keyword(s):  
Auditory Information ◽  
Orientation Behavior ◽  
Neonatal Brain ◽  
Compensatory Mechanisms ◽  
Anterior Ectosylvian Sulcus ◽  
Auditory Cues ◽  
Cortical Ablation ◽  
Multisensory Enhancement ◽  
Response Amplification ◽  
Sensory Responses

The integration of visual and auditory information can significantly amplify the sensory responses of superior colliculus (SC) neurons and the behaviors that depend on them. This response amplification depends on the development of SC inputs that are derived from two regions of cortex: the anterior ectosylvian sulcus (AES) and the rostral lateral suprasylvian sulcus (rLS). Neonatal ablation of these cortico-collicular areas has been shown to disrupt the development of the multisensory enhancement capabilities of SC neurons and the present results demonstrate that it also precludes the development of the normal multisensory enhancements in orientation behavior. Animals with neonatal ablation of AES and rLS were tested at maturity and found unable to benefit from the combination of visual and auditory cues in their efforts to localize targets in contralesional space. In contrast, their ipsilesional multisensory orientation capabilities were indistinguishable from those of normal animals. However, when only one of these cortical areas was removed during early life, later behavioral consequences were negligible. Whether similar compensatory processes would occur in adult animals remains to be determined. These observations, coupled with those from previous studies, also suggest that a surprisingly high proportion of SC neurons capable of multisensory integration must be present for orientation behavior benefits to be realized. Compensatory mechanisms can achieve this if early lesions spare either AES or rLS, but even the impressive plasticity of the neonatal brain cannot compensate for the early loss of both of them.

Effects of cooling somatosensory cortex on response properties of tactile cells in the superior colliculus

1986 ◽  
Vol 55 (6) ◽  
pp. 1352-1368 ◽  
Author(s):  
H. R. Clemo ◽  
B. E. Stein
Keyword(s):  
Receptive Field ◽  
Superior Colliculus ◽  
Somatosensory Cortex ◽  
Critical Role ◽  
Receptive Fields ◽  
Field Size ◽  
Specific Cell ◽  
Anterior Ectosylvian Sulcus ◽  
Cortical Cooling ◽  
Cortical Regions

The corticotectal influences of somatosensory cortex were investigated by using reversible deactivation of cortex by cooling. More than half of the somatosensory superior colliculus (SC) cells studied exhibited a response depression (often not apparent qualitatively) or an elimination of responses to somatosensory stimuli during the period in which cortex was rendered inactive. Responses were restored to their initial levels by cortical rewarming. Hyperresponsiveness was never observed as a consequence of cortical cooling. Susceptibility to cooling-induced depression was not invariably linked to a specific cell type, location in the SC, or receptive-field size. Yet cells that had small receptive fields and were activated by hair displacement had the highest probability of being affected by this procedure. In some cells a contraction of the receptive field was induced by cortical cooling. This observation is consistent with previous experiments that showed that SC somatosensory receptive fields are constructed by the convergence of ascending and descending inputs and indicates that the responsiveness of specific receptive-field regions may depend on the functional integrity of cortex. Two cortical regions were found to produce cooling-induced effects in somatosensory SC cells: 1) SIV (and para-SIV), located in the anterior ectosylvian sulcus, and 2) the cortex within the rostral suprasylvian sulcus. These results indicate that somatosensory cortex, like visual cortex, plays a critical role in modulating the responses of SC cells. Apparently, the ability of both somatosensory and visual SC cells to code the presence of peripheral stimuli depends largely on the functional influences of their respective cortices. However, in contrast to previous observations on visual corticotectal influences, no specific receptive-field properties could be shown to be impressed on SC cells by somatosensory cortex.

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