Cross-modal synthesis in the midbrain depends on input from cortex

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.

1993 ◽  
Vol 69 (6) ◽  
pp. 1797-1809 ◽  
Author(s):  
M. T. Wallace ◽  
M. A. Meredith ◽  
B. E. Stein

1. Physiological methods were used to examine the pattern of inputs from different sensory cortices onto individual superior colliculus neurons. 2. Visual, auditory, and somatosensory influences from anterior ectosylvian sulcus (AES) and visual influences from lateral suprasylvian (LS) cortex were found to converge onto individual multisensory neurons in the cat superior colliculus. An excellent topographic relationship was found between the different sensory cortices and their target neurons in the superior colliculus. 3. Corticotectal inputs were derived solely from unimodal neurons. Multisensory neurons in AES and LS were not antidromically activated from the superior colliculus. 4. Orthodromic and antidromic latencies were consistent with monosynaptic corticotectal inputs arising from LS and the three subdivisions of AES (SIV, Field AES, and AEV). 5. Superior colliculus neurons that received convergent cortical inputs formed a principal component of the tecto-reticulospinal tract. Thus there appears to be extensive cortical control over the output neurons through which the superior colliculus mediates attentive and orientation behaviors. 6. Two other multisensory circuits were identified. A population of multisensory superior colliculus neurons was found, which neither received convergent cortical input nor projected into the tecto-reticulo-spinal tract. In addition, multisensory neurons in AES and LS proved to be independent of the superior colliculus (i.e., they were not corticotectal). While it is likely that these three distinct multisensory neural circuits have different functional roles, their constituent neurons appear to integrate their various sensory inputs in much the same way.


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.


2014 ◽  
Vol 26 (3) ◽  
pp. 1130-1137 ◽  
Author(s):  
Liping Yu ◽  
Jinghong Xu ◽  
Benjamin A. Rowland ◽  
Barry E. Stein

2001 ◽  
Vol 85 (2) ◽  
pp. 506-522 ◽  
Author(s):  
Wan Jiang ◽  
Mark T. Wallace ◽  
Huai Jiang ◽  
J. William Vaughan ◽  
Barry E. Stein

The majority of multisensory neurons in the cat superior colliculus (SC) are able to synthesize cross-modal cues (e.g., visual and auditory) and thereby produce responses greater than those elicited by the most effective single modality stimulus and, sometimes, greater than those predicted by the arithmetic sum of their modality-specific responses. The present study examined the role of corticotectal inputs from two cortical areas, the anterior ectosylvian sulcus (AES) and the rostral aspect of the lateral suprasylvian sulcus (rLS), in producing these response enhancements. This was accomplished by evaluating the multisensory properties of individual SC neurons during reversible deactivation of these cortices individually and in combination using cryogenic deactivation techniques. Cortical deactivation eliminated the characteristic multisensory response enhancement of nearly all SC neurons but generally had little or no effect on a neuron's modality-specific responses. Thus, the responses of SC neurons to combinations of cross-modal stimuli were now no different from those evoked by one or the other of these stimuli individually. Of the two cortical areas, AES had a much greater impact on SC multisensory integrative processes, with nearly half the SC neurons sampled dependent on it alone. In contrast, only a small number of SC neurons depended solely on rLS. However, most SC neurons exhibited dual dependencies, and their multisensory enhancement was mediated by either synergistic or redundant influences from AES and rLS. Corticotectal synergy was evident when deactivating either cortical area compromised the multisensory enhancement of an SC neuron, whereas corticotectal redundancy was evident when deactivation of both cortical areas was required to produce this effect. The results suggest that, although multisensory SC neurons can be created as a consequence of a variety of converging tectopetal afferents that are derived from a host of subcortical and cortical structures, the ability to synthesize cross-modal inputs, and thereby produce an enhanced multisensory response, requires functional inputs from the AES, the rLS, or both.


1983 ◽  
Vol 50 (4) ◽  
pp. 896-909 ◽  
Author(s):  
B. E. Stein ◽  
R. F. Spencer ◽  
S. B. Edwards

Substantial corticotectal (and corticothalamic) projections from the cortex of the anterior ectosylvian sulcus (AES) were demonstrated in the cat using the axonal transport methods of autoradiography and horseradish peroxidase. The corticotectal projection arises nearly exclusively from medium-large pyramidal cells in lamina V. One of the densest projecting areas of the AES is the rostral aspect of its superior bank, where a fourth somatotopic representation (SIV) has recently been demonstrated. It terminates in the intermediate and deep laminae of the superior colliculus, where somatic cells are located. The pathway is bilateral but much heavier ipsilaterally than contralaterally. In contrast to the substantial corticotectal projection from SIV and adjacent tissue, there was no unequivocal evidence for a corticotectal projection from traditional somatosensory cortex SI-SIII. This finding, that somatosensory projections to the cat superior colliculus arise from an area outside of SI-SIII, was unexpected on the basis of what is known about visual corticotectal projections. However, it is consistent with the patterns of other cortical projections that terminate in the intermediate and deep laminae of this structure and with the absence of demonstrable corticotectal influences from SI to SIII in this animal. These data are in contrast to demonstrations by other investigators that there is a corticotectal projection from SI cortex in rodents. Apparently there is a fundamental species difference in the organization of descending somatosensory pathways. A corticothalamic projection of the AES was also observed. This descending projection appeared to form a shell of labeled cells and fibers around the ventrobasal complex, but unequivocal terminal labeling within the ventrobasal complex could not be demonstrated. Dense terminal labeling was apparent in the posterior group of thalamic nuclei (PO) where thalamocortical afferents to the AES originate.


Sign in / Sign up

Export Citation Format

Share Document