Biomedical subjects

Barry E Stein

Publications and source records attributed to Barry E Stein.

16 recordsLinked to original sources

PubMed2005

Neonatal cortical ablation disrupts multisensory development in superior colliculus.

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.

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PubMed2005

Evaluating the operations underlying multisensory integration in the cat superior colliculus.

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.

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PubMed2005

On the use of superadditivity as a metric for characterizing multisensory integration in functional neuroimaging studies.

A growing number of brain imaging studies are being undertaken in order to better understand the contributions of multisensory processes to human behavior and perception. Many of these studies are designed on the basis of the physiological findings from single neurons in animal models, which have shown that multisensory neurons have the capacity for integrating their different sensory inputs and give rise to a product that differs significantly from either of the unisensory responses. At certain points these multisensory interactions can be superadditive, resulting in a neural response that exceeds the sum of the unisensory responses. Because of the difficulties inherent in interpreting the results of imaging large neuronal populations, superadditivity has been put forth as a stringent criterion for identifying potential sites of multisensory integration. In the present manuscript we discuss issues related to using the superadditive model in human brain imaging studies, focusing on population responses to multisensory stimuli and the relationship between single neuron measures and functional brain imaging measures. We suggest that the results of brain imaging studies be interpreted with caution in regards to multisensory integration. Future directions for imaging multisensory integration are discussed in light of the ideas presented.

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PubMed2005

The development of a dialogue between cortex and midbrain to integrate multisensory information.

The anterior ectosylvian (AES) and rostral lateral suprasylvian (rLS) sulci send critical signals to multisensory superior colliculus (SC) neurons that enable them to integrate information from different senses. When either of these areas is temporarily deactivated in adult animals, the ability of SC neurons to integrate multisensory information and, thereby, enhance their responses to cross-modal stimuli is temporarily compromised. As a consequence, the ability to use cross-modal stimuli to enhance SC-mediated behavioral performance is also compromised. In contrast, removal of either one of these areas during early life has little effect on the development of multisensory processes in the SC or on SC-mediated multisensory behaviors and these animals seem very similar to normal controls. These observations suggest that there is considerable plasticity in these cortico-collicular systems during early life, with each area able to compensate for the early loss of the other. However, when both AES and rLS are removed early in life, there appears to be no compensation. The SC neurons now deal with sensory stimuli, even those embedded in multisensory complexes, as if they were there alone, precluding any SC-mediated behavioral benefit to cross-modal stimuli.

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PubMed2005

Superior colliculus neurons use distinct operational modes in the integration of multisensory stimuli.

Many neurons in the superior colliculus (SC) integrate sensory information from multiple modalities, giving rise to significant response enhancements. Although enhanced multisensory responses have been shown to depend on the spatial and temporal relationships of the stimuli as well as on their relative effectiveness, these factors alone do not appear sufficient to account for the substantial heterogeneity in the magnitude of the multisensory products that have been observed. Toward this end, the present experiments have revealed that there are substantial differences in the operations used by different multisensory SC neurons to integrate their cross-modal inputs, suggesting that intrinsic differences in these neurons may also play an important deterministic role in multisensory integration. In addition, the integrative operation employed by a given neuron was found to be well correlated with the neuron's dynamic range. In total, four categories of SC neurons were identified based on how their multisensory responses changed relative to the predicted addition of the two unisensory inputs as stimulus effectiveness was altered. Despite the presence of these categories, a general rule was that the most robust multisensory enhancements were seen with combinations of the least effective unisensory stimuli. Together, these results provide a better quantitative picture of the integrative operations performed by multisensory SC neurons and suggest mechanistic differences in the way in which these neurons synthesize cross-modal information.

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PubMed2005

Subcortical loops through the basal ganglia.

Parallel, largely segregated, closed-loop projections are an important component of cortical-basal ganglia-cortical connectional architecture. Here, we present the hypothesis that such loops involving the neocortex are neither novel nor the first evolutionary example of closed-loop architecture involving the basal ganglia. Specifically, we propose that a phylogenetically older, closed-loop series of subcortical connections exists between the basal ganglia and brainstem sensorimotor structures, a good example of which is the midbrain superior colliculus. Insofar as this organization represents a general feature of brain architecture, cortical and subcortical inputs to the basal ganglia might act independently, co-operatively or competitively to influence the mechanisms of action selection.

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PubMed2004

Visual experience is necessary for the development of multisensory integration.

Multisensory neurons and their ability to integrate multisensory cues develop gradually in the midbrain [i.e., superior colliculus (SC)]. To examine the possibility that early sensory experiences might play a critical role in these maturational processes, animals were raised in the absence of visual cues. As adults, the SC of these animals were found to contain many multisensory neurons, the large majority of which were visually responsive. Although these neurons responded robustly to each of their cross-modal inputs when presented individually, they were incapable of synthesizing this information. These observations suggest that visual experiences are critical for the SC to develop the ability to integrate multisensory information and lead to the prediction that, in the absence of such experience, animals will be compromised in their sensitivity to cross-modal events.

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PubMed2004

A revised view of sensory cortical parcellation.

Traditional cortical parcellation schemes have emphasized the presence of sharply defined visual, auditory, and somatosensory domains populated exclusively by modality-specific neurons (i.e., neurons responsive to sensory stimuli from a single sensory modality). However, the modality-exclusivity of this scheme has recently been challenged. Observations in a variety of species suggest that each of these domains is subject to influences from other senses. Using the cerebral cortex of the rat as a model, the present study systematically examined the capability of individual neurons in visual, auditory, and somatosensory cortex to be activated by stimuli from other senses. Within the major modality-specific domains, the incidence of inappropriate (i.e., nonmatching) and/or multisensory neurons was very low. However, at the borders between each of these domains a concentration of multisensory neurons was found whose modality profile matched the representations in neighboring cortices and that were able to integrate their cross-modal inputs to give rise to enhanced and/or depressed responses. The results of these studies are consistent with some features of both the traditional and challenging views of cortical organization, and they suggest a parcellation scheme in which modality-specific cortical domains are separated from one another by transitional multisensory zones.

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PubMed2003

Neuron-specific response characteristics predict the magnitude of multisensory integration.

Multisensory neurons in the superior colliculus (SC) typically respond to combinations of stimuli from multiple modalities with enhancements and/or depressions in their activity. Although such changes in response have been shown to follow a predictive set of integrative principles, these principles fail to completely account for the full range of interactions seen throughout the SC population. In an effort to better define this variability, we sought to determine if there were additional features of the neuronal response profile that were predictive of the magnitude of the multisensory interaction. To do this, we recorded from 109 visual-auditory SC neurons while systematically manipulating stimulus intensity. Along with the previously described roles of space, time, and stimulus effectiveness, two features of a neuron's response profile were found to offer predictive value as to the magnitude of the multisensory interaction: spontaneous activity and the level of sensory responsiveness. Multisensory neurons with little or no spontaneous activity and weak sensory responses had the capacity to exhibit large response enhancements. Conversely, neurons with modest spontaneous activity and robust sensory responses exhibited relatively small response enhancements. Together, these results provide a better view into multisensory integration, and suggest substantial heterogeneity in the integrative characteristics of the multisensory SC population.

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PubMed2003

Opposing basal ganglia processes shape midbrain visuomotor activity bilaterally.

The manner in which the nervous system allocates limited motor resources when confronted with conflicting behavioural demands is a crucial issue in understanding how sensory information is transformed into adaptive motor responses. Understanding this selection process is of particular concern in current models of functions of the basal ganglia. Here we report that the basal ganglia use simultaneous enhancing and suppressing processes synergistically to modulate sensory activity in the superior colliculi, which are bilaterally paired midbrain structures involved in the control of visual orientation behaviours. These complementary processes presumably ensure accurate gaze shifts mediated by the superior colliculi despite the presence of potential distractors.

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PubMed2003

Cross-modal sensory processing in the anterior cingulate and medial prefrontal cortices.

One of the principal functions of the nervous system is to synthesize information from multiple sensory channels into a coherent behavioral and perceptual gestalt. A critical feature of this multisensory synthesis is the sorting and coupling of information derived from the same event. One of the singular features of stimuli conveying such information is their contextual or semantic congruence. Illustrating this fact, subjects are typically faster and more accurate when performing tasks that include congruent compared to incongruent cross-modal stimuli. Using functional magnetic resonance imaging, we demonstrate that activity in select brain areas is sensitive to the contextual congruence among cross-modal cues and to task difficulty. The anterior cingulate gyrus and adjacent medial prefrontal cortices showed significantly greater activity when visual and auditory stimuli were contextually congruent (i.e., matching) than when they were nonmatching. Although activity in these regions was also dependent on task difficulty, showing decreased activity with decreasing task difficulty, the activity changes associated with stimulus congruence predominated.

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PubMed2003

An irrelevant light enhances auditory detection in humans: a psychophysical analysis of multisensory integration in stimulus detection.

Physiological and behavioral studies in animal models have revealed that information from the different senses can be used synergistically to enhance the detection of objects and events. Although a great deal of evidence exists which demonstrates the synergistic use of multisensory cues in human behavior and perception, there is conflicting evidence about whether such interactions can be used to aid in stimulus detection. To examine this issue, we had volunteers indicate the presence or absence of a brief, low-intensity sound that was either presented alone or paired with a simultaneous light in a one-interval signal detection task. In the first experiment, the task-irrelevant light was found to enhance the detectability of the sound, but also to increase the subject's willingness to report the presence of a sound (i.e., response bias). In the second experiment, designed to eliminate this response bias, we found an improvement in stimulus detectability in the absence of any change in bias. These findings demonstrate the presence of a significant multisensory-mediated gain in stimulus detection in human subjects.

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PubMed2003

Cortex controls multisensory depression in superior colliculus.

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.

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PubMed2002

Two corticotectal areas facilitate multisensory orientation behavior.

It had previously been shown that influences from two cortical areas, the anterior ectosylvian sulcus (AES) and the rostral lateral suprasylvian sulcus (rLS), play critical roles in rendering superior colliculus (SC) neurons capable of synthesizing their cross-modal inputs. The present studies examined the consequences of selectively eliminating these cortical influences on SC-mediated orientation responses to cross-modal stimuli. Cats were trained to orient to a low-intensity modality-specific cue (visual) in the presence or absence of a neutral cue from another modality (auditory). The visual target could appear at various locations within 45 degrees of the midline, and the stimulus effectiveness was varied to yield an average of correct orientation responses of approximately 45%. Response enhancement and depression were observed when the auditory cue was coupled with the target stimulus: A substantially enhanced probability in correct responses was evident when the cross-modal stimuli were spatially coincident, and a substantially decreased response probability was obtained when the stimuli were spatially disparate. Cryogenic blockade of either AES or rLS disrupted these behavioral effects, thereby eliminating the enhanced performance in response to spatially coincident cross-modal cues and degrading the depressed performance in response to spatially disparate cross-modal cues. These disruptive effects on targets contralateral to the deactivated cortex were restricted to multisensory interactive processes. Orientation to modality-specific targets was unchanged. Furthermore, the pattern of orientation errors was unaffected by cortical deactivation. These data bear striking similarities to the effects of AES and rLS deactivation on multisensory integration at the level of individual SC neurons. Presumably, eliminating the critical influences from AES or rLS cortex disrupts SC multisensory synthesis that, in turn, disables SC-mediated multisensory orientation behaviors.

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PubMed2002

Deactivation of sensory-specific cortex by cross-modal stimuli.

Visual and auditory cortices traditionally have been considered to be "modality-specific." Thus, their activity has been thought to be unchanged by information in other sensory modalities. However, using functional magnetic resonance imaging (fMRI), the present experiments revealed that ongoing activity in the visual cortex could be modulated by auditory information and ongoing activity in the auditory cortex could be modulated by visual information. In both cases, this cross-modal modulation of activity took the form of deactivation. Yet, the deactivation response was not evident in either cortical area during the paired presentation of visual and auditory stimuli. These data suggest that cross-modal inhibitory processes operate within traditional modality-specific cortices and that these processes can be switched on or off in different circumstances.

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PubMed2002

Cortex governs multisensory integration in the midbrain.

Neurons in the superior colliculus (SC), a prominent midbrain structure, are able to synthesize information from different senses. This synthesis plays an important role in determining whether SC-mediated orientation behaviors will be initiated. In some circumstances, multisensory integration in the SC is evident as a response that is significantly enhanced above that evoked by the most effective single-modality stimulus. It can sometimes even exceed the arithmetic sum of the single-modality responses. In other circumstances, multisensory integration is evident as response depression, an effect sometimes powerful enough to eliminate even robust single-modality responses. The conditions that produce multisensory enhancement also increase the probability of orientation responses, and those that produce multisensory response depression decrease the probability of orientation responses. Although one might posit that the capability to integrate cross-modal cues (and, in this case, alter overt behavior) would be evident in all neurons capable of responding to stimuli from two or more sensory modalities, this turns out to be incorrect. When descending influences from the cortex are temporarily inactivated, SC neurons are rendered unable to synthesize their multiple sensory inputs, and animals no longer show enhanced orientation responses. Nevertheless, the ability to respond to cues from multiple sensory modalities is retained at both the single neuron and behavioral levels. Two cortical areas have been implicated in controlling these midbrain processes: the anterior ectosylvian sulcus and the rostral lateral suprasylvian sulcus.

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