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.     

Mechanisms of within- and cross-modality suppression in the superior colliculus

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.     

Neural mechanisms for synthesizing sensory information and producing adaptive behaviors

The ability to integrate information from different sensory systems is a fundamental characteristic of the brain. Because different bits of information are derived from different sensory channels, their synthesis markedly enhances the detection and identification of external stimuli. The neural substrate for such "multisensory" integration is provided by neurons that receive convergent input from two or more sensory modalities. Many such multisensory neurons are found in the superior colliculus (SC), a midbrain structure that plays a significant role in overt attentive and orientation behaviors. The various principles governing the integration of visual, auditory, and somatosensory inputs in SC neurons have been explored in several species. Thus far, the evidence suggests a remarkable conservation of integrative features during vertebrate evolution. One of the most robust of these principles is based on spatial relationships: a striking enhancement in activity is induced in a multisensory neuron when two different sensory stimuli (e.g., visual and auditory) are in spatial concordance, whereas a profound response depression can be induced when these cues are spatially discordant. The most extensive physiological observations have been made in cat, and in this species the same principles that have been shown to govern multisensory integration at the level of the individual SC neuron have also been shown to govern overt attentive and orientation responses to multisensory stimuli. Most surprising, however, is the critical role played by association (i.e. anterior ectosylvian) cortex in facilitating these midbrain processes. In the absence of the modulating corticotectal influences, multisensory SC neurons in cat are unable to integrate the different sensory cues converging upon them in an adult-like fashion, and are unable to mediate overt multisensory behaviors. This situation appears quite similar to that observed during early postnatal life. When multisensory SC neurons first appear, they are able to respond to multiple sensory inputs but are unable to synthesize these inputs to significantly enhance or degrade their responses. During ontogeny, individual multisensory neurons develop this capacity abruptly, but at very different ages, until the mature population condition is reached after several postnatal months. It appears likely that the abrupt onset of this capacity in any individual SC neuron reflects the maturation of inputs from anterior ectosylvian cortex. Presumably, the functional coupling of cortex with an individual SC neuron is essential to initiate and maintain that neuron's capability for multisensory integration throughout its life.     

Visual, somatosensory, auditory and nociceptive modality properties in the feline suprageniculate nucleus

Response properties of 252 single-units to visual, auditory, somatosensory and noxious stimulation were recorded by means of extracellular microelectrodes in the suprageniculate nucleus of anaesthetized, immobilized cats. Of the 141 units tested for modality properties the majority (n=113, 80.1%) was found unimodal in the sense that stimuli of exclusively one sensory modality were able to elicit an activation of the unit. Twenty-four (17.0%) cells were bimodal and four (2.8%) were trimodal (visual, somatosensory and auditory). The visual modality dominated the unimodal cells (n=74, 65.5%), while cells responsive to somatic stimulation (n=20, 17.6%), auditory stimulation (n=16, 14.1%) or noxious stimulation of the tooth pulp (n=3, 2.6%) were less frequently encountered. Visual sensitivity dominated the multisensory cells, too. The visually responsive units were characterized by having a sensitivity to stimuli moving in a rather large, uniform receptive field that covered the contralateral lower quadrant, and encompassed a flanking area of about 20 degree width in both the upper contralateral and lower ipsilateral visual fields. Many cells (n=52, 47%) were sensitive to the direction of the stimulation and reacted to stimuli moving at a high velocity (20-200 deg/s). Most cells responded differently to stimuli of a variety of sizes. Somatosensory units reacted to stimuli presented over a wide area on the contralateral side of the body, thus showing no sign of somatotopic organization. The auditory sensitivity fell within a wide range of acoustic stimuli in extremely large auditory receptive fields. The physiological properties of suprageniculate nucleus cells strongly resemble the sensory properties of cells found along the ventral bank of the anterior ectosylvian sulcus and the deeper layers of the superior colliculus. Our results provide further support for the notion of a separate tecto-suprageniculate-anterior ectosylvian sulcus/insular pathway that takes part in the processing of multimodal signals important for various types of sensory related behaviours.     

The role of motivation and orientation in sensory preconditioning.

Explored the effect of hunger on sensory preconditioning. Ss were 17 male cats. An appetitive task was used to test for sensory preconditioning effects in order to avoid complications arising from differences of drive state during preconditioning and testing for preconditioning. It was found that hunger facilitated the association between paired auditory and visual stimuli, but not between stimuli presented separately and in random order. Examination of the orientation responses of Ss during preconditioning indicate that the auditory stimulus becomes an arousing cue that signals the onset of the visual stimulus. It is suggested that the orientation responses produced as a consequence of this cue function are responsible for the association of the auditory and visual stimuli. (French summary) (19 ref.) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Multisensory prior entry.

Despite 2 centuries of research, the question of whether attending to a sensory modality speeds the perception of stimuli in that modality has yet to be resolved. The authors highlight weaknesses inherent in this previous research and report the results of 4 experiments in which a novel methodology was used to investigate the effects on temporal order judgments (TOJs) of attending to a particular sensory modality or spatial location. Participants were presented with pairs of visual and tactile stimuli from the left and/or right at varying stimulus onset asynchronies and were required to make unspeeded TOJs regarding which stimulus appeared first. The results provide the strongest evidence to date for the existence of multisensory prior entry and support previous claims for attentional biases toward the visual modality and toward the right side of space. These findings have important implications for studies in many areas of human and animal cognition. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Sensory dominance in infants: I. Six-month-old infants' response to auditory-visual compounds.

To investigate sensory dominance in early development, a series of studies was conducted to examine 6-month-old infants' processing of multisensory stimulus compounds. The infants were first habituated with a compound stimulus consisting of a flashing checkerboard and a pulsing sound. To assess attention to aspects of the compound stimulus, the infants received separate test trials where compounds differed in the rate and/or duration at which the visual, the auditory, or both components were presented. One consistent finding was that the infants discriminated changes in the temporal characteristics of the auditory component but not in the visual component. Their responsiveness to the auditory information depended on the number of discriminative cues available during either the habituation or the test phases and on the temporal distinctiveness of the auditory and visual components during the habituation phase. This consistent failure to respond to changes in the visual component led to the conclusion that auditory dominance was operating. This conclusion was reinforced by the finding that the infants failed to discriminate a change in the rate of the visual component even when the intensity of the visual component was increased relative to that of the auditory component, and by the finding that the infants could discriminate temporal changes in the visual component following habituation with just the visual component. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Sensory modality distribution in the anterior ectosylvian cortex (AEC) of cats

Modality specificity of neuronal responses to visual, somesthetic and auditory stimuli was investigated in the anterior ectosylvian cortex (AEC) of cats, using single-unit recording techniques. Seven classes of neurons were found, and according to their responsiveness to sensory stimuli regrouped into three categories: unimodal, bimodal and trimodal. Unimodal cells that responded to only one of the three stimulus modalities formed 59% of the units; 30.2% were bimodal, in that they showed a clear increase of neuronal discharges to two of the three stimulus types; 10.8% were defined as trimodal because they responded to all three stimulus modalities. Although the different categories of cells were intermingled within the AEC, indicating a certain degree of overlap between sensory modalities, some clustering of cell types was nonetheless evident. Thus, the somatosensory responsive cells were mainly located in the anterior two-thirds of the dorsal bank of the anterior ectosylvian sulcus. Visually responsive cells were concentrated on the ventral bank of the sulcus, whereas neurons with an auditory response occupied the banks and fundus of the posterior three-quarters of the sulcus. The histological distribution and physiological properties of AEC neurons suggest that this cortical region is a higher-order associative area whose function may be to integrate information from different sensory modalities.     

Development of multisensory neurons and multisensory integration in cat superior colliculus

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.     

Cross-modal equivalence in early infancy: Auditory–visual intensity matching.

To examine the hypothesis that young infants ignore differences between lights and sounds and instead respond to auditory and visual stimuli as more or less similar depending on their intensity, a cardiac habituation/dishabituation method with a test for stimulus generalization was employed. In 2 experiments, a total of 40 3-wk-old Ss were repeatedly presented with white-light followed by white-noise stimuli of different intensities. A U-shaped relationship between magnitude of cardiac response (CR) and loudness was found. In view of previous findings that without prior visual stimulation a monotonic increase in CR to the same range of auditory stimuli results, this finding of a significant quadratic relationship with loudness suggests that Ss were responding to the auditory stimuli in terms of their similarity to the previously presented visual stimulus. A separate group of 14 infants presented with a more intense visual stimulus exhibited a shift in the intensity at which a minimal CR occurred. Results of a study with 31 adults did not show any systematic relationship between CR and loudness, indicating that unlike infants, adults do not spontaneously make cross-modal matches of intensity. (28 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Superior colliculus and active navigation: role of visual and non-visual cues in controlling cellular representations of space

To begin investigation of the contribution of the superior colliculus to unrestrained navigation, the nature of behavioral representation by individual neurons was identified as rats performed a spatial memory task. Similar to what has been observed for hippocampus, many superior collicular cells showed elevated firing as animals traversed particular locations on the maze, and also during directional movement. However, when compared to hippocampal place fields, superior collicular location fields were found to be more broad and did not exhibit mnemonic properties. Organism-centered spatial coding was illustrated by other neurons that discharged preferentially during right or left turns made by the animal on the maze, or after lateralized sensory presentation of somatosensory, visual, or auditory stimuli. Nonspatial movement-related neurons increased or decreased firing when animals engaged in specific behaviors on the maze regardless of location or direction of movement. Manipulations of the visual environment showed that many, but not all, spatial cells were dependent on visual information. The majority of movement-related cells, however, did not require visual information to establish or maintain the correlates. Several superior collicular cells fired in response to multiple maze behaviors; in some of these cases a dissociation of visual sensitivity to one component of the behavioral correlate, but not the other, could be achieved for a single cell. This suggests that multiple modalities influence the activity of single neurons in superior colliculus of behaving rats. Similarly, several sensory-related cells showed dramatic increases in firing rate during the presentation of multisensory stimuli compared to the unimodal stimuli. These data reveal for the first time how previous findings of sensory/motor representation by the superior colliculus of restrained/anesthetized animals might be manifested in freely behaving rats performing a navigational task. Furthermore, the findings of both visually dependent and visually independent spatial coding suggest that superior colliculus may be involved in sending visual information for establishing spatial representations in efferent structures and for directing spatially-guided movements.     

Validity and boundary conditions of automatic response activation in the Simon task.

Three experiments were conducted to determine whether spatial stimulus-response compatibility effects are caused by automatic response activation by stimulus properties or by interference between codes during translation of stimulus into response coordinates. The main evidence against activation has been that in a Simon task with hands crossed, responses are faster at the response location ipsilateral to the stimulus though manipulated by the hand contralateral to the stimulus. The experiments were conducted with hands in standard and in crossed positions and electroencephalogram measures showed coactivation of the motor cortex induced by stimulus position primarily during standard hand positions with visual stimuli. Only in this condition did the Simon effect decay with longer response times. The visual Simon effect appeared to be due to specific mechanisms of visuomotor information transmission that are not responsible for the effects obtained with crossed hands or auditory stimuli. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Lexical Influences in Audiovisual Speech Perception.

Phoneme identification with audiovisually discrepant stimuli is influenced hy information in the visual signal (the McGurk effect). Additionally, lexical status affects identification of auditorily presented phonemes. The present study tested for lexical influences on the McGurk effect. Participants identified phonemes in audiovisually discrepant stimuli in which lexical status of the auditory component and of a visually influenced percept was independently varied. Visually influenced (McGurk) responses were more frequent when they formed a word and when the auditory signal was a nonword (Experiment 1). Lexical effects were larger for slow than for fast responses (Experiment 2), as with auditory speech, and were replicated with stimuli matched on physical properties (Experiment 3). These results are consistent with models in which lexical processing of speech is modality independent. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Attempts at saving severely ischaemic limbs

The relative efficacy of (1) repeated auditory and somesthetic stimulation for the habituation of cardiac acceleration responses and (2) intramodal and cross-modal stimulation for the dishabituation of cardiac responses was studied in 45 full-term 2-day-old infants. Although the stimuli were equally effective initially, repeated presentation of the somesthetic stimulus had a greater decremental effect than repeated presentation of the auditory stimulus. The stimuli were equally effective in producing dishabituation when in a different modality from that of the habituating stimulus (cross-modal) but not when in the same modality (intramodal). Changes in the locus of stimulation without a change in modality were ineffective for producing dishabituation. The findings indicate the human newborn discriminates auditory and somesthetic inputs effectively and equally but does not discriminate contralateral from ipsilateral stimulation in either modality.     

Transfer of noncorresponding spatial associations to the auditory Simon task.

Four experiments examined transfer of noncorresponding spatial stimulus-response associations to an auditory Simon task for which stimulus location was irrelevant. Experiment 1 established that, for a horizontal auditory Simon task, transfer of spatial associations occurs after 300 trials of practice with an incompatible mapping of auditory stimuli to keypress responses. Experiments 2-4 examined transfer effects within the auditory modality when the stimuli and responses were varied along vertical and horizontal dimensions. Transfer occurred when the stimuli and responses were arrayed along the same dimension in practice and transfer but not when they were arrayed along orthogonal dimensions. These findings indicate that prior task-defined associations have less influence on the auditory Simon effect than on the visual Simon effect, possibly because of the stronger tendency for an auditory stimulus to activate its corresponding response. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Activating response codes by stimuli in the neglected visual field.

The ability of 2 patients with a clinical deficit of extinction to process stimuli presented contralaterally to their lesions was tested with 2 variants of the flanker task. The patients saw 2 colored stimuli, 1 of which appeared in the center of the visual field and the other either on the ipsior contralateral side. In the peripheral report task, the patients had to report the color of the peripheral stimulus. In the center report task, the patients had to report the color of the central stimulus. The patients were much slower in the peripheral report task when the target was presented contralaterally to their lesion. By contrast, the responses in the center report task were equally influenced by ipsi- and contralateral flankers. The findings indicate that the patients were not impaired in the perceptual processing or the activation of response codes for contralateral stimuli. Their impairment is related to processes needed for generation of overt responses. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Signals from the superficial layers of the superior colliculus enable the development of the auditory space map in the deeper layers

We have examined whether the superficial layers of the superior colliculus (SC) provide the source of visual signals that guide the development of the auditory space map in the deeper layers. Anatomical tracing experiments with fluorescent microspheres revealed that a retinotopic map is present in the newborn ferret SC. Aspiration of the caudal region of the superficial layers of the right SC on postnatal day 0 did not cause a reorganization of this projection. Consequently, recordings made when the animals were mature showed that visual units in the remaining superficial layers in rostral SC had receptive fields that spanned a restricted region of anterior space. Auditory units recorded beneath the remaining superficial layers were tuned to corresponding anterior locations. Both the superficial layer visual map and the deeper layer auditory map were normal in the left, unoperated SC. The majority of auditory units recorded throughout the deeper layers ventral to the superficial layer lesion were also tuned to single sound directions. In this region of the SC, however, we observed much greater scatter in the distribution of preferred sound directions and a significant increase in the proportion of units with spatially ambiguous responses. The auditory representation was degraded, although many of these units were also visually responsive. Equivalent lesions of the superficial layers made in adult ferrets did not alter the topographic order in the auditory representation, suggesting that visual activity in these layers may be involved in aligning the different sensory maps in the developing SC.     

Analysis of neural interactions explains the activation of occipital cortex by an auditory stimulus

Analysis of neural interactions explains the activation of occipital cortex by an auditory stimulus. J. Neurophysiol. 80: 2790-2796, 1998. Large-scale neural interactions were characterized in human subjects as they learned that an auditory stimulus signaled a visual event. Once learned, activation of left dorsal occipital cortex (increased regional cerebral blood flow) was observed when the auditory stimulus was presented alone. Partial least-squares analysis of the interregional correlations (functional connectivity) between the occipital area and the rest of the brain identified a pattern of covariation with four dominant brain areas that could have mediated this activation: prefrontal cortex (near Brodmann area 10, A10), premotor cortex (A6), superior temporal cortex (A41/42), and contralateral occipital cortex (A18). Interactions among these regions and the occipital area were quantified with structural equation modeling to identify the strongest sources of the effect on left occipital activity (effective connectivity). Learning-related changes in feedback effects from A10 and A41/42 appeared to account for this change in occipital activity. Influences from these areas on the occipital area were initially suppressive, or negative, becoming facilitory, or positive, as the association between the auditory and visual stimuli was acquired. Evaluating the total effects within the functional models showed positive influences throughout the network, suggesting enhanced interactions may have primed the system for the now-expected visual discrimination. By characterizing both changes in activity and the interactions underlying sensory associative learning, we demonstrated how parts of the nervous system operate as a cohesive network in learning about and responding to the environment.     

Directed attention prolongs the perceived duration of a brief stimulus

Stelmach, Herdman, and McNeil (1994) suggested recently that the perceived duration for attended stimuli is shorter than that for unattended ones. In contrast, the attenuation hypothesis (Thomas & Weaver, 1975) suggests the reverse relation between directed attention and perceived duration. We conducted six experiments to test the validity of the two contradictory hypotheses. In all the experiments, attention was directed to one of two possible stimulus sources. Experiments 1 and 2 employed stimulus durations from 70 to 270 msec. A stimulus appeared in either the visual or the auditory modality. Stimuli in the attended modality were rated as longer than stimuli in the unattended modality. Experiment 3 replicated this finding using a different psychophysical procedure. Experiments 4-6 showed that the finding applies not only to stimuli from different sensory modalities but also to stimuli appearing at different locations within the visual field. The results of all six experiments support the assumption that directed attention prolongs the perceived duration of a stimulus.     

Crossmodal semantic priming by naturalistic sounds and spoken words enhances visual sensitivity.

We propose a multisensory framework based on Glaser and Glaser's (1989) general reading-naming interference model to account for the semantic priming effect by naturalistic sounds and spoken words on visual picture sensitivity. Four experiments were designed to investigate two key issues: First, can auditory stimuli enhance visual sensitivity when the sound leads the picture as well as when they are presented simultaneously? And, second, do naturalistic sounds (e.g., a dog's “woofing”) and spoken words (e.g., /d?g/) elicit similar semantic priming effects? Here, we estimated participants' sensitivity and response criterion using signal detection theory in a picture detection task. The results demonstrate that naturalistic sounds enhanced visual sensitivity when the onset of the sounds led that of the picture by 346 ms (but not when the sounds led the pictures by 173 ms, nor when they were presented simultaneously, Experiments 1-3A). At the same SOA, however, spoken words did not induce semantic priming effects on visual detection sensitivity (Experiments 3B and 4A). When using a dual picture detection/identification task, both kinds of auditory stimulus induced a similar semantic priming effect (Experiment 4B). Therefore, we suggest that there needs to be sufficient processing time for the auditory stimulus to access its associated meaning to modulate visual perception. Besides, the interactions between pictures and the two types of sounds depend not only on their processing route to access semantic representations, but also on the response to be made to fulfill the requirements of the task. (PsycINFO Database Record (c) 2011 APA, all rights reserved)