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Multisensory information facilitates reaction speed by enlarging activity difference between superior colliculus hemispheres in rats.

ABSTRACT: Animals can make faster behavioral responses to multisensory stimuli than to unisensory stimuli. The superior colliculus (SC), which receives multiple inputs from different sensory modalities, is considered to be involved in the initiation of motor responses. However, the mechanism by which multisensory information facilitates motor responses is not yet understood. Here, we demonstrate that multisensory information modulates competition among SC neurons to elicit faster responses. We conducted multiunit recordings from the SC of rats performing a two-alternative spatial discrimination task using auditory and/or visual stimuli. We found that a large population of SC neurons showed direction-selective activity before the onset of movement in response to the stimuli irrespective of stimulation modality. Trial-by-trial correlation analysis showed that the premovement activity of many SC neurons increased with faster reaction speed for the contraversive movement, whereas the premovement activity of another population of neurons decreased with faster reaction speed for the ipsiversive movement. When visual and auditory stimuli were presented simultaneously, the premovement activity of a population of neurons for the contraversive movement was enhanced, whereas the premovement activity of another population of neurons for the ipsiversive movement was depressed. Unilateral inactivation of SC using muscimol prolonged reaction times of contraversive movements, but it shortened those of ipsiversive movements. These findings suggest that the difference in activity between the SC hemispheres regulates the reaction speed of motor responses, and multisensory information enlarges the activity difference resulting in faster responses.

SUBMITTER: Hirokawa J

PROVIDER: S-EPMC3180293 | biostudies-literature | 2011

REPOSITORIES: biostudies-literature

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Multisensory information facilitates reaction speed by enlarging activity difference between superior colliculus hemispheres in rats.

Hirokawa Junya J Sadakane Osamu O Sakata Shuzo S Bosch Miquel M Sakurai Yoshio Y Yamamori Tetsuo T

PloS one 20110926 9

Animals can make faster behavioral responses to multisensory stimuli than to unisensory stimuli. The superior colliculus (SC), which receives multiple inputs from different sensory modalities, is considered to be involved in the initiation of motor responses. However, the mechanism by which multisensory information facilitates motor responses is not yet understood. Here, we demonstrate that multisensory information modulates competition among SC neurons to elicit faster responses. We conducted m ...[more]

PMID: 21966481

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Project description:Although vision is the dominating sensory system in sports, many situations require multisensory integration. Faster processing of auditory information in the brain may facilitate time-critical abilities such as reaction speed however previous research was limited by generic auditory and visual stimuli that did not consider audio-visual characteristics in ecologically valid environments. This study investigated the reaction speed in response to sport-specific monosensory (visual and auditory) and multisensory (audio-visual) stimulation. Neurophysiological analyses identified the neural processes contributing to differences in reaction speed. Nineteen elite badminton players participated in this study. In a first recording phase, the sound profile and shuttle speed of smash and drop strokes were identified on a badminton court using high-speed video cameras and binaural recordings. The speed and sound characteristics were transferred into auditory and visual stimuli and presented in a lab-based experiment, where participants reacted in response to sport-specific monosensory or multisensory stimulation. Auditory signal presentation was delayed by 26 ms to account for realistic audio-visual signal interaction on the court. N1 and N2 event-related potentials as indicators of auditory and visual information perception/processing, respectively were identified using a 64-channel EEG. Despite the 26 ms delay, auditory reactions were significantly faster than visual reactions (236.6 ms vs. 287.7 ms, p < 0.001) but still slower when compared to multisensory stimulation (224.4 ms, p = 0.002). Across conditions response times to smashes were faster when compared to drops (233.2 ms, 265.9 ms, p < 0.001). Faster reactions were paralleled by a lower latency and higher amplitude of the auditory N1 and visual N2 potentials. The results emphasize the potential of auditory information to accelerate the reaction time in sport-specific multisensory situations. This highlights auditory processes as a promising target for training interventions in racquet sports.

Project description:The superior colliculus (SC) and pulvinar are thought to function as a subcortical visual pathway that bypasses the striate cortex and detects fundamental facial information. We previously investigated neuronal responses in the SC and pulvinar of monkeys during a delayed nonmatching-to-sample task, in which the monkeys were required to discriminate among 35 facial photos of five models and other categories of visual stimuli, and reported that population coding by multiple SC and pulvinar neurons well discriminated facial photos from other categories of stimuli (Nguyen et al., 2013, 2014). However, it remains unknown whether population coding could represent multiple types of facial information including facial identity, gender, facial orientation, and gaze direction. In the present study, to investigate population coding of multiple types of facial information by the SC and pulvinar neurons, we reanalyzed the same neuronal responses in the SC and pulvinar; the responses of 112 neurons in the SC and 68 neurons in the pulvinar in serial 50-ms epochs after stimulus onset were reanalyzed with multidimensional scaling (MDS). The results indicated that population coding by neurons in both the SC and pulvinar classified some aspects of facial information, such as face orientation, gender, and identity, of the facial photos in the second epoch (50-100 ms after stimulus onset). The Euclidean distances between all the pairs of stimuli in the MDS spaces in the SC were significantly correlated with those in the pulvinar, which suggested that the SC and pulvinar function as a unit. However, in contrast with the known population coding of face neurons in the temporal cortex, the facial information coding in the SC and pulvinar was coarse and insufficient. In these subcortical areas, identity discrimination was face orientation-dependent and the left and right profiles were not discriminated. Furthermore, gaze direction information was not extracted in the SC and pulvinar. These results suggest that the SC and pulvinar, which comprise the subcortical visual pathway, send coarse and rapid information on faces to the cortical system in a bottom-up process.

Project description:BACKGROUND:Impaired naming is a ubiquitous symptom in all types of aphasia, which often adversely impacts independence, quality of life, and recovery of affected individuals. Previous research has demonstrated that naming can be facilitated by phonological and semantic cueing strategies that are largely incorporated into the treatment of anomic disturbances. Beneficial effects of cueing, whereby naming becomes faster and more accurate, are often attributed to the priming mechanisms occurring within the distributed language network. OBJECTIVE:We proposed and explored two novel cueing techniques: (1) Silent Visuomotor Cues (SVC), which provided articulatory information of target words presented in the form of silent videos, and (2) Semantic Auditory Cues (SAC), which consisted of acoustic information semantically relevant to target words (ringing for "telephone"). Grounded in neurophysiological evidence, we hypothesized that both SVC and SAC might aid communicative effectiveness possibly by triggering activity in perceptual and semantic language regions, respectively. METHODS:Ten participants with chronic non-fluent aphasia were recruited for a longitudinal clinical intervention. Participants were split into dyads (i.e., five pairs of two participants) and required to engage in a turn-based peer-to-peer language game using the Rehabilitation Gaming System for aphasia (RGSa). The objective of the RGSa sessions was to practice communicative acts, such as making a request. We administered SVCs and SACs in a pseudorandomized manner at the moment when the active player selected the object to be requested from the interlocutor. For the analysis, we compared the times from selection to the reception of the desired object between cued and non-cued trials. RESULTS:Naming accuracy, as measured by a standard clinical scale, significantly improved for all stimuli at each evaluation point, including the follow-up. Moreover, the results yielded beneficial effects of both SVC and SAC cues on word naming, especially at the early intervention sessions when the exposure to the target lexicon was infrequent. CONCLUSIONS:This study supports the efficacy of the proposed cueing strategies which could be integrated into the clinic or mobile technology to aid naming even at the chronic stages of aphasia. These findings are consistent with sensorimotor accounts of language processing, suggesting a coupling between language, motor, and semantic brain regions. TRIAL REGISTRATION:NCT02928822 . Registered 30 May 2016.

Dataset Information

Multisensory information facilitates reaction speed by enlarging activity difference between superior colliculus hemispheres in rats.

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Multisensory information facilitates reaction speed by enlarging activity difference between superior colliculus hemispheres in rats.

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