Neuronal plasticity and multisensory integration in filial imprinting

Many organisms sample their environment through multiple sensory systems and the integration of multisensory information enhances learning. However, the mechanisms underlying multisensory memory formation and their similarity to unisensory mechanisms remain unclear. Filial imprinting is one example in which experience is multisensory, and the mechanisms of unisensory neuronal plasticity are well established. We investigated the storage of audiovisual information through experience by comparing the activity of neurons in the intermediate and medial mesopallium of imprinted and naïve domestic chicks (Gallus gallus domesticus) in response to an audiovisual imprinting stimulus and novel object and their auditory and visual components. We find that imprinting enhanced the mean response magnitude of neurons to unisensory but not multisensory stimuli. Furthermore, imprinting enhanced responses to incongruent audiovisual stimuli comprised of mismatched auditory and visual components. Our results suggest that the effects of imprinting on the unisensory and multisensory responsiveness of IMM neurons differ and that IMM neurons may function to detect unexpected deviations from the audiovisual imprinting stimulus.     

Effects of Auditory Stimuli in the Horizontal Plane on Audiovisual Integration: An Event-Related Potential Study

This article aims to investigate whether auditory stimuli in the horizontal plane, particularly originating from behind the participant, affect audiovisual integration by using behavioral and event-related potential (ERP) measurements. In this study, visual stimuli were presented directly in front of the participants, auditory stimuli were presented at one location in an equidistant horizontal plane at the front (0°, the fixation point), right (90°), back (180°), or left (270°) of the participants, and audiovisual stimuli that include both visual stimuli and auditory stimuli originating from one of the four locations were simultaneously presented. These stimuli were presented randomly with equal probability; during this time, participants were asked to attend to the visual stimulus and respond promptly only to visual target stimuli (a unimodal visual target stimulus and the visual target of the audiovisual stimulus). A significant facilitation of reaction times and hit rates was obtained following audiovisual stimulation, irrespective of whether the auditory stimuli were presented in the front or back of the participant. However, no significant interactions were found between visual stimuli and auditory stimuli from the right or left. Two main ERP components related to audiovisual integration were found: first, auditory stimuli from the front location produced an ERP reaction over the right temporal area and right occipital area at approximately 160–200 milliseconds; second, auditory stimuli from the back produced a reaction over the parietal and occipital areas at approximately 360–400 milliseconds. Our results confirmed that audiovisual integration was also elicited, even though auditory stimuli were presented behind the participant, but no integration occurred when auditory stimuli were presented in the right or left spaces, suggesting that the human brain might be particularly sensitive to information received from behind than both sides.     

An fMRI Study of Audiovisual Speech Perception Reveals Multisensory Interactions in Auditory Cortex

Research on the neural basis of speech-reading implicates a network of auditory language regions involving inferior frontal cortex, premotor cortex and sites along superior temporal cortex. In audiovisual speech studies, neural activity is consistently reported in posterior superior temporal Sulcus (pSTS) and this site has been implicated in multimodal integration. Traditionally, multisensory interactions are considered high-level processing that engages heteromodal association cortices (such as STS). Recent work, however, challenges this notion and suggests that multisensory interactions may occur in low-level unimodal sensory cortices. While previous audiovisual speech studies demonstrate that high-level multisensory interactions occur in pSTS, what remains unclear is how early in the processing hierarchy these multisensory interactions may occur. The goal of the present fMRI experiment is to investigate how visual speech can influence activity in auditory cortex above and beyond its response to auditory speech. In an audiovisual speech experiment, subjects were presented with auditory speech with and without congruent visual input. Holding the auditory stimulus constant across the experiment, we investigated how the addition of visual speech influences activity in auditory cortex. We demonstrate that congruent visual speech increases the activity in auditory cortex.     

Effects of Sound Frequency on Audiovisual Integration: An Event-Related Potential Study

A combination of signals across modalities can facilitate sensory perception. The audiovisual facilitative effect strongly depends on the features of the stimulus. Here, we investigated how sound frequency, which is one of basic features of an auditory signal, modulates audiovisual integration. In this study, the task of the participant was to respond to a visual target stimulus by pressing a key while ignoring auditory stimuli, comprising of tones of different frequencies (0.5, 1, 2.5 and 5 kHz). A significant facilitation of reaction times was obtained following audiovisual stimulation, irrespective of whether the task-irrelevant sounds were low or high frequency. Using event-related potential (ERP), audiovisual integration was found over the occipital area for 0.5 kHz auditory stimuli from 190–210 ms, for 1 kHz stimuli from 170–200 ms, for 2.5 kHz stimuli from 140–200 ms, 5 kHz stimuli from 100–200 ms. These findings suggest that a higher frequency sound signal paired with visual stimuli might be early processed or integrated despite the auditory stimuli being task-irrelevant information. Furthermore, audiovisual integration in late latency (300–340 ms) ERPs with fronto-central topography was found for auditory stimuli of lower frequencies (0.5, 1 and 2.5 kHz). Our results confirmed that audiovisual integration is affected by the frequency of an auditory stimulus. Taken together, the neurophysiological results provide unique insight into how the brain processes a multisensory visual signal and auditory stimuli of different frequencies.     

Reproducibility and discriminability of brain patterns of semantic categories enhanced by congruent audiovisual stimuli

One of the central questions in cognitive neuroscience is the precise neural representation, or brain pattern, associated with a semantic category. In this study, we explored the influence of audiovisual stimuli on the brain patterns of concepts or semantic categories through a functional magnetic resonance imaging (fMRI) experiment. We used a pattern search method to extract brain patterns corresponding to two semantic categories: "old people" and "young people." These brain patterns were elicited by semantically congruent audiovisual, semantically incongruent audiovisual, unimodal visual, and unimodal auditory stimuli belonging to the two semantic categories. We calculated the reproducibility index, which measures the similarity of the patterns within the same category. We also decoded the semantic categories from these brain patterns. The decoding accuracy reflects the discriminability of the brain patterns between two categories. The results showed that both the reproducibility index of brain patterns and the decoding accuracy were significantly higher for semantically congruent audiovisual stimuli than for unimodal visual and unimodal auditory stimuli, while the semantically incongruent stimuli did not elicit brain patterns with significantly higher reproducibility index or decoding accuracy. Thus, the semantically congruent audiovisual stimuli enhanced the within-class reproducibility of brain patterns and the between-class discriminability of brain patterns, and facilitate neural representations of semantic categories or concepts. Furthermore, we analyzed the brain activity in superior temporal sulcus and middle temporal gyrus (STS/MTG). The strength of the fMRI signal and the reproducibility index were enhanced by the semantically congruent audiovisual stimuli. Our results support the use of the reproducibility index as a potential tool to supplement the fMRI signal amplitude for evaluating multimodal integration.     

How bodies and voices interact in early emotion perception

Successful social communication draws strongly on the correct interpretation of others' body and vocal expressions. Both can provide emotional information and often occur simultaneously. Yet their interplay has hardly been studied. Using electroencephalography, we investigated the temporal development underlying their neural interaction in auditory and visual perception. In particular, we tested whether this interaction qualifies as true integration following multisensory integration principles such as inverse effectiveness. Emotional vocalizations were embedded in either low or high levels of noise and presented with or without video clips of matching emotional body expressions. In both, high and low noise conditions, a reduction in auditory N100 amplitude was observed for audiovisual stimuli. However, only under high noise, the N100 peaked earlier in the audiovisual than the auditory condition, suggesting facilitatory effects as predicted by the inverse effectiveness principle. Similarly, we observed earlier N100 peaks in response to emotional compared to neutral audiovisual stimuli. This was not the case in the unimodal auditory condition. Furthermore, suppression of beta-band oscillations (15-25 Hz) primarily reflecting biological motion perception was modulated 200-400 ms after the vocalization. While larger differences in suppression between audiovisual and audio stimuli in high compared to low noise levels were found for emotional stimuli, no such difference was observed for neutral stimuli. This observation is in accordance with the inverse effectiveness principle and suggests a modulation of integration by emotional content. Overall, results show that ecologically valid, complex stimuli such as joined body and vocal expressions are effectively integrated very early in processing.     

Sparse representation of sounds in the unanesthetized auditory cortex

How do neuronal populations in the auditory cortex represent acoustic stimuli? Although sound-evoked neural responses in the anesthetized auditory cortex are mainly transient, recent experiments in the unanesthetized preparation have emphasized subpopulations with other response properties. To quantify the relative contributions of these different subpopulations in the awake preparation, we have estimated the representation of sounds across the neuronal population using a representative ensemble of stimuli. We used cell-attached recording with a glass electrode, a method for which single-unit isolation does not depend on neuronal activity, to quantify the fraction of neurons engaged by acoustic stimuli (tones, frequency modulated sweeps, white-noise bursts, and natural stimuli) in the primary auditory cortex of awake head-fixed rats. We find that the population response is sparse, with stimuli typically eliciting high firing rates (>20 spikes/second) in less than 5% of neurons at any instant. Some neurons had very low spontaneous firing rates (<0.01 spikes/second). At the other extreme, some neurons had driven rates in excess of 50 spikes/second. Interestingly, the overall population response was well described by a lognormal distribution, rather than the exponential distribution that is often reported. Our results represent, to our knowledge, the first quantitative evidence for sparse representations of sounds in the unanesthetized auditory cortex. Our results are compatible with a model in which most neurons are silent much of the time, and in which representations are composed of small dynamic subsets of highly active neurons.     

Brain damage and global stereopsis.

When a single object lies in front of or beyond the plane of fixation its retinal image lies on disparate positions in the two eyes. This 'local' retinal disparity is an excellent cue to depth, and retinal disparties of a few seconds of arc are detectable by people and monkeys. However, most visual scenes produce a complex array of contours in each eye and we can detect the disparity in the arrays despite the ambiguous nature of the disparities, i.e. each contour in one eye could be related to any of several similar contours in the other eye. This ability, known as 'global' stereopsis, may be selectively impaired following brain damage in man. Global stereopsis was measured in rhesus monkeys before and after removing a different cortical visual area in different groups of animals. Only removal of the inferotemporal cortex impaired global stereopsis. The result is related to the findings with human patients and to receptive field properties of neurons in the inferotemporal cortex of monkeys.     

Eye position affects activity in primary auditory cortex of primates

BACKGROUND: Neurons in primary auditory cortex are known to be sensitive to the locations of sounds in space, but the reference frame for this spatial sensitivity has not been investigated. Conventional wisdom holds that the auditory and visual pathways employ different reference frames, with the auditory pathway using a head-centered reference frame and the visual pathway using an eye-centered reference frame. Reconciling these discrepant reference frames is therefore a critical component of multisensory integration. RESULTS: We tested the reference frame of neurons in the auditory cortex of primates trained to fixate visual stimuli at different orbital positions. We found that eye position altered the activity of about one third of the neurons in this region (35 of 113, or 31%). Eye position affected not only the responses to sounds (26 of 113, or 23%), but also the spontaneous activity (14 of 113, or 12%). Such effects were also evident when monkeys moved their eyes freely in the dark. Eye position and sound location interacted to produce a representation for auditory space that was neither head- nor eye-centered in reference frame. CONCLUSIONS: Taken together with emerging results in both visual and other auditory areas, these findings suggest that neurons whose responses reflect complex interactions between stimulus position and eye position set the stage for the eventual convergence of auditory and visual information.     

Causal inference regulates audiovisual spatial recalibration via its influence on audiovisual perception

To obtain a coherent perception of the world, our senses need to be in alignment. When we encounter misaligned cues from two sensory modalities, the brain must infer which cue is faulty and recalibrate the corresponding sense. We examined whether and how the brain uses cue reliability to identify the miscalibrated sense by measuring the audiovisual ventriloquism aftereffect for stimuli of varying visual reliability. To adjust for modality-specific biases, visual stimulus locations were chosen based on perceived alignment with auditory stimulus locations for each participant. During an audiovisual recalibration phase, participants were presented with bimodal stimuli with a fixed perceptual spatial discrepancy; they localized one modality, cued after stimulus presentation. Unimodal auditory and visual localization was measured before and after the audiovisual recalibration phase. We compared participants’ behavior to the predictions of three models of recalibration: (a) Reliability-based: each modality is recalibrated based on its relative reliability—less reliable cues are recalibrated more; (b) Fixed-ratio: the degree of recalibration for each modality is fixed; (c) Causal-inference: recalibration is directly determined by the discrepancy between a cue and its estimate, which in turn depends on the reliability of both cues, and inference about how likely the two cues derive from a common source. Vision was hardly recalibrated by audition. Auditory recalibration by vision changed idiosyncratically as visual reliability decreased: the extent of auditory recalibration either decreased monotonically, peaked at medium visual reliability, or increased monotonically. The latter two patterns cannot be explained by either the reliability-based or fixed-ratio models. Only the causal-inference model of recalibration captures the idiosyncratic influences of cue reliability on recalibration. We conclude that cue reliability, causal inference, and modality-specific biases guide cross-modal recalibration indirectly by determining the perception of audiovisual stimuli.     

Behavioral and Neurogenomic Responses to Acoustic and Visual Sexual Cues are Correlated in Female Torrent Frogs

Diverse a nimal species use multimodal communica tion signals to coordina te reproductive behavior.Despite active research in this field,the brain mechanisms underlying multimodal communication remain poorly understood.Similar to humans and many mammalian species,anurans often produce auditory signals accompanied by conspicuous visual cues(e.g.,vocal sac inflation).In this study,we used video playbacks to determine the role of vocal-sac inflation in little torrent frogs(Amolops torrentis).Then we exposed females to blank,visual,auditory,and audiovisual stimuli and analyzed whole brain tissue gene expression changes using RNAseq.The results showed that both auditory cues(i.e.,male advertisement calls)and visual cues were attractive to female frogs,although auditory cues were more attractive than visual cues.Females preferred simultaneous bimodal cues to unimodal cues.The hierarchical clustering of differentially expressed genes showed a close relationship between neurogenomic states and momentarily expressed sexual signals.We also found that the Gene Ontology terms and KEGG pathways involved in energy metabolism were mostly increased in blank contrast versus visual,acoustic,or audiovisual stimuli,indicating that brain energy use may play an important role in response to these stimuli.In sum,behavioral and neurogenomic responses to acoustic and visual cues are correlated in female little torrent frogs.     

The attentional window modulates capture by audiovisual events

Visual search is markedly improved when a target color change is synchronized with a spatially non-informative auditory signal. This "pip and pop" effect is an automatic process as even a distractor captures attention when accompanied by a tone. Previous studies investigating visual attention have indicated that automatic capture is susceptible to the size of the attentional window. The present study investigated whether the pip and pop effect is modulated by the extent to which participants divide their attention across the visual field We show that participants were better in detecting a synchronized audiovisual event when they divided their attention across the visual field relative to a condition in which they focused their attention. We argue that audiovisual capture is reduced under focused conditions relative to distributed settings.     

Rapid,generalized adaptation to asynchronous audiovisual speech

The brain is adaptive. The speed of propagation through air, and of low-level sensory processing, differs markedly between auditory and visual stimuli; yet the brain can adapt to compensate for the resulting cross-modal delays. Studies investigating temporal recalibration to audiovisual speech have used prolonged adaptation procedures, suggesting that adaptation is sluggish. Here, we show that adaptation to asynchronous audiovisual speech occurs rapidly. Participants viewed a brief clip of an actor pronouncing a single syllable. The voice was either advanced or delayed relative to the corresponding lip movements, and participants were asked to make a synchrony judgement. Although we did not use an explicit adaptation procedure, we demonstrate rapid recalibration based on a single audiovisual event. We find that the point of subjective simultaneity on each trial is highly contingent upon the modality order of the preceding trial. We find compelling evidence that rapid recalibration generalizes across different stimuli, and different actors. Finally, we demonstrate that rapid recalibration occurs even when auditory and visual events clearly belong to different actors. These results suggest that rapid temporal recalibration to audiovisual speech is primarily mediated by basic temporal factors, rather than higher-order factors such as perceived simultaneity and source identity.     

Evidence for Enhanced Multisensory Facilitation with Stimulus Relevance: An Electrophysiological Investigation

Currently debate exists relating to the interplay between multisensory processes and bottom-up and top-down influences. However, few studies have looked at neural responses to newly paired audiovisual stimuli that differ in their prescribed relevance. For such newly associated audiovisual stimuli, optimal facilitation of motor actions was observed only when both components of the audiovisual stimuli were targets. Relevant auditory stimuli were found to significantly increase the amplitudes of the event-related potentials at the occipital pole during the first 100 ms post-stimulus onset, though this early integration was not predictive of multisensory facilitation. Activity related to multisensory behavioral facilitation was observed approximately 166 ms post-stimulus, at left central and occipital sites. Furthermore, optimal multisensory facilitation was found to be associated with a latency shift of induced oscillations in the beta range (14–30 Hz) at right hemisphere parietal scalp regions. These findings demonstrate the importance of stimulus relevance to multisensory processing by providing the first evidence that the neural processes underlying multisensory integration are modulated by the relevance of the stimuli being combined. We also provide evidence that such facilitation may be mediated by changes in neural synchronization in occipital and centro-parietal neural populations at early and late stages of neural processing that coincided with stimulus selection, and the preparation and initiation of motor action.     

Long-Term Stability of Visual Pattern Selective Responses of Monkey Temporal Lobe Neurons

Many neurons in primate inferotemporal (IT) cortex respond selectively to complex, often meaningful, stimuli such as faces and objects. An important unanswered question is whether such response selectivity, which is thought to arise from experience-dependent plasticity, is maintained from day to day, or whether the roles of individual cells are continually reassigned based on the diet of natural vision. We addressed this question using microwire electrodes that were chronically implanted in the temporal lobe of two monkeys, often allowing us to monitor activity of individual neurons across days. We found that neurons maintained their selectivity in both response magnitude and patterns of spike timing across a large set of visual images throughout periods of stable signal isolation from the same cell that sometimes exceeded two weeks. These results indicate that stimulus-selectivity of responses in IT is stable across days and weeks of visual experience.     

Nonlinear visuoauditory integration in the mouse superior colliculus

Sensory information from different modalities is processed in parallel, and then integrated in associative brain areas to improve object identification and the interpretation of sensory experiences. The Superior Colliculus (SC) is a midbrain structure that plays a critical role in integrating visual, auditory, and somatosensory input to assess saliency and promote action. Although the response properties of the individual SC neurons to visuoauditory stimuli have been characterized, little is known about the spatial and temporal dynamics of the integration at the population level. Here we recorded the response properties of SC neurons to spatially restricted visual and auditory stimuli using large-scale electrophysiology. We then created a general, population-level model that explains the spatial, temporal, and intensity requirements of stimuli needed for sensory integration. We found that the mouse SC contains topographically organized visual and auditory neurons that exhibit nonlinear multisensory integration. We show that nonlinear integration depends on properties of auditory but not visual stimuli. We also find that a heuristically derived nonlinear modulation function reveals conditions required for sensory integration that are consistent with previously proposed models of sensory integration such as spatial matching and the principle of inverse effectiveness.     

Realigning Thunder and Lightning: Temporal Adaptation to Spatiotemporally Distant Events

The brain is able to realign asynchronous signals that approximately coincide in both space and time. Given that many experience-based links between visual and auditory stimuli are established in the absence of spatiotemporal proximity, we investigated whether or not temporal realignment arises in these conditions. Participants received a 3-min exposure to visual and auditory stimuli that were separated by 706 ms and appeared either from the same (Experiment 1) or from different spatial positions (Experiment 2). A simultaneity judgment task (SJ) was administered right afterwards. Temporal realignment between vision and audition was observed, in both Experiment 1 and 2, when comparing the participants’ SJs after this exposure phase with those obtained after a baseline exposure to audiovisual synchrony. However, this effect was present only when the visual stimuli preceded the auditory stimuli during the exposure to asynchrony. A similar pattern of results (temporal realignment after exposure to visual-leading asynchrony but not after exposure to auditory-leading asynchrony) was obtained using temporal order judgments (TOJs) instead of SJs (Experiment 3). Taken together, these results suggest that temporal recalibration still occurs for visual and auditory stimuli that fall clearly outside the so-called temporal window for multisensory integration and appear from different spatial positions. This temporal realignment may be modulated by long-term experience with the kind of asynchrony (vision-leading) that we most frequently encounter in the outside world (e.g., while perceiving distant events).     

Response variability in the mammalian auditory cortex: an objection to feature detection?

Research strategy in the auditory system has tended to parallel that in the visual system, where neurons have been shown to respond selectively to specific stimulus parameters. Auditory neurons have been shown to be sensitive to changes in acoustic parameters, but only rarely have neurons been reported that respond exclusively to only one biologically significant sound. Even at higher levels of the auditory system very few cells have been found that could be described as "vocalization detectors." In addition, variability in responses to artificial sounds have been reported for auditory cortical neurons similar to the response variability that has been reported in the visual system. Recent evidence indicates that the responses of auditory cortical neurons to species-specific vocalizations can also be labile, varying in both strength and selectivity. This is especially true of the secondary auditory cortex. This variability, coupled with the lack of extreme specificity in the secondary auditory cortex, suggests that secondary cortical neurons are not well suited for the role of "vocalization detectors."     

幼年大鼠皮层听-视多感觉神经元和听-视信息整合

应用常规电生理学细胞外记录技术,研究了生后3周龄幼年大鼠皮层听-视双模态神经元及听-视信息整合特性,并与成年动物进行对照。在听皮层的背侧,听皮层和视皮层的交界处,即颞-顶-枕联合皮层区,共记录到了324个神经元,其中45个为听-视双模态神经元,占13.9%,远低于成年动物双模态神经元所占比例(42.8%)。这些双模态神经元可分为A-V型,v-A型和a-V型3种类型。根据它们对听-视信息的整合效应,可分为增强型、抑制型和调制型。整合效应与给予的声和光组合刺激的时间间隔有关,以获得整合效应的时间间隔范围为整合时间窗,幼年动物的平均整合时间窗为11.9 ms,远小于成年动物的整合时间窗(平均为23.2 ms)。结果提示,与单模态感觉神经元对模态特异性反应特性一样,皮层听-视双模态神经元生后有一个发育、成熟的过程。研究结果为深入研究中枢神经元多感觉整合机制提供了重要实验资料。     

The Brain’s Dorsal Route for Speech Represents Word Meaning: Evidence from Gesture

The dual-route model of speech processing includes a dorsal stream that maps auditory to motor features at the sublexical level rather than at the lexico-semantic level. However, the literature on gesture is an invitation to revise this model because it suggests that the premotor cortex of the dorsal route is a major site of lexico-semantic interaction. Here we investigated lexico-semantic mapping using word-gesture pairs that were either congruent or incongruent. Using fMRI-adaptation in 28 subjects, we found that temporo-parietal and premotor activity during auditory processing of single action words was modulated by the prior audiovisual context in which the words had been repeated. The BOLD signal was suppressed following repetition of the auditory word alone, and further suppressed following repetition of the word accompanied by a congruent gesture (e.g. [“grasp” + grasping gesture]). Conversely, repetition suppression was not observed when the same action word was accompanied by an incongruent gesture (e.g. [“grasp” + sprinkle]). We propose a simple model to explain these results: auditory and visual information converge onto premotor cortex where it is represented in a comparable format to determine (in)congruence between speech and gesture. This ability of the dorsal route to detect audiovisual semantic (in)congruence suggests that its function is not restricted to the sublexical level.