Temporal Acuity Research Articles

Review of chaos in hair-cell dynamics.

The remarkable signal-detection capabilities of the auditory and vestibular systems have been studied for decades. Much of the conceptual framework that arose from this research has suggested that these sensory systems rest on the verge of instability, near a Hopf bifurcation, in order to explain the detection specifications. However, this paradigm contains several unresolved issues. Critical systems are not robust to stochastic fluctuations or imprecise tuning of the system parameters. Further, a system poised at criticality exhibits a phenomenon known in dynamical systems theory as critical slowing down, where the response time diverges as the system approaches the critical point. An alternative description of these sensory systems is based on the notion of chaotic dynamics, where the instabilities inherent to the dynamics produce high temporal acuity and sensitivity to weak signals, even in the presence of noise. This alternative description resolves the issues that arise in the criticality picture. We review the conceptual framework and experimental evidence that supports the use of chaos for signal detection by these systems, and propose future validation experiments.

Criticality and chaos in auditory and vestibular sensing

The auditory and vestibular systems exhibit remarkable sensitivity of detection, responding to deflections on the order of angstroms, even in the presence of biological noise. The auditory system exhibits high temporal acuity and frequency selectivity, allowing us to make sense of the acoustic world around us. As the acoustic signals of interest span many orders of magnitude in both amplitude and frequency, this system relies heavily on nonlinearities and power-law scaling. The vestibular system, which detects ground-borne vibrations and creates the sense of balance, exhibits highly sensitive, broadband detection. It likewise requires high temporal acuity so as to allow us to maintain balance while in motion. The behavior of these sensory systems has been extensively studied in the context of dynamical systems theory, with many empirical phenomena described by critical dynamics. Other phenomena have been explained by systems in the chaotic regime, where weak perturbations drastically impact the future state of the system. Using a Hopf oscillator as a simple numerical model for a sensory element in these systems, we explore the intersection of the two types of dynamical phenomena. We identify the relative tradeoffs between different detection metrics, and propose that, for both types of sensory systems, the instabilities giving rise to chaotic dynamics improve signal detection.

Working memory updating as a mediator of the relation between temporal resolution power and psychometric intelligence

The temporal resolution power (TRP) hypothesis states that higher temporal acuity of the brain leads to better coordinated mental operations and, in turn, to better performance on tests of psychometric intelligence. Here, we examined this idea and concretized the vague construct “coordination of mental operations” through working memory (WM) updating. In 228 participants (age range: 18 to 30 years), TRP as derived from three timing tasks was significantly related to psychometric intelligence. Furthermore, WM updating was measured by Stankov's swaps task and depicted as a latent variable with increasing factor loadings to represent the increasing number of WM updates in different task conditions. WM updating correlated significantly with psychometric intelligence. In a latent mediation analysis, TRP and WM updating were still directly related to psychometric intelligence. Although the TRP-intelligence link did not substantially decrease in this model, the indirect path from TRP via WM updating to intelligence was statistically significant. This result suggests that higher TRP leads to temporally more precise mental representations in WM. Thereby, the present study provides a first answer to the question of how higher TRP translates into better performance and, eventually, to higher intelligence. Alternative views on the results are critically discussed.

Binaural advantages in sound temporal information processing by neurons in the rat inferior colliculus.

Previous studies on the advantages of binaural hearing have long been focused on sound localization and spatial stream segregation. The binaural advantages have also been observed in speech perception in reverberation. Both human speech and animal vocalizations contain temporal features that are critical for speech perception and animal communication. However, whether there are binaural advantages for sound temporal information processing in the central auditory system has not been elucidated. Gap detection threshold (GDT), the ability to detect the shortest silent interval in a sound, has been widely used to measure the auditory temporal resolution. In the present study, we determined GDTs of rat inferior collicular neurons under both monaural and binaural hearing conditions. We found that the majority of the inferior collicular neurons in adult rats exhibited binaural advantages in gap detection, i.e., better neural gap detection ability in binaural hearing conditions compared to monaural hearing condition. However, this binaural advantage in sound temporal information processing was not significant in the inferior collicular neurons of P14-21 and P22-30 rats. Additionally, we also observed age-related changes in neural temporal acuity in the rat inferior colliculus. These results demonstrate a new advantage of binaural hearing (i.e., binaural advantage in temporal processing) in the central auditory system in addition to sound localization and spatial stream segregation.

Alpha-band sensory entrainment improves audiovisual temporal acuity.

Visual and auditory stimuli are transmitted from the environment to sensory cortices with different timing, requiring the brain to encode when sensory inputs must be segregated or integrated into a single percept. The probability that different audiovisual (AV) stimuli are integrated into a single percept even when presented asynchronously is reflected in the construct of temporal binding window (TBW). There is a strong interest in testing whether it is possible to broaden or shrink TBW by using different neuromodulatory approaches that can speed up or slow down ongoing alpha oscillations, which have been repeatedly hypothesized to be an important determinant of the TBWs size. Here, we employed a web-based sensory entrainment protocol combined with a simultaneity judgment task using simple flash-beep stimuli. The aim was to test whether AV temporal acuity could be modulated trial by trial by synchronizing ongoing neural oscillations in the prestimulus period to a rhythmic sensory stream presented in the upper (∼12 Hz) or lower (∼8.5 Hz) alpha range. As a control, we implemented a nonrhythmic condition where only the first and the last entrainers were employed. Results show that upper alpha entrainment shrinks AV TBW and improves AV temporal acuity when compared with lower alpha and control conditions. Our findings represent a proof of concept of the efficacy of sensory entrainment to improve AV temporal acuity in a trial-by-trial manner, and they strengthen the idea that alpha oscillations may reflect the temporal unit of AV temporal binding.

Electrophysiological and behavioral assessment of binaural processing: Effects of age

Spatial hearing deteriorates with age, but the basis(es) of this age-dependency is not clear and could reflect both bottom-up and top-down factors. Since binaural processing depends in part on interaural time difference cues, this study assessed binaural temporal acuity using both objective and behavioral measures. Three tasks incorporating interaural time/phase differences were tested: (1) in-phase and out-of-phase frequency modulation (FM) detection as a function of FM rate; (2) upper frequency limit of in-phase versus out-of-phase tone discrimination; and (3) minimum audible angle for low frequency tones. Each task incorporated parallel behavioral and electrophysiological measures: For behavior, forced-choice adaptive methods were employed; for electrophysiology, the acoustic change complex (ACC) was recorded. Additional measures of peripheral auditory function, as well as cognitive status, were also collected. Young and middle-aged adults (n = 20 per age group) with normal audiometric hearing were tested. Differences in behavioral measures of binaural performance were noted between the two age groups and these were reflected to some extent in the ACC results. However, group differences were also noted in terms of cochlear function and in terms of cognitive abilities. This pattern of results suggests that age-related deterioration in spatial perception is likely to be multi-faceted.

Keep your finger on the pulse: Better rate perception and gap detection with vibrotactile compared to visual stimuli

Important characteristics of the environment can be represented in the temporal pattern of sensory stimulation. In two experiments, we compared accuracy of temporal processing by different modalities. Experiment 1 examined binary categorization of rate for visual (V) or vibrotactile (T) stimulus pulses presented at either 4 or 6 Hz. Inter-pulse intervals were either constant or variable, perturbed by random Gaussian variates. Subjects categorized the rate of T pulse sequences more accurately than V sequences. In V conditions only, subjects disproportionately tended to mis-categorize 4-Hz pulse rates, for all but the most variable sequences. In Experiment 2, we compared gap detection thresholds across modalities, using the same V and T pulses from Experiment 1, as well as with bimodal (VT) pulses. Visual gap detection thresholds were larger (3times ) than tactile thresholds. Additionally, performance with VT stimuli seemed to be nearly completely dominated by their T components. Together, these results suggest (i) that vibrotactile temporal acuity surpasses visual temporal acuity, and (ii) that vibrotactile stimulation has considerable, untapped potential to convey temporal information like that needed for eyes-free alerting signals.

An imbalance of excitation and inhibition in the multisensory cortex impairs the temporal acuity of audiovisual processing and perception.

The neural integration of closely timed auditory and visual stimuli can offer several behavioral advantages; however, an overly broad window of temporal integration-a phenomenon observed in various neurodevelopmental disorders-could have far-reaching perceptual consequences. Non-invasive studies in humans have suggested that the level of GABAergic inhibition in the multisensory cortex influences the temporal window over which auditory and visual stimuli are bound into a unified percept. Although this suggestion aligns with the theory that an imbalance of cortical excitation and inhibition alters multisensory processing, no prior studies have performed experimental manipulations to determine the causal effects of a reduction of GABAergic inhibition on audiovisual temporal perception. To that end, we used a combination of in vivo electrophysiology, neuropharmacology, and translational behavioral testing in rats to provide the first mechanistic evidence that a reduction of GABAergic inhibition in the audiovisual cortex is sufficient to disrupt unisensory and multisensory processing across the cortical layers, and ultimately impair the temporal acuity of audiovisual perception and its rapid adaptation to recent sensory experience. Looking forward, our findings provide support for using rat models to further investigate the neural mechanisms underlying the audiovisual perceptual alterations observed in neurodevelopmental disorders, such as autism, schizophrenia, and dyslexia.

High Spectral and Temporal Acuity in Primary Auditory Cortex of Awake Cats

Most accounts of single- and multi-unit responses in auditory cortex under anesthetized conditions have emphasized V-shaped frequency tuning curves and low-pass sensitivity to rates of repeated sounds. In contrast, single-unit recordings in awake marmosets also show I-shaped and O-shaped response areas having restricted tuning to frequency and (for O units) sound level. That preparation also demonstrates synchrony to moderate click rates and representation of higher click rates by spike rates of non-synchronized tonic responses, neither of which are commonly seen in anesthetized conditions. The spectral and temporal representation observed in the marmoset might reflect special adaptations of that species, might be due to single- rather than multi-unit recording, or might indicate characteristics of awake-versus-anesthetized recording conditions. We studied spectral and temporal representation in the primary auditory cortex of alert cats. We observed V-, I-, and O-shaped response areas like those demonstrated in awake marmosets. Neurons could synchronize to click trains at rates about an octave higher than is usually seen with anesthesia. Representations of click rates by rates of non-synchronized tonic responses exhibited dynamic ranges that covered the entire range of tested click rates. The observation of these spectral and temporal representations in cats demonstrates that they are not unique to primates and, indeed, might be widespread among mammalian species. Moreover, we observed no significant difference in stimulus representation between single- and multi-unit recordings. It appears that the principal factor that has hindered observations of high spectral and temporal acuity in the auditory cortex has been the use of general anesthesia.

Effects of Spatial Attention on Spatial and Temporal Acuity Explained by Parvo-Magno Interactions: A Computational Account

Effects of Spatial Attention on Spatial and Temporal Acuity Explained by Parvo-Magno Interactions: A Computational Account

Low Intensity Noise Exposure Enhanced Auditory Loudness and Temporal Processing by Increasing Excitability of DCN.

Sound stimulation is generally used for tinnitus and hyperacusis treatment. Recent studies found that long-term noise exposure can change synaptic and firing properties in the central auditory system, which will be detected by the acoustic startle reflex. However, the perceptual consequences of long-term low-intensity sound exposure are indistinct. This study will detect the effects of moderate-level noise exposure (83 dB SPL) on auditory loudness, and temporal processing was evaluated using CBA/CaJ mice. C-Fos staining was used to detect neural activity changes in the central auditory pathway. With two weeks of 83 dB SPL noise exposure (8 hours per day), no persistent threshold shift of the auditory brainstem response (ABR) was identified. On the other hand, noise exposure enhanced the acoustic startle response (ASR) and gap-induced prepulse inhibition significantly (gap-PPI). Low-level noise exposure, according to the findings, can alter temporal acuity. Noise exposure increased the number of c-Fos labeled neurons in the dorsal cochlear nucleus (DCN) and caudal pontine reticular nucleus (PnC) but not at a higher level in the central auditory nuclei. Our results suggested that noise stimulation can change acoustical temporal processing presumably by increasing the excitability of auditory brainstem neurons.

The effect of input sensory modality on the multimodal encoding of motion events

ABSTRACT Each sensory modality has different affordances: vision has higher spatial acuity than audition, whereas audition has better temporal acuity. This may have consequences for the encoding of events and its subsequent multimodal language production—an issue that has received relatively little attention to date. In this study, we compared motion events presented as audio-only, visual-only, or multimodal (visual + audio) input and measured speech and co-speech gesture depicting path and manner of motion in Turkish. Input modality affected speech production. Speakers with audio-only input produced more path descriptions and fewer manner descriptions in speech compared to speakers who received visual input. In contrast, the type and frequency of gestures did not change across conditions. Path-only gestures dominated throughout. Our results suggest that while speech is more susceptible to auditory vs. visual input in encoding aspects of motion events, gesture is less sensitive to such differences.

The influence of temporal asynchrony on character-speech integration in Chinese children with and without dyslexia: An ERP study

Dyslexic readers have been reported to show abnormal temporal acuity and multisensory integration deficiency. Here, we investigated the influence of temporal intervals on Chinese character-speech integration in children with and without dyslexia. Visual characters were presented synchronously to the onset of speech sounds (AV0) or before speech sound by 300 ms (AV300). Event-related potentials (ERP) evoked by congruent condition (speech sounds presented with congruent Chinese characters) and by baseline condition (speech sounds presented with Korean characters) were compared. Typically developing (TD) children exhibited congruency effect in AV0 condition, whereas dyslexic children exhibited congruency effect in AV300 condition. Moreover, congruency effect in TD children was due to enhanced neural activation to congruent trials, congruency effect in dyslexic children was contributed by neural suppression for baseline trials. These results suggested that different underlying mechanisms were involved in character-speech integration for typical and dyslexic children.

Synaptic Mechanisms Underlying Temporally Precise Information Processing in the VNLL, an Auditory Brainstem Nucleus.

Large glutamatergic, somatic synapses mediate temporally precise information transfer. In the ventral nucleus of the lateral lemniscus, an auditory brainstem nucleus, the signal of an excitatory large somatic synapse is sign inverted to generate rapid feedforward inhibition with high temporal acuity at sound onsets, a mechanism involved in the suppression of spurious frequency information. The mechanisms of the synaptically driven input-output functions in the ventral nucleus of the lateral lemniscus are not fully resolved. Here, we show in Mongolian gerbils of both sexes that, for stimulation frequencies up to 200 Hz, the EPSC kinetics together with short-term plasticity allow for faithful transmission with only a small increase in latency. Glutamatergic currents are exclusively mediated by AMPARs and NMDARs. Short-term plasticity is frequency-dependent and composed of an initial facilitation followed by depression. Physiologically relevant output generation is limited by the decrease in synaptic conductance through short-term plasticity (STP). At this endbulb synapse, STP acts as a low pass filter and increases the dynamic range of the conductance dependent input-output relation, while NMDAR signaling slightly increases the sensitivity of the input-output function. Our computational model shows that STP-mediated filtering limits the intensity dependence of the spike output, thus maintaining selectivity to sound transients. Our results highlight the interaction of cellular features that together give rise to the computations in the circuit.SIGNIFICANCE STATEMENT Auditory information processing in the brainstem is a prerequisite for generating our auditory representation of the environment. Thereby, many processing steps rely on temporally precise filtering. Precise feedforward inhibition is a key motif in auditory brainstem processing and produced through sign inversion at several large somatic excitatory synapses. A particular feature of the ventral nucleus of the lateral lemniscus is to produce temporally precise onset inhibition with little temporal variance independent of sound intensity. Our cell-physiology and modeling data explain how the synaptic characteristics of different current components and their short-term plasticity are tuned to establish sound intensity-invariant onset inhibition that is crucial for filtering out spurious frequency information.

Effects of spatial attention on spatial and temporal acuity: A computational account.

In our daily lives, the visual system receives a plethora of visual information that competes for the brain's limited processing capacity. Nevertheless, not all visual information is useful for our cognitive, emotional, social, and ultimately survival purposes. Therefore, the brain employs mechanisms to select critical information and thereby optimizes its limited resources. Attention is the selective process that serves such a function. In particular, covert spatial attention - attending to a particular location in the visual field without eye movements - improves spatial resolution and paradoxically deteriorates temporal resolution. The neural correlates underlying these attentional effects still remainelusive. In this work, we tested a neural model's predictions that explain these phenomena based on interactions between channels with different spatiotemporal sensitivities - namely, the magnocellular (transient) and parvocellular (sustained) channels. More specifically, our model postulates that spatial attention enhances activities in the parvocellular pathway, thereby producing improved performance in spatial resolution tasks. However, the enhancement of parvocellular activities leads to decreased magnocellular activities due to parvo-magno inhibitory interactions. As a result, spatial attention hampers temporal resolution. We compared the predictions of the model to psychophysical data, and show that our model can account qualitatively and quantitatively for the effects of spatial attention on spatial and temporal acuity.

Auditory steady state responses elicited by silent gaps embedded within a broadband noise.

BackgroundAuditory temporal processing plays an important role in speech comprehension. Usually, behavioral tests that require subjects to detect silent gaps embedded within a continuous sound are used to assess the ability of auditory temporal processing in humans. To evaluate auditory temporal processing objectively, the present study aimed to measure the auditory steady state responses (ASSRs) elicited by silent gaps of different lengths embedded within a broadband noise. We presented a broadband noise with 40-Hz silent gaps of 3.125, 6.25, and 12.5 ms.ResultsThe 40-Hz silent gaps of 3.125, 6.25, and 12.5 ms elicited clear ASSRs. Longer silent gaps elicited larger ASSR amplitudes and ASSR phases significantly differed between conditions.ConclusionThe 40 Hz gap-evoked ASSR contributes to our understanding of the neural mechanisms underlying auditory temporal processing and may lead to the development of objective measures of auditory temporal acuity in humans.Supplementary InformationThe online version contains supplementary material available at 10.1186/s12868-022-00712-0.

Lower multisensory temporal acuity in individuals with high schizotypal traits: a web-based study

Natural events are often multisensory, requiring the brain to combine information from the same spatial location and timing, across different senses. The importance of temporal coincidence has led to the introduction of the temporal binding window (TBW) construct, defined as the time range within which multisensory inputs are highly likely to be perceptually bound into a single entity. Anomalies in TBWs have been linked to confused perceptual experiences and inaccurate filtering of sensory inputs coming from different environmental sources. Indeed, larger TBWs have been associated with disorders such as schizophrenia and autism and are also correlated to a higher level of subclinical traits of these conditions in the general population. Here, we tested the feasibility of using a web-based version of a classic audio-visual simultaneity judgment (SJ) task with simple flash-beep stimuli in order to measure multisensory temporal acuity and its relationship with schizotypal traits as measured in the general population. Results show that: (i) the response distribution obtained in the web-based SJ task was strongly similar to those reported by studies carried out in controlled laboratory settings, and (ii) lower multisensory temporal acuity was associated with higher schizotypal traits in the “cognitive-perceptual” domains. Our findings reveal the possibility of adequately using a web-based audio-visual SJ task outside a controlled laboratory setting, available to a more diverse and representative pool of participants. These results provide additional evidence for a close relationship between lower multisensory acuity and the expression of schizotypal traits in the general population.

Abnormal multisensory integration in relapsing\u2013remitting multiple sclerosis

Temporal Binding Window (TBW) represents a reliable index of efficient multisensory integration process, which allows individuals to infer which sensory inputs from different modalities pertain to the same event. TBW alterations have been reported in some neurological and neuropsychiatric disorders and seem to negatively affects cognition and behavior. So far, it is still unknown whether deficits of multisensory integration, as indexed by an abnormal TBW, are present even in Multiple Sclerosis. We addressed this issue by testing 25 participants affected by relapsing–remitting Multiple Sclerosis (RRMS) and 30 age-matched healthy controls. Participants completed a simultaneity judgment task (SJ2) to assess the audio-visual TBW; two unimodal SJ2 versions were used as control tasks. Individuals with RRMS showed an enlarged audio-visual TBW (width range = from − 166 ms to + 198 ms), as compared to healthy controls (width range = − 177/ + 66 ms), thus showing an increased tendency to integrate temporally asynchronous visual and auditory stimuli. Instead, simultaneity perception of unimodal (visual or auditory) events overall did not differ from that of controls. These results provide first evidence of a selective deficit of multisensory integration in individuals affected by RRMS, besides the well-known motor and cognitive impairments. The reduced multisensory temporal acuity is likely caused by a disruption of the neural interplay between different sensory systems caused by multiple sclerosis.

Acuity and summation strategies differ in vinegar and desert fruit flies

SummaryAn animal's vision depends on terrain features that limit the amount and distribution of available light. Approximately 10,000 years ago, vinegar flies (Drosophila melanogaster) transitioned from a single plant specialist into a cosmopolitan generalist. Much earlier, desert flies (D. mojavensis) colonized the New World, specializing on rotting cactuses in southwest North America. Their desert habitats are characteristically flat, bright, and barren, implying environmental differences in light availability. Here, we demonstrate differences in eye morphology and visual motion perception under three ambient light levels. Reducing ambient light from 35 to 18 cd/m2 causes sensitivity loss in desert but not vinegar flies. However, at 3 cd/m2, desert flies sacrifice spatial and temporal acuity more severely than vinegar flies to maintain contrast sensitivity. These visual differences help vinegar flies navigate under variably lit habitats around the world and desert flies brave the harsh desert while accommodating their crepuscular lifestyle.

Temporal acuity is preserved in the auditory midbrain of aged mice

Impaired temporal resolution of the central auditory system has long been suggested to contribute to speech understanding deficits in the elderly. However, it has been difficult to differentiate between direct age-related central deficits and indirect effects of confounding peripheral age-related hearing loss on temporal resolution. To differentiate this, we measured temporal acuity in the inferior colliculus (IC) of aged CBA/J and C57BL/6 mice, as a model of aging with and without concomitant hearing loss. We used two common measures of auditory temporal processing: gap detection as a measure of temporal fine structure and amplitude-modulated noise as a measure of envelope sensitivity. Importantly, auditory temporal acuity remained precise in the IC of old CBA/J mice when no or only minimal age-related hearing loss was present. In contrast, temporal acuity was only indirectly reduced by the presence of age-related hearing loss in aged C57BL/6 mice, not by affecting the brainstem precision, but by affecting the signal-to-noise ratio of the neuronal activity in the IC. This demonstrates that indirect effects of age-related peripheral hearing loss likely remain an important factor for temporal processing in aging in comparison to 'pure' central auditory decline itself. It also draws attention to the issue that the threshold difference between ‘nearly normal’ or ‘clinically normal’ hearing aging subjects in comparison to normal hearing young subjects still can have indirect effects on central auditory neural representations of temporal processing.