Prefrontal Cortex Regulates Sensory Filtering through a Basal Ganglia-to-Thalamus Pathway.

To make adaptive decisions, organisms must appropriately filter sensory inputs, augmenting relevant signals and suppressing noise. The prefrontal cortex (PFC) partly implements this process by regulating thalamic activity through modality-specific thalamic reticular nucleus (TRN) subnetworks. However, because the PFC does not directly project to sensory TRN subnetworks, the circuitry underlying this process had been unknown. Here, using anatomical tracing, functional manipulations, and optical identification of PFC projection neurons, we find that the PFC regulates sensory thalamic activity through a basal ganglia (BG) pathway. Engagement of this PFC-BG-thalamus pathway enables selection between vision and audition by primarily suppressing the distracting modality. This pathway also enhances sensory discrimination and is used for goal-directed background noise suppression. Overall, our results identify a new pathway for attentional filtering and reveal its multiple roles in sensory processing on the basis of internal goals.

Electro-cortical correlates of multisensory integration using ecologically valid emotional stimuli: Differential effects for fear and disgust.

Multisensory integration (MSI) is crucial for human communication and social interaction and has been investigated in healthy populations and neurodevelopmental disorders. However, the use of stimuli with high ecological validity is sparse, especially in event-related potential (ERP) studies. The present study examined the ERP correlates of MSI in healthy adults using short (500 ms) ecologically valid professional actor-produced emotions of fear or disgust as vocal exclamation or facial expression (unimodal conditions) or both (bimodal condition). Behaviourally, our results show a general visual dominance effect (similarly fast responses following bimodal and visual stimuli) and an MSI-related speedup of responses only for fear. Electrophysiologically, both P100 and N170 showed MSI-related amplitude increases only following fear, but not disgust stimuli. Our results show for the first time that the known differential neural processing of fear and disgust also holds for the integration of dynamic auditory and visual information.

Differential coactivation in a redundant signals task with weak and strong go/no-go stimuli.

When participants respond to stimuli of two sources, response times (RTs) are often faster when both stimuli are presented together relative to the RTs obtained when presented separately (redundant signals effect [RSE]). Race models and coactivation models can explain the RSE. In race models, separate channels process the two stimulus components, and the faster processing time determines the overall RT. In audiovisual experiments, the RSE is often higher than predicted by race models, and coactivation models have been proposed that assume integrated processing of the two stimuli. Where does coactivation occur? We implemented a go/no-go task with randomly intermixed weak and strong auditory, visual, and audiovisual stimuli. In one experimental session, participants had to respond to strong stimuli and withhold their response to weak stimuli. In the other session, these roles were reversed. Interestingly, coactivation was only observed in the experimental session in which participants had to respond to strong stimuli. If weak stimuli served as targets, results were widely consistent with the race model prediction. The pattern of results contradicts the inverse effectiveness law. We present two models that explain the result in terms of absolute and relative thresholds.

Effects of signal bandwidth and noise on individual speaker identification.

Two experiments were conducted to evaluate the effects of increasing spectral bandwidth from 3 to 10 kHz on individual speaker recognition in noisy conditions (+5, 0, and -5 dB signal-to-noise ratio). Experiment 1 utilized h(Vowel)d (hVd) signals, while experiment 2 utilized sentences from the Rainbow Passage. Both experiments showed significant improvements in individual speaker identification in the 10 kHz bandwidth condition (6% for hVds; 10% for sentences). These results coincide with the extant machine recognition literature demonstrating significant amounts of individual speaker information present in the speech signal above approximately 3-4 kHz. Cues from the high-frequency region for speaker identity warrant further study.

A New Foreperiod Effect on Intertrial Phase Coherence. Part I: Existence and Behavioral Relevance.

This letter makes scientific and methodological contributions. Scientifically, it demonstrates a new and behaviorally relevant effect of temporal expectation on the phase coherence of the electroencephalogram (EEG). Methodologically, it introduces novel methods to characterize EEG recordings at the single-trial level. Expecting events in time can lead to more efficient behavior. A remarkable finding in the study of temporal expectation is the foreperiod effect on reaction time, that is, the influence on reaction time of the delay between a warning signal and a succeeding imperative stimulus to which subjects are instructed to respond as quickly as possible. Here we study a new foreperiod effect in an audiovisual attention-shifting oddball task in which attention-shift cues directed the attention of subjects to impendent deviant stimuli of a given modality and therefore acted as warning signals for these deviants. Standard stimuli, to which subjects did not respond, were interspersed between warning signals and deviants. We hypothesized that foreperiod durations modulated intertrial phase coherence (ITPC, the degree of phase alignment across multiple trials) evoked by behaviorally irrelevant standards and that these modulations are behaviorally meaningful. Using averaged data, we first observed that ITPC evoked by standards closer to the warning signal was significantly different from that evoked by standards further away from it, establishing a new foreperiod effect on ITPC evoked by standards. We call this effect the standard foreperiod (SFP) effect on ITPC. We reasoned that if the SFP influences ITPC evoked by standards, it should be possible to decode the former from the latter on a trial-by-trial basis. We were able to do so showing that this effect can be observed in single trials. We demonstrated the behavioral relevance of the SFP effect on ITPC by showing significant correlations between its strength and subjects' behavioral performance.

Primary Tactile Thalamus Spiking Reflects Cognitive Signals.

Little is known about whether information transfer at primary sensory thalamic nuclei is modified by behavioral context. Here we studied the influence of previous decisions/rewards on current choices and preceding spike responses of ventroposterior medial thalamus (VPm; the primary sensory thalamus in the rat whisker-related tactile system). We trained head-fixed rats to detect a ramp-like deflection of one whisker interspersed within ongoing white noise stimulation. Using generative modeling of behavior, we identify two task-related variables that are predictive of actual decisions. The first reflects task engagement on a local scale ("trial history": defined as the decisions and outcomes of a small number of past trials), whereas the other captures behavioral dynamics on a global scale ("satiation": slow dynamics of the response pattern along an entire session). Although satiation brought about a slow drift from Go to NoGo decisions during the session, trial history was related to local (trial-by-trial) patterning of Go and NoGo decisions. A second model that related the same predictors first to VPm spike responses, and from there to decisions, indicated that spiking, in contrast to behavior, is sensitive to trial history but relatively insensitive to satiation. Trial history influences VPm spike rates and regularity such that a history of Go decisions would predict fewer noise-driven spikes (but more regular ones), and more ramp-driven spikes. Neuronal activity in VPm, thus, is sensitive to local behavioral history, and may play an important role in higher-order cognitive signaling.SIGNIFICANCE STATEMENT It is an important question for perceptual and brain functions to find out whether cognitive signals modulate the sensory signal stream and if so, where in the brain this happens. This study provides evidence that decision and reward history can already be reflected in the ascending sensory pathway, on the level of first-order sensory thalamus. Cognitive signals are relayed very selectively such that only local trial history (spanning a few trials) but not global history (spanning an entire session) are reflected.

Validation of auditory detection response task method for assessing the attentional effects of cognitive load.

OBJECTIVES: There are 3 standardized versions of the Detection Response Task (DRT), 2 using visual stimuli (remote DRT and head-mounted DRT) and one using tactile stimuli. In this article, we present a study that proposes and validates a type of auditory signal to be used as DRT stimulus and evaluate the proposed auditory version of this method by comparing it with the standardized visual and tactile version. METHODS: This was a within-subject design study performed in a driving simulator with 24 participants. Each participant performed 8 2-min-long driving sessions in which they had to perform 3 different tasks: driving, answering to DRT stimuli, and performing a cognitive task (n-back task). Presence of additional cognitive load and type of DRT stimuli were defined as independent variables. DRT response times and hit rates, n-back task performance, and pupil size were observed as dependent variables. RESULTS: Significant changes in pupil size for trials with a cognitive task compared to trials without showed that cognitive load was induced properly. Each DRT version showed a significant increase in response times and a decrease in hit rates for trials with a secondary cognitive task compared to trials without. Similar and significantly better results in differences in response times and hit rates were obtained for the auditory and tactile version compared to the visual version. There were no significant differences in performance rate between the trials without DRT stimuli compared to trials with and among the trials with different DRT stimuli modalities. CONCLUSIONS: The results from this study show that the auditory DRT version, using the signal implementation suggested in this article, is sensitive to the effects of cognitive load on driver's attention and is significantly better than the remote visual and tactile version for auditory-vocal cognitive (n-back) secondary tasks.

Sonification of scalp-recorded frequency-following responses (FFRs) offers improved response detection over conventional statistical metrics.

BACKGROUND: The human frequency-following response (FFR) is a neurophonic potential used to examine the brain's encoding of complex sounds (e.g., speech) and monitor neuroplastic changes in auditory processing. Given the FFR's low amplitude (order of nanovolts), current conventions in literature recommend collecting several thousand trials to obtain a robust evoked response with adequate signal-to-noise ratio. NEW METHOD: By exploiting the spectrotemporal fidelity of the response, we examined whether auditory playbacks (i.e., "sonifications") of the neural FFR could be used to assess the quality of running recordings and provide a stopping rule for signal averaging. RESULTS AND COMPARISON WITH EXISTING METHOD: In a listening task over headphones, naïve listeners detected speech-evoked FFRs within ∼500 sweeps based solely on their perception of the presence/absence of a tonal quality to the response. Moreover, response detection based on aural sonifications offered similar and in some cases a 2-3× improvement over objective statistical techniques proposed in the literature (i.e., MI, SNR, MSC, F-test, Corr). CONCLUSIONS: Our findings suggest that simply listening to FFR responses (sonifications) might offer a rapid technique to monitor real-time EEG recordings and provide a stopping rule to terminate signal averaging that performs comparably or better than current approaches.

Human subthalamic nucleus - Automatic auditory change detection as a basis for action selection.

The subthalamic nucleus (STN) shapes motor behavior and is important for the initiation and termination of movements. Here we ask whether the STN takes aggregated sensory information into account, in order to exert this function. To this end, local field potentials (LFP) were recorded in eight patients suffering from Parkinson's disease and receiving deep-brain stimulation of the STN bilaterally. Bipolar recordings were obtained postoperatively from the externalized electrode leads. Patients were passively exposed to trains of auditory stimuli containing global deviants, local deviants or combined global/local deviants. The surface event-related potentials of the Parkinson's patients as well as those of 19 age-matched healthy controls were characterized by a mismatch negativity (MMN) that was most pronounced for the global/local double deviants and less prominent for the other deviant conditions. The left and right STN LFPs similarly were modulated by stimulus deviance starting at about 100ms post-stimulus onset. The MMN has been viewed as an index of an automatic auditory change detection system, more recently phrased in terms of predictive coding theory, which prepares the organism for attention shifts and for action. The LFP-data from the STN clearly demonstrate that the STN receives information on stimulus deviance, possibly as a means to bias the system to interrupt ongoing and to allow alternative actions.

Hierarchical differences in population coding within auditory cortex.

Most models of auditory cortical (AC) population coding have focused on primary auditory cortex (A1). Thus our understanding of how neural coding for sounds progresses along the cortical hierarchy remains obscure. To illuminate this, we recorded from two AC fields: A1 and middle lateral belt (ML) of rhesus macaques. We presented amplitude-modulated (AM) noise during both passive listening and while the animals performed an AM detection task ("active" condition). In both fields, neurons exhibit monotonic AM-depth tuning, with A1 neurons mostly exhibiting increasing rate-depth functions and ML neurons approximately evenly distributed between increasing and decreasing functions. We measured noise correlation (rnoise) between simultaneously recorded neurons and found that whereas engagement decreased average rnoise in A1, engagement increased average rnoise in ML. This finding surprised us, because attentive states are commonly reported to decrease average rnoise We analyzed the effect of rnoise on AM coding in both A1 and ML and found that whereas engagement-related shifts in rnoise in A1 enhance AM coding, rnoise shifts in ML have little effect. These results imply that the effect of rnoise differs between sensory areas, based on the distribution of tuning properties among the neurons within each population. A possible explanation of this is that higher areas need to encode nonsensory variables (e.g., attention, choice, and motor preparation), which impart common noise, thus increasing rnoise Therefore, the hierarchical emergence of rnoise-robust population coding (e.g., as we observed in ML) enhances the ability of sensory cortex to integrate cognitive and sensory information without a loss of sensory fidelity.NEW & NOTEWORTHY Prevailing models of population coding of sensory information are based on a limited subset of neural structures. An important and under-explored question in neuroscience is how distinct areas of sensory cortex differ in their population coding strategies. In this study, we compared population coding between primary and secondary auditory cortex. Our findings demonstrate striking differences between the two areas and highlight the importance of considering the diversity of neural structures as we develop models of population coding.

Detection of Tones Masked by Fluctuating Noise in Rat Auditory Cortex.

Sounds in natural settings always appear over a noisy background. The masked threshold of a pure tone in white noise (the lowest sound level at which the tone can be detected in the presence of masking noise) is largely determined by energy masking in the peripheral auditory system: when the signal-to-noise ratio within a frequency band centered at the target tone frequency is large enough, the tone can be detected. However, when additional information is supplied to the auditory system, for example in the presence of slow and coherent modulations of a broadband masker (often found in natural sounds), masked thresholds can be reduced substantially below the values expected from pure energy masking. Here, we used intracellular recordings in vivo in rat auditory cortex in order to study neuronal responses to pure tones masked by broadband maskers and amplitude-modulated broadband maskers. When tones were embedded in amplitude-modulated noise, detection thresholds were substantially lower than when embedded in unmodulated noise. The main cue for tone detection in modulated noise consisted of the suppression of the locking of the neuronal responses to the amplitude modulation of the noise by low-level tones.

Sensitivity and Bias in the Resolution of Stream-Bounce Stimuli.

The audiovisual stream-bounce effect refers to the resolution of ambiguous motion sequences as streaming or bouncing depending on the presence or absence of a sound. We used a novel experimental design and signal detection theory (SDT) to determine its sensory or decisional origins. To account for issues raised by Witt et al. on the interpretation of SDT results, we devised a pure signal detection (as opposed to signal discrimination) paradigm and measured participants' sensitivity and criterion when detecting a weak tone concurrent with objectively streaming or bouncing visual displays. We observed no change in sensitivity but a significant change in criterion with participants' criterion more liberal with bouncing targets than for streaming targets with. In a second experiment, we tasked participants with detecting a weak tone in noise while viewing an ambiguous motion sequence. They also indicated whether the targets appeared to stream or bounce. Participants' reported equivalent, mostly bouncing responses for hit and false alarm trials, and equivalent, mostly streaming responses for correct rejection and miss trials. Further, differences in participants' sensitivity and criterion measures for detecting tones in subjectively streaming compared to subjectively bouncing targets were inconsistent with sensory factors. These results support a decisional account of the sound-induced switch from mostly streaming to mostly bouncing responses in audiovisual stream-bounce displays.

Memory for temporally dynamic scenes.

Recognition memory was investigated for individual frames extracted from temporally continuous, visually rich film segments of 5-15 min. Participants viewed a short clip from a film in either a coherent or a jumbled order, followed by a recognition test of studied frames. Foils came either from an earlier or a later part of the film (Experiment 1) or from deleted segments selected from random cuts of varying duration (0.5 to 30 s) within the film itself (Experiment 2). When the foils came from an earlier or later part of the film (Experiment 1), recognition was excellent, with the hit rate far exceeding the false-alarm rate (.78 vs. 18). In Experiment 2, recognition was far worse, with the hit rate (.76) exceeding the false-alarm rate only for foils drawn from the longest cuts (15 and 30 s) and matching the false-alarm rate for the 5 s segments. When the foils were drawn from the briefest cuts (0.5 and 1.0 s), the false-alarm rate exceeded the hit rate. Unexpectedly, jumbling had no effect on recognition in either experiment. These results are consistent with the view that memory for complex visually temporal events is excellent, with the integrity unperturbed by disruption of the global structure of the visual stream. Disruption of memory was observed only when foils were drawn from embedded segments of duration less than 5 s, an outcome consistent with the view that memory at these shortest durations are consolidated with expectations drawn from the previous stream.

Go-activation endures following the presentation of a stop-signal: evidence from startle.

It has been proposed that, in a stop-signal task (SST), independent go- and stop-processes "race" to control behavior. If the go-process wins, an overt response is produced, whereas, if the stop-process wins, the response is withheld. One prediction that follows from this proposal is that, if the activation associated with one process is enhanced, it is more likely to win the race. We looked to determine whether these initiation and inhibition processes (and thus response outcomes) could be manipulated by using a startling acoustic stimulus (SAS), which has been shown to provide additional response activation. In the present study, participants were to respond to a visual go-stimulus; however, if a subsequent stop-signal appeared, they were to inhibit the response. The stop-signal was presented at a delay corresponding to a probability of responding of 0.4 (determined from a baseline block of trials). On stop-trials, a SAS was presented either simultaneously with the go-signal or stop-signal or 100, 150, or 200 ms following the stop-signal. Results showed that presenting a SAS during stop-trials led to an increase in probability of responding when presented with or following the stop-signal. The latency of SAS responses at the stop-signal + 150 ms and stop-signal + 200 ms probe times suggests that they would have been voluntarily inhibited but instead were involuntarily initiated by the SAS. Thus results demonstrate that go-activation endures even 200 ms following a stop-signal and remains accessible well after the response has been inhibited, providing evidence against a winner-take-all race between independent go- and stop-processes. NEW & NOTEWORTHY: In this study, a startling acoustic stimulus (SAS) was used to determine whether response outcome could be manipulated in a stop-signal task. Results revealed that presenting a SAS during stop-signal trials led to an increase in probability of responding even when presented 200 ms following the stop-signal. The latency of SAS responses indicates that go-activation remains accessible and modifiable well after the response is voluntarily inhibited, providing evidence against an irrevocable commitment to inhibition.

Comodulation Enhances Signal Detection via Priming of Auditory Cortical Circuits.

Acoustic environments are composed of complex overlapping sounds that the auditory system is required to segregate into discrete perceptual objects. The functions of distinct auditory processing stations in this challenging task are poorly understood. Here we show a direct role for mouse auditory cortex in detection and segregation of acoustic information. We measured the sensitivity of auditory cortical neurons to brief tones embedded in masking noise. By altering spectrotemporal characteristics of the masker, we reveal that sensitivity to pure tone stimuli is strongly enhanced in coherently modulated broadband noise, corresponding to the psychoacoustic phenomenon comodulation masking release. Improvements in detection were largest following priming periods of noise alone, indicating that cortical segregation is enhanced over time. Transient opsin-mediated silencing of auditory cortex during the priming period almost completely abolished these improvements, suggesting that cortical processing may play a direct and significant role in detection of quiet sounds in noisy environments. SIGNIFICANCE STATEMENT: Auditory systems are adept at detecting and segregating competing sound sources, but there is little direct evidence of how this process occurs in the mammalian auditory pathway. We demonstrate that coherent broadband noise enhances signal representation in auditory cortex, and that prolonged exposure to noise is necessary to produce this enhancement. Using optogenetic perturbation to selectively silence auditory cortex during early noise processing, we show that cortical processing plays a crucial role in the segregation of competing sounds.

Children use object-level category knowledge to detect changes in complex auditory scenes.

Children interact with and learn about all types of sound sources, including dogs, bells, trains, and human beings. Although it is clear that knowledge of semantic categories for everyday sights and sounds develops during childhood, there are very few studies examining how children use this knowledge to make sense of auditory scenes. We used a change deafness paradigm and an object-encoding task to investigate how children (6, 8, and 10 years of age) and adults process auditory scenes composed of everyday sounds (e.g., human voices, animal calls, environmental sounds, and musical instruments). Results indicated that although change deafness was present and robust at all ages, listeners improved at detecting changes with age. All listeners were less sensitive to changes within the same semantic category than to small acoustic changes, suggesting that, regardless of age, listeners relied heavily on semantic category knowledge to detect changes. Furthermore, all listeners showed less change deafness when they correctly encoded change-relevant objects (i.e., when they remembered hearing the changing object during the task). Finally, we found that all listeners were better at encoding human voices and were more sensitive to detecting changes involving the human voice. Despite poorer overall performance compared with adults, children detect changes in complex auditory scenes much like adults, using high-level knowledge about auditory objects to guide processing, with special attention to the human voice. (PsycINFO Database Record

Transitional Probabilities Are Prioritized over Stimulus/Pattern Probabilities in Auditory Deviance Detection: Memory Basis for Predictive Sound Processing.

UNLABELLED: Representations encoding the probabilities of auditory events do not directly support predictive processing. In contrast, information about the probability with which a given sound follows another (transitional probability) allows predictions of upcoming sounds. We tested whether behavioral and cortical auditory deviance detection (the latter indexed by the mismatch negativity event-related potential) relies on probabilities of sound patterns or on transitional probabilities. We presented healthy adult volunteers with three types of rare tone-triplets among frequent standard triplets of high-low-high (H-L-H) or L-H-L pitch structure: proximity deviant (H-H-H/L-L-L), reversal deviant (L-H-L/H-L-H), and first-tone deviant (L-L-H/H-H-L). If deviance detection was based on pattern probability, reversal and first-tone deviants should be detected with similar latency because both differ from the standard at the first pattern position. If deviance detection was based on transitional probabilities, then reversal deviants should be the most difficult to detect because, unlike the other two deviants, they contain no low-probability pitch transitions. The data clearly showed that both behavioral and cortical auditory deviance detection uses transitional probabilities. Thus, the memory traces underlying cortical deviance detection may provide a link between stimulus probability-based change/novelty detectors operating at lower levels of the auditory system and higher auditory cognitive functions that involve predictive processing. SIGNIFICANCE STATEMENT: Our research presents the first definite evidence for the auditory system prioritizing transitional probabilities over probabilities of individual sensory events. Forming representations for transitional probabilities paves the way for predictions of upcoming sounds. Several recent theories suggest that predictive processing provides the general basis of human perception, including important auditory functions, such as auditory scene analysis. Our results demonstrate that the memory traces underlying cortical deviance detection form a link between stimulus probability-based change/novelty detectors operating at lower levels of the auditory system and higher auditory cognitive functions that involve predictive processing.

Representational pseudoneglect for detecting changes to Rey-Osterrieth figures.

When dividing attention between the left and right sides of physical space, most individuals pay slightly more attention to the left side. This phenomenon, known as pseudoneglect, may also occur for the left and right sides of mental representations of stimuli. Representational pseudoneglect has been shown for the recall of real-world scenes and for simple, briefly presented stimuli. The current study sought to investigate the effect of exposure duration and complexity using adaptations of the Rey-Osterrieth figures. Undergraduates (n = 97) were shown a stimulus for 20 s and asked to remember it. Participants were then shown a probe and indicated whether it was the same or different. Results showed that, irrespective of whether an element was added or subtracted, changes on the left side of the remembered image were better detected. These results are consistent with representational pseudoneglect and demonstrate that this effect occurs for complex stimuli when presented for an extended period of time. Representation neglect is therefore unlikely to be the result of an initial saccade to the left-but could be related to the formation or recall of the representation.

Oscillatory power and functional connectivity in the speech change detection network.

We used passive and active oddball conditions with two types of acoustic contrasts, between speech syllables that cross phonetic boundaries (across-category, AC) and between those that do not cross them (within-category, WC), to explore the effects of meaningful speech contrasts on the dynamics of the neural network underlying the mismatch negativity (MMN) to the speech deviants. We found that easily detected AC deviants evoked a MMN response that lateralized to the left hemisphere, but the very difficult to detect WC deviants did not elicit a MMN response at all. Based on independent component analysis of the continuous EEG, we computed both power changes within, and functional connectivity (phase synchronization) between, brain regional sources comprising the neural network associated with the MMN for these speech stimuli. We found that for acoustic contrasts for which an MMN was generated, power changes suggested whether a particular brain region was more involved with processing standards or deviants. Moreover, we not only replicated the changes in functional connectivity between orbitofrontal cortex and superior temporal gyrus found in previous experiments, but also found significant increases in synchronization between those regions and regions of the left inferior frontal gyrus (Broca's area), which is thought to be involved in the storage and retrieval of phonological and semantic information.