Effects of neural oscillation power and phase on discrimination performance in a visual tilt illusion.

Neural oscillations reflect fluctuations in the relative excitation/inhibition of neural systems1,2,3,4,5 and are theorized to play a critical role in canonical neural computations6,7,8,9 and cognitive processes.10,11,12,13,14 These theories have been supported by findings that detection of visual stimuli fluctuates with the phase of oscillations prior to stimulus onset.15,16,17,18,19,20,21,22,23 However, null results have emerged in studies seeking to demonstrate these effects in visual discrimination tasks,24,25,26,27 raising questions about the generalizability of these phenomena to wider neural processes. Recently, we suggested that methodological limitations may mask effects of phase in higher-level sensory processing.28 To test the generality of phasic influences on perception requires a task that involves stimulus discrimination while also depending on early sensory processing. Here, we examined the influence of oscillation phase on the visual tilt illusion, in which a center grating has its perceived orientation biased away from the orientation of a surround grating29 due to lateral inhibitory interactions in early visual processing.30,31,32 We presented center gratings at participants' subjective vertical angle and had participants report whether the grating appeared tilted clockwise or counterclockwise from vertical on each trial while measuring their brain activity with electroencephalography (EEG). In addition to effects of alpha power and aperiodic slope, we observed robust associations between orientation perception and alpha and theta phase, consistent with fluctuating illusion magnitude across the oscillatory cycle. These results confirm that oscillation phase affects the complex processing involved in stimulus discrimination, consistent with its purported role in canonical computations that underpin cognition.

Behavior-relevant top-down cross-modal predictions in mouse neocortex.

Animals adapt to a constantly changing world by predicting their environment and the consequences of their actions. The predictive coding hypothesis proposes that the brain generates predictions and continuously compares them with sensory inputs to guide behavior. However, how the brain reconciles conflicting top-down predictions and bottom-up sensory information remains unclear. To address this question, we simultaneously imaged neuronal populations in the mouse somatosensory barrel cortex and posterior parietal cortex during an auditory-cued texture discrimination task. In mice that had learned the task with fixed tone-texture matching, the presentation of mismatched pairing induced conflicts between tone-based texture predictions and actual texture inputs. When decisions were based on the predicted rather than the actual texture, top-down information flow was dominant and texture representations in both areas were modified, whereas dominant bottom-up information flow led to correct representations and behavioral choice. Our findings provide evidence for hierarchical predictive coding in the mouse neocortex.

Targeted V1 comodulation supports task-adaptive sensory decisions.

Sensory-guided behavior requires reliable encoding of stimulus information in neural populations, and flexible, task-specific readout. The former has been studied extensively, but the latter remains poorly understood. We introduce a theory for adaptive sensory processing based on functionally-targeted stochastic modulation. We show that responses of neurons in area V1 of monkeys performing a visual discrimination task exhibit low-dimensional, rapidly fluctuating gain modulation, which is stronger in task-informative neurons and can be used to decode from neural activity after few training trials, consistent with observed behavior. In a simulated hierarchical neural network model, such labels are learned quickly and can be used to adapt downstream readout, even after several intervening processing stages. Consistently, we find the modulatory signal estimated in V1 is also present in the activity of simultaneously recorded MT units, and is again strongest in task-informative neurons. These results support the idea that co-modulation facilitates task-adaptive hierarchical information routing.

Neural sensitivity to facial identity and facial expression discrimination in adults with autism.

The fluent processing of faces can be challenging for autistic individuals. Here, we assessed the neural sensitivity to rapid changes in subtle facial cues in 23 autistic men and 23 age and IQ matched non-autistic (NA) controls using frequency-tagging electroencephalography (EEG). In oddball paradigms examining the automatic and implicit discrimination of facial identity and facial expression, base rate images were presented at 6 Hz, periodically interleaved every fifth image with an oddball image (i.e. 1.2 Hz oddball frequency). These distinctive frequency tags for base rate and oddball stimuli allowed direct and objective quantification of the neural discrimination responses. We found no large differences in the neural sensitivity of participants in both groups, not for facial identity discrimination, nor for facial expression discrimination. Both groups also showed a clear face-inversion effect, with reduced brain responses for inverted versus upright faces. Furthermore, sad faces generally elicited significantly lower neural amplitudes than angry, fearful and happy faces. The only minor group difference is the larger involvement of high-level right-hemisphere visual areas in NA men for facial expression processing. These findings are discussed from a developmental perspective, as they strikingly contrast with robust face processing deficits observed in autistic children using identical EEG paradigms.

Event-related potentials indicate differential neural reactivity to species and valence information in vocal stimuli in sleeping dogs.

Dogs live in a complex social environment where they regularly interact with conspecific and heterospecific partners. Awake dogs are able to process a variety of information based on vocalisations emitted by dogs and humans. Whether dogs are also able to process such information while asleep, is unknown. In the current explorative study, we investigated in N = 13 family dogs, neural response to conspecific and human emotional vocalisations. Data were recorded while dogs were asleep, using a fully non-invasive event-related potential (ERP) paradigm. A species (between 250-450 and 600-800 ms after stimulus onset) and a species by valence interaction (between 550 to 650 ms after stimulus onset) effect was observed during drowsiness. A valence (750-850 ms after stimulus onset) and a species x valence interaction (between 200 to 300 ms and 450 to 650 ms after stimulus onset) effect was also observed during non-REM specific at the Cz electrode. Although further research is needed, these results not only suggest that dogs neurally differentiate between differently valenced con- and heterospecific vocalisations, but they also provide the first evidence of complex vocal processing during sleep in dogs. Assessment and detection of ERPs during sleep in dogs appear feasible.

Duration discrimination: A diffusion decision modeling approach.

The human ability to discriminate the duration of two subsequently presented stimuli is often studied with tasks that involve a comparison between a standard stimulus (with fixed duration) and comparison stimuli (with varying durations). The performance in such tasks is influenced by the presentation order of these successively presented stimuli. The so-called Type A effect refers to the impact of presentation order on the point of subjective equality. The Type B effect describes effects of presentation order on the just-noticeable-difference. Cognitive models that account for these context effects assume that participants' duration estimation is influenced by the history of previously encountered stimuli. For example, the internal reference model assumes that the magnitude of a "typical" stimulus is represented by an internal reference. This internal reference evolves throughout an experiment and is updated on every trial. Different recent models have in common that they describe how the internal reference is computed but are agnostic to the decision process itself. In this study, we develop a new model that incorporates the mechanisms of perceptual discrimination models into a diffusion model. The diffusion model focuses on the dynamics of the decision process itself and accounts for choice and response times based on a set of latent cognitive variables. We show that our model accurately predicts the accuracy and response time distribution in a classical duration discrimination task. Further, model parameters were sensitive to the Type A and B effect. The proposed model opens up new opportunities for studying human discrimination performance (e.g., individual differences).

Rule-based and stimulus-based cues bias auditory decisions via different computational and physiological mechanisms.

Expectations, such as those arising from either learned rules or recent stimulus regularities, can bias subsequent auditory perception in diverse ways. However, it is not well understood if and how these diverse effects depend on the source of the expectations. Further, it is unknown whether different sources of bias use the same or different computational and physiological mechanisms. We examined how rule-based and stimulus-based expectations influenced behavior and pupil-linked arousal, a marker of certain forms of expectation-based processing, of human subjects performing an auditory frequency-discrimination task. Rule-based cues consistently biased choices and response times (RTs) toward the more-probable stimulus. In contrast, stimulus-based cues had a complex combination of effects, including choice and RT biases toward and away from the frequency of recently presented stimuli. These different behavioral patterns also had: 1) distinct computational signatures, including different modulations of key components of a novel form of a drift-diffusion decision model and 2) distinct physiological signatures, including substantial bias-dependent modulations of pupil size in response to rule-based but not stimulus-based cues. These results imply that different sources of expectations can modulate auditory processing via distinct mechanisms: one that uses arousal-linked, rule-based information and another that uses arousal-independent, stimulus-based information to bias the speed and accuracy of auditory perceptual decisions.

Enhancing performance with multisensory cues in a realistic target discrimination task.

Making decisions is an important aspect of people's lives. Decisions can be highly critical in nature, with mistakes possibly resulting in extremely adverse consequences. Yet, such decisions have often to be made within a very short period of time and with limited information. This can result in decreased accuracy and efficiency. In this paper, we explore the possibility of increasing speed and accuracy of users engaged in the discrimination of realistic targets presented for a very short time, in the presence of unimodal or bimodal cues. More specifically, we present results from an experiment where users were asked to discriminate between targets rapidly appearing in an indoor environment. Unimodal (auditory) or bimodal (audio-visual) cues could shortly precede the target stimulus, warning the users about its location. Our findings show that, when used to facilitate perceptual decision under time pressure, and in condition of limited information in real-world scenarios, spoken cues can be effective in boosting performance (accuracy, reaction times or both), and even more so when presented in bimodal form. However, we also found that cue timing plays a critical role and, if the cue-stimulus interval is too short, cues may offer no advantage. In a post-hoc analysis of our data, we also show that congruency between the response location and both the target location and the cues, can interfere with the speed and accuracy in the task. These effects should be taken in consideration, particularly when investigating performance in realistic tasks.

Response Time Distributions and the Accumulation of Visual Evidence in Freely Moving Mice.

Response time (RT) distributions are histograms of the observed RTs for discriminative choices, comprising a rich source of empirical information to study perceptual processes. The drift-diffusion model (DDM), a mathematical formulation predicting decision tasks, reproduces the RT distributions, contributing to our understanding of these processes from a theoretical perspective. Notably, although the mouse is a popular model system for studying brain function and behavior, little is known about mouse perceptual RT distributions, and their description from an information-accumulation perspective. We combined an automated visual discrimination task with pharmacological micro-infusions of targeted brain regions to acquire thousands of responses from freely-moving adult mice. Both choices and escape latencies showed a strong dependency on stimulus discriminability. By applying a DDM fit to our experimental data, we found that the rate of incoming evidence (drift rate) increased with stimulus contrast but was reversibly impaired when inactivating the primary visual cortex (V1). Other brain regions involved in the decision-making process, the posterior parietal cortex (PPC) and the frontal orienting fields (FOF), also influenced relevant parameters from the DDM. The large number of empirical observations that we collected for this study allowed us to achieve accurate convergence for the model fit. Therefore, changes in the experimental conditions were mirrored by changes in model parameters, suggesting the participation of relevant brain areas in the decision-making process. This approach could help interpret future studies involving attention, discrimination, and learning in adult mice.

Multisensory interactions on auditory and somatosensory information in expert pianists.

Fine-tuned sensory functions typically characterize skilled individuals. Although numerous studies demonstrated enhanced unimodal sensory functions at both neural and behavioral levels in skilled individuals, little is known about their multisensory interaction function, especially multisensory integration and selective attention that involve volitional control of information derived from multiple sensory organs. In the current study, expert pianists and musically untrained individuals performed five sets of intensity discrimination tasks at the auditory and somatosensory modalities with different conditions: (1) auditory stimulus, (2) somatosensory stimulus, (3) congruent auditory and somatosensory stimuli (i.e., multisensory integration), (4) auditory and task-irrelevant somatosensory stimuli, and (5) somatosensory and task-irrelevant auditory stimuli. In the fourth and fifth conditions, participants were instructed to ignore a task-irrelevant stimulus and to pay attention to a task-relevant stimulus (i.e., selective attention), respectively. While the discrimination perception was superior in the condition (3) compared to the better one of the individual unimodal conditions only in the pianists, the task-irrelevant somatosensory stimulus worsened the auditory discrimination more in the pianists than the nonmusicians. These findings indicate unique multisensory interactions in expert pianists, which enables pianists to efficiently integrate the auditory and somatosensory information, but exacerbates top-down selective inhibition of somatosensory information during auditory processing.

Existing function in primary visual cortex is not perturbed by new skill acquisition of a non-matched sensory task.

Acquisition of new skills has the potential to disturb existing network function. To directly assess whether previously acquired cortical function is altered during learning, mice were trained in an abstract task in which selected activity patterns were rewarded using an optical brain-computer interface device coupled to primary visual cortex (V1) neurons. Excitatory neurons were longitudinally recorded using 2-photon calcium imaging. Despite significant changes in local neural activity during task performance, tuning properties and stimulus encoding assessed outside of the trained context were not perturbed. Similarly, stimulus tuning was stable in neurons that remained responsive following a different, visual discrimination training task. However, visual discrimination training increased the rate of representational drift. Our results indicate that while some forms of perceptual learning may modify the contribution of individual neurons to stimulus encoding, new skill learning is not inherently disruptive to the quality of stimulus representation in adult V1.

Emergent reliability in sensory cortical coding and inter-area communication.

Reliable sensory discrimination must arise from high-fidelity neural representations and communication between brain areas. However, how neocortical sensory processing overcomes the substantial variability of neuronal sensory responses remains undetermined1-6. Here we imaged neuronal activity in eight neocortical areas concurrently and over five days in mice performing a visual discrimination task, yielding longitudinal recordings of more than 21,000 neurons. Analyses revealed a sequence of events across the neocortex starting from a resting state, to early stages of perception, and through the formation of a task response. At rest, the neocortex had one pattern of functional connections, identified through sets of areas that shared activity cofluctuations7,8. Within about 200 ms after the onset of the sensory stimulus, such connections rearranged, with different areas sharing cofluctuations and task-related information. During this short-lived state (approximately 300 ms duration), both inter-area sensory data transmission and the redundancy of sensory encoding peaked, reflecting a transient increase in correlated fluctuations among task-related neurons. By around 0.5 s after stimulus onset, the visual representation reached a more stable form, the structure of which was robust to the prominent, day-to-day variations in the responses of individual cells. About 1 s into stimulus presentation, a global fluctuation mode conveyed the upcoming response of the mouse to every area examined and was orthogonal to modes carrying sensory data. Overall, the neocortex supports sensory performance through brief elevations in sensory coding redundancy near the start of perception, neural population codes that are robust to cellular variability, and widespread inter-area fluctuation modes that transmit sensory data and task responses in non-interfering channels.

Measurement of the exploration-exploitation response of dogs through a concurrent visual discrimination task.

In many species, the allocation of exploration and exploitation responses to environmental stimuli is important for survival. In this exploratory study, we determined whether dogs (Canis familiaris) explored novel stimuli in a visual discrimination task using food reinforcers. Initially, the dogs were trained with two pairs of simultaneous visual discrimination tasks. Having achieved the learning criterion, the dogs were presented with a pair of stimuli including a novel stimulus and a previously reinforced stimulus in the probe trials (familiar stimulus). Dogs were reinforced by 50% for novel stimuli and 100% for familiar stimuli. The proportions of responses to novel and familiar stimuli in the probe trials were considered to reflect the propensity for exploration and exploitation, respectively. The five dogs tested selected the novel stimulus more frequently (in 22 of the 30 probe trials; binomial test, P = 0.016). Therefore, dogs prefer novel stimuli over familiar ones, suggesting that this species, which is less neophobic than wolves (Canis lupus), would likely allocate more responses to exploration. Comparisons among breeds or with wolves are warranted in future studies.

Perceptual decisions and oculomotor responses rely on temporally distinct streams of evidence.

Perceptual decisions often require the integration of noisy sensory evidence over time. This process is formalized with sequential sampling models, where evidence is accumulated up to a decision threshold before a choice is made. Although intuition suggests that decision formation must precede the preparation of a motor response (i.e., the action used to communicate the choice), neurophysiological findings have suggested that these two processes might be one and the same. To test this idea, we developed a reverse-correlation protocol in which the visual stimuli that influence decisions can be distinguished from those guiding motor responses. In three experiments, we found that the temporal weighting function of oculomotor responses did not overlap with the relatively early weighting function of stimulus properties having an impact on decision formation. These results support a timeline in which perceptual decisions are formed, at least in part, prior to the preparation of a motor response.

Dynamics of Visual Perceptual Decision-Making in Freely Behaving Mice.

The temporal dynamics of perceptual decisions offer a key window into the cognitive processes contributing to decision-making. Investigating perceptual dynamics in a genetically tractable animal model can facilitate the subsequent unpacking of the underlying neural mechanisms. Here, we investigated the time course as well as fundamental psychophysical constants governing visual perceptual decision-making in freely behaving mice. We did so by analyzing response accuracy against reaction time (RT), i.e., conditional accuracy, in a series of two-alternative forced choice (2-AFC) orientation discrimination tasks in which we varied target size, luminance, duration, and presence of a foil. Our results quantified two distinct stages in the time course of mouse visual decision-making: a "sensory encoding" stage in which conditional accuracy exhibits a classic trade-off with response speed, and a subsequent "short-term memory (STM)-dependent" stage in which conditional accuracy exhibits a classic asymptotic decay following stimulus offset. We estimated the duration of visual sensory encoding as 200-320 ms across tasks, the lower bound of the duration of STM as ∼1700 ms, and the briefest duration of visual stimulus input that is informative as ≤50 ms. Separately, by varying stimulus onset delay, we demonstrated that the conditional accuracy function (CAF) and RT distribution can be independently modulated, and found that the duration for which mice naturally withhold from responding is a quantitative metric of impulsivity. Taken together, our results establish a quantitative foundation for investigating the neural circuit bases of visual decision dynamics in mice.

Making heads or tails of body inversion effects: Do heads matter?

Observers are better at discriminating upright bodies than inverted bodies, and this body inversion effect (BIE) is reliable with whole figures (bodies with heads), but not with bodies presented without heads or the heads occluded suggesting that heads may be key to BIEs. Some studies present whole figures and bodies without heads between groups, and BIEs are not found for bodies without heads [1]. Other studies present whole figures and bodies without heads in the same blocks and BIEs are found with bodies without heads [2]. Does seeing the heads of whole figures induce BIEs in bodies without heads? Here, participants discriminated bodies with either whole figures and bodies without heads presented within blocks, or in separate blocks with bodies without heads presented first. We tested body identity and posture discrimination and measured participants' gaze. BIEs were found with whole figures and bodies without heads in both identity and posture discrimination, and in both study designs. However, efficiency scores were better for the whole figures than the bodies without heads, but only when whole figures appeared in separate blocks. The magnitude of the BIE was overall stronger for whole figures compared to bodies without heads, but only in identity discrimination. BIE magnitudes were similar in the identity and posture tasks. Participants were better at identity discrimination, yet, there was greater looking at heads and less at bodies. During posture discrimination, greater looking at bodies and less at heads was associated with better performance. Faces might influence BIEs but are not essential. Configural representations of bodies without heads are sufficient for BIEs in posture and identity discrimination.

A hippocampus dependent neural circuit loop underlying the generation of auditory mismatch negativity.

Extracting relevant information and transforming it into appropriate behavior, is a fundamental brain function, and requires the coordination between the sensory and cognitive systems, however, the underlying mechanisms of interplay between sensory and cognition systems remain largely unknown. Here, we developed a mouse model for mimicking human auditory mismatch negativity (MMN), a well-characterized translational biomarker for schizophrenia, and an index of early auditory information processing. We found that a subanesthetic dose of ketamine decreased the amplitude of MMN in adult mice. Using pharmacological and chemogenetic approaches, we identified an auditory cortex-entorhinal cortex-hippocampus neural circuit loop that is required for the generation of MMN. In addition, we found that inhibition of dCA1→MEC circuit impaired the auditory related fear discrimination. Moreover, we found that ketamine induced MMN deficiency by inhibition of long-range GABAergic projection from the CA1 region of the dorsal hippocampus to the medial entorhinal cortex. These results provided circuit insights for ketamine effects and early auditory information processing. As the entorhinal cortex is the interface between the neocortex and hippocampus, and the hippocampus is critical for the formation, consolidation, and retrieval of episodic memories and other cognition, our results provide a neural mechanism for the interplay between the sensory and cognition systems.

Rabbits use both spectral and temporal cues to discriminate the fundamental frequency of harmonic complexes with missing fundamentals.

The pitch of harmonic complex tones (HCTs) common in speech, music, and animal vocalizations plays a key role in the perceptual organization of sound. Unraveling the neural mechanisms of pitch perception requires animal models, but little is known about complex pitch perception by animals, and some species appear to use different pitch mechanisms than humans. Here, we tested rabbits' ability to discriminate the fundamental frequency (F0) of HCTs with missing fundamentals, using a behavioral paradigm inspired by foraging behavior in which rabbits learned to harness a spatial gradient in F0 to find the location of a virtual target within a room for a food reward. Rabbits were initially trained to discriminate HCTs with F0s in the range 400-800 Hz and with harmonics covering a wide frequency range (800-16,000 Hz) and then tested with stimuli differing in spectral composition to test the role of harmonic resolvability (experiment 1) or in F0 range (experiment 2) or in both F0 and spectral content (experiment 3). Together, these experiments show that rabbits can discriminate HCTs over a wide F0 range (200-1,600 Hz) encompassing the range of conspecific vocalizations and can use either the spectral pattern of harmonics resolved by the cochlea for higher F0s or temporal envelope cues resulting from interaction between unresolved harmonics for lower F0s. The qualitative similarity of these results to human performance supports the use of rabbits as an animal model for studies of pitch mechanisms, providing species differences in cochlear frequency selectivity and F0 range of vocalizations are taken into account.NEW & NOTEWORTHY Understanding the neural mechanisms of pitch perception requires experiments in animal models, but little is known about pitch perception by animals. Here we show that rabbits, a popular animal in auditory neuroscience, can discriminate complex sounds differing in pitch using either spectral cues or temporal cues. The results suggest that the role of spectral cues in pitch perception by animals may have been underestimated by predominantly testing low frequencies in the range of human voice.

Ongoing neural oscillations influence behavior and sensory representations by suppressing neuronal excitability.

The ability to process and respond to external input is critical for adaptive behavior. Why, then, do neural and behavioral responses vary across repeated presentations of the same sensory input? Ongoing fluctuations of neuronal excitability are currently hypothesized to underlie the trial-by-trial variability in sensory processing. To test this, we capitalized on intracranial electrophysiology in neurosurgical patients performing an auditory discrimination task with visual cues: specifically, we examined the interaction between prestimulus alpha oscillations, excitability, task performance, and decoded neural stimulus representations. We found that strong prestimulus oscillations in the alpha+ band (i.e., alpha and neighboring frequencies), rather than the aperiodic signal, correlated with a low excitability state, indexed by reduced broadband high-frequency activity. This state was related to slower reaction times and reduced neural stimulus encoding strength. We propose that the alpha+ rhythm modulates excitability, thereby resulting in variability in behavior and sensory representations despite identical input.

Prestimulus alpha power but not phase influences visual discrimination of long-duration visual stimuli.

Occipital oscillations in the alpha band are closely related to visual perception and attention. In multiple studies, increased alpha power has been shown to reduce detection rates of hard-to-detect visual stimuli. Recent studies explain this finding by a shift in perceptual bias. Moreover, the phase of alpha oscillations prior to stimulus onset appears to be critical for the detection of visual stimuli. This is explained by a shift in cortical excitability over the course of each alpha cycle. However, prior studies often used short presentation times of visual stimuli at the perceptual threshold. Here, we use longer presentation times to elucidate whether the same mechanisms hold for the perception of salient but challenging visual stimuli presented for up to 1,500 ms. To this end, we presented participants with hard to distinguish but salient upright or tilted Gaussian gratings in a two-alternative forced choice task, while recording occipital electroencephalographic activity. Previous reports link alpha power to stimulus detection hit rates, and we found that low prestimulus power at the individual alpha frequency relates to higher perceptual accuracy. Contrary to recent findings, we neither found an influence of alpha power on criterion, nor an influence of alpha phase on perception or response speed. We argue that longer presentation times might attenuate a possible response bias, and increased excitability might sharpen the discrimination ability, thereby leading to increased perceptual accuracy and unaffected response criterion.