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Treue, S.

Publications and source records attributed to Treue, S..

14 recordsLinked to original sources

Multivariate Transfer Entropy Quantifies Information Transfer Between Dyadic Partners During Real-Time Perceptual Decision-Making

1Many social behaviours unfold continuously in time, yet most studies of social influence rely on discrete, trial-based paradigms. To quantify how humans actually integrate sensory and social signals during ongoing perceptual decision-making we here apply an information-theoretic analysis to data obtained with the Continuous Perceptual Report (CPR) paradigm. In the CPR task, pairs of participants tracked a dynamic random-dot motion stimulus, continuously reporting perceived direction and their confidence. Crucially, each participant had access to their partners moment-by-moment direction and confidence reports embedded within the stimulus display. We quantified information flow between the stimulus and behavioural responses using multivariate transfer entropy, allowing us to detect whether participants acquired additional information from their partner once stimulus information had been received and integrated it into their behavioural response. We show that real-time social interactions predominantly occur within matching behavioural dimensions: partners perceptual choices influence participants own choices, and partners confidence influences participants confidence. Using both, more stimulus and social information contributed to improved task performance, and participants selectively acquired more information from better-performing partners. Crucially, information integration was flexibly modulated by stimulus reliability: as sensory evidence became noisier, participants relied more on social information, but only when interacting with a highly reliable (e.g. computer-controlled) partner. Latency analyses further revealed that participants responded faster to changes in their partners perceptual choices of direction than to changes in stimulus direction. They also responded more slowly to changes in their partners confidence than to changes in their partners choice of direction. Together, these findings demonstrate that humans dynamically and adaptively integrate social information in a time-continuous manner, and they establish multivariate information-theoretic analyses as a powerful framework for studying real-time social cognition.

animal behavior and cognition↗

Single neuron diversity supports area functional specialization along the visual cortical pathways

Humans and other primates have specialized visual pathways composed of interconnected cortical areas. The input area V1 contains neurons that encode basic visual features, whereas downstream in the lateral prefrontal cortex (LPFC) neurons acquire tuning for novel complex feature associations. It has been assumed that each cortical area is composed of repeatable neuronal subtypes, and variations in synaptic strength and connectivity patterns underlie functional specialization. Here we test the hypothesis that diversity in the intrinsic make-up of single neurons contributes to area specialization along the visual pathways. We measured morphological and electrophysiological properties of single neurons in areas V1 and LPFC of marmosets. Excitatory neurons in LPFC were larger, less excitable, and fired broader spikes than V1 neurons. Some inhibitory fast spiking interneurons in the LPFC had longer axons and fired spikes with longer latencies and a more depolarized action potential trough than in V1. Intrinsic bursting was found in subpopulations of both excitatory and inhibitory LPFC but not V1 neurons. The latter may favour temporal summation of spikes and therefore enhanced synaptic plasticity in LPFC relative to V1. Our results show that specialization within the primate visual system permeates the most basic processing level, the single neuron.

neuroscience↗

Spike frequency adaptation in primate lateral prefrontal cortex neurons results from interplay between intrinsic properties and circuit dynamics

Recordings of cortical neurons isolated from brain slices and dissociated from their networks, display intrinsic spike frequency adaptation (I-SFA) to a constant current input. Interestingly, extracellular recordings in behaving subjects also show extrinsic-SFA (E-SFA) in response to sustained visual stimulation. Because neurons are isolated from brain networks in slice recordings, it is challenging to infer how I-SFA contributes to E-SFA in interconnected brains during behavior. To investigate this, we recorded responses of macaque lateral prefrontal cortex neurons in vivo during a visually guided saccade task and in acute brain slices in vitro. Broad spiking (BS) putative pyramidal cells and narrow spiking (NS) putative inhibitory interneurons exhibited E-SFA in vivo. In acute brain slices, both cell types displayed I-SFA though their magnitudes differed. To investigate how in vitro I-SFA contributes to in vivo E-SFA, we developed a data-driven hybrid circuit model in which local NS neurons are driven by BS input. We observed that model NS cell responses show longer SFA than observed in vivo. Introducing inhibition of NS cells to the model circuit removed this discrepancy. Our results indicate that both I-SFA and inhibitory circuit dynamics contribute to E-SFA in LPFC neurons. They highlight the contribution of single neuron and network dependent computations to neural activity underlying behavior.

neuroscience↗

Confidence over competence: Real-time integration of social information in human continuous perceptual decision-making

Human perceptual decision-making is susceptible to social influences. To determine if and how individuals opportunistically integrate real-time social information about noisy stimuli into their judgment, we tracked perceptual accuracy and confidence in social (dyadic) and non-social (solo) settings using a novel continuous perceptual report (CPR) task with peri-decision wagering. In the dyadic setting, most participants showed a higher degree of perceptual confidence. In contrast, average accuracy did not improve compared to solo performance. Underlying these net effects, partners in a dyad exhibit mutual convergence of accuracy and confidence, benefiting less competent or confident individuals, at the expense of the better-performing partner. In conclusion, real-time social information asymmetrically shapes human perceptual decision-making, with most dyads expressing more confidence without a matching gain in overall competence.

neuroscience↗

Bilateral field advantage of spatial attention in macaque lateral prefrontal cortex

Allocating visual attention to behaviorally relevant stimuli is easier when distractors are located in the opposite visual hemifield relative to when they are in the same hemifield. The neural mechanisms underlying this bilateral field advantage remains unclear. We documented this effect in two macaques performing a covert spatial attention task in two different conditions: when the target and distracter were positioned in different hemifields (across condition), and when they were positioned on the top and bottom quadrants within the same visual hemifield (within condition). The animals behavioral performance at detecting a change in the attended stimulus was higher in the across relative to the within condition. We recorded the responses of lateral prefrontal cortex (LPFC, area 8A) neurons in one animal. The proportion of LPFC neurons encoding the allocation of attention was larger in the across relative to the within condition. The latter was accompanied by an increase in the ability of single neurons to discriminate the allocation of attention in the across relative to the within condition. Finally, we used linear classifiers to decode the allocation of attention from the activity of neuronal ensembles and found a similar bilateral field advantage in decoding performance in the across relative to the within condition. Our finding provides a neural correlate of the bilateral field advantage reported in behavioral studies of attention and suggest that the effect may originate within the LPFC circuitry.

neuroscience↗

Behavioral relevance of category selectivity revealed by human ECoG data

Object recognition is a crucial brain function that involves a complex interplay between various brain regions. However, the behavioral relevance of functional interactions between these regions remains largely unexplored. In this study, we examined the functional interactions between different brain regions during object recognition using intracranial electrocorticography (ECoG) recordings in subjects diagnosed with pharmacologically intractable epilepsy. We computed the phase locking value (PLV) between different brain areas and its category selectivity, and assessed its behavioral relevance by comparing correctly and incorrectly performed trials. Our results revealed that phase locking between brain regions varies across different object categories and that this variability significantly influences the perceptual behavior of subjects. Importantly, we found that the behavioral relevance of these interactions is spatially organized, with long-range (global) connections being more behaviorally relevant for the frontal lobe and local connections being more crucial for the occipital lobe. These findings underscore the unique roles of different brain areas in object recognition and pave the way for more nuanced explorations of the interplay between brain regions in object recognition and other cognitive functions.

neuroscience↗

Rhythmic entrainment of saccadic eye-movements in macaque FEF

Saccadic eye movements play a key role in gaining information about the surrounding environment. However, the neural mechanisms underlying the timing of these eye movements remain poorly understood. Here, we investigated the entrainment of saccadic eye movement by oscillatory neural activities in rhesus monkeys performing a visual foraging task. We found that saccades are phase-locked to beta LFP oscillations (16-22 Hz) in the frontal eye field (FEF), 100 ms before saccade onset, supporting a causal role of these oscillations in saccade timing. Furthermore, we show that the alignment between saccades and FEF LFPs varies, depending on the spatial relationship between the saccade target and the response field (RF) of neurons in the FEF. These findings suggest that the phase of the oscillatory neural activities determines the timing and direction of saccades.

neuroscience↗

Phase of neural oscillations as a reference frame for attention-based routing in visual cortex

Selective attention allows the brain to efficiently process the image projected onto the retina, selectively focusing neural processing resources on behaviorally relevant visual information. While previous studies have documented the crucial role of the action potential rate of single neurons in relaying such information, little is known about how the activity of single neurons relative to their neighboring network contributes to the efficient representation of attended stimuli and transmission of this information to downstream areas. Here, we show in the dorsal visual pathway of monkeys (medial superior temporal (MST) area) that neurons fire spikes preferentially at a specific phase of the ongoing population beta (~20 Hz) oscillations of the surrounding local network. This preferred spiking phase shifts towards a later phase when monkeys selectively attend towards (rather than away from) the receptive field of the neuron. This shift of the locking phase is positively correlated with the speed at which animals report a visual change. Furthermore, our computational modelling suggests that neural networks can manipulate the preferred phase of coupling by imposing differential synaptic delays on postsynaptic potentials. This distinction between the locking phase of neurons activated by the spatially attended stimulus vs. that of neurons activated by the unattended stimulus, may enable the neural system to discriminate relevant from irrelevant sensory inputs and consequently filter out distracting stimuli information by aligning the spikes which convey relevant/irrelevant information to distinct phases linked to periods of better/worse perceptual sensitivity for higher cortices. This strategy may be used to reserve the narrow windows of highest perceptual efficacy to the processing of the most behaviorally relevant information, ensuring highly efficient responses to attended sensory events.

animal behavior and cognition↗

Feature-based gating of cortical information transmission

In highly developed visual systems, spatial- and feature-based attentional modulation interact to prioritize relevant information and suppress irrelevant details. We investigated the specific role and integration of these two attentional mechanisms in visual cortical area MST of rhesus monkeys. We show that spatial attention acts as a gate for information processing by providing unimpeded high-gain pass-through processing for all sensory information from attended visual locations. Feature-based attentional enhancement does not only show the known dependency on a match between the attended feature and a given cells selectivity, but surprisingly is restricted to those features for which a given cell contributes to perception. This necessitates a refinement of the feature-similarity gain model of attention and documents highly optimized attentional gating of sensory information for cortical processing. This gating is shaped by neuronal sensory preferences, behavioral relevance, and the causal link to perception of neurons that process this visual input.

neuroscience↗

Feature-based attention induces surround suppression during the perception of visual motion

Feature-based attention prioritizes the processing of the attended feature while strongly suppressing the processing of nearby ones. This creates a non-linearity or attentional suppressive surround predicted by the Selective Tuning model of visual attention. However, previously reported effects of feature-based attention on neuronal responses are linear, e.g., feature-similarity gain. Here, we investigated this apparent contradiction by neurophysiological and psychophysical approaches. Responses of motion direction-selective neurons in area MT/MST of monkeys were recorded during a motion task. When attention was allocated to a stimulus moving in the neurons preferred direction response tuning curves showed its minimum for directions 60-90 degrees away from the preferred direction, an attentional suppressive surround. This effect was modeled via the interaction of two Gaussian fields representing excitatory narrowly-tuned and inhibitory widely-tuned inputs into a neuron, with feature-based attention predominantly increasing the gain of inhibitory inputs. We further showed using a motion repulsion paradigm in humans that feature-based attention produces a similar non-linearity on motion discrimination performance. Our results link the gain modulation of neuronal inputs and tuning curves examined through the feature-similarity gain lens to the attentional impact on neural population responses predicted by the Selective Tuning model, providing a unified framework for the documented effects of feature-based attention on neuronal responses and behavior.

neuroscience↗

Human and macaque pairs coordinate differently in a dyadic decision game with face-to-face action visibility

Many real-world decisions in social contexts are made while observing a partners actions. To study dynamic interactions during such decisions, we developed a setup where two agents seated face-to-face engage in game-theoretical tasks on a shared transparent touchscreen display ("transparent games"). We compared human and macaque pairs in a transparent version of the coordination game "Bach-or-Stravinsky", which entails a conflict about which of two individually-preferred opposing options to choose to achieve coordination. Most human pairs developed coordinated behavior and adopted dynamic turn-taking to equalize the payoffs. All macaque pairs converged on simpler, static coordination. Remarkably, two animals learned to coordinate dynamically after training with a human confederate. This pair selected the faster agents preferred option, exhibiting turn-taking behavior that was captured by modeling the visibility of the partners action before ones own movement. Such competitive turn-taking was unlike the prosocial turn-taking in humans, who equally often initiated switches to and from their preferred option. Thus, the dynamic coordination is not restricted to humans, but can occur on the background of different social attitudes and cognitive capacities in rhesus monkeys. Overall, our results illustrate how action visibility promotes emergence and maintenance of coordination when agents can observe and time their mutual actions.

neuroscience↗

Development of a monkey avatar to study social perception in macaques

Following the expanding use and applications of virtual reality in every-day life, dynamic virtual stimuli are of increasing interest in cognitive studies. They allow for control of features such as gaze, expression and movement, which may help to overcome limitations of using either static or poorly controlled real stimuli. In using virtual stimuli however, one must be careful to avoid the uncanny valley effect - where realistic stimuli can be perceived as eerie, and induce an aversion response. At the same time, it is important to establish whether responses to virtual stimuli mirror responses to depictions of a real conspecific. In the current study, we describe the development of a new avatar with realistic features for nonhuman primates, the primatar. As a first step towards validation, we assessed how monkeys respond to images of this avatar compared to images of real monkeys, and an unrealistic avatar. We also compared responses between original images and scrambled as well as obfuscated versions of these images. We measured looking time to images in six free moving long-tailed macaques (Macaca fascicularis) and eye movement exploration behaviour in three rhesus macaques (Macaca mulatta). Both groups showed more of such signs of overt attention to original images than scrambled or obfuscated images. In addition, we assessed whether the realistic avatar created an uncanny valley effect through decreased looking time, finding that in both groups, monkeys did not differentiate between real, realistic or unrealistic images. These results provide support for further development of our avatar for use in social cognition studies, and more generally for cognitive research with virtual stimuli in nonhuman primates. Future research needs to shed light on the source of the inconsistent findings for the uncanny valley effect in macaques, to elucidate the roots of this mechanism in humans.

animal behavior and cognition↗

Attention enhances LFP phase coherence in macaque visual cortex, improving sensory processing

Attention selectively routes the most behaviorally relevant information among the vast pool of sensory inputs through cortical regions. Previous studies have shown that visual attention samples the surrounding stimuli periodically. However, the neural mechanism underlying this sampling in the sensory cortex, and whether the brain actively uses these rhythms, has remained elusive. Here, we hypothesize that selective attention controls the phase of oscillatory synaptic activities to efficiently process the relevant information in the brain. We document an attentional modulation of pre-stimulus inter-trial phase coherence (a measure of deviation between instantaneous phases of trials) at low frequencies in macaque visual area MT. Our data reveal that phase coherence increases when attention is deployed towards the receptive field of the recorded neural population. We further show that the attentional enhancement of phase coherence is positively correlated with the attentional modulation of stimulus induced firing rate, and importantly, a higher phase coherence leads to a faster behavioral response. Our results suggest a functional utilization of intrinsic neural oscillatory activities for better processing upcoming environmental stimuli, generating the optimal behavior.

neuroscience↗

Using imaging photoplethysmography for heart rate estimation in non-human primates

For humans and for non-human primates heart rate is a reliable indicator of an individuals current physiological state, with applications ranging from health checks to experimental studies of cognitive and emotional state. In humans, changes in the optical properties of the skin tissue correlated with cardiac cycles (imaging photoplethysmogram, iPPG) allow non-contact estimation of heart rate by its proxy, pulse rate. Yet, there is no established simple and non-invasive technique for pulse rate measurements in awake and behaving animals. Using iPPG, we here demonstrate that pulse rate in rhesus monkeys can be accurately estimated from facial videos. We computed iPPGs from seven color facial videos of three awake head-stabilized rhesus monkeys. Pulse rate estimated from iPPGs was in good agreement with reference data from a pulse-oximeter with error of pulse rate estimation below 5% for 82% of all epochs, and below 10% for 98% of the epochs. We conclude that iPPG allows non-invasive and non-contact estimation of pulse rate in non-human primates, which is useful for physiological studies and can be used toward welfare-assessment of non-human primates in research.

bioengineering↗