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Biology subjects

Kagan, I.

Publications and source records attributed to Kagan, I..

At least 19 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↗

Continuous dynamics of cooperation and competition in social foraging

Real-life social interactions often unfold continuously and involve dynamic cooperation and competition, yet most studies rely on discrete games that do not capture the adaptive and graded nature of continuous sensorimotor decisions. To address this gap, we developed the Cooperation-Competition Foraging game -- an ecologically grounded paradigm in which pairs of participants (dyads) navigate a continuous shared space under face-to-face visibility, deciding in real-time to collect rewarded targets either individually or jointly. Dyads (n=58, 116 participants) spontaneously converged on distinct stable strategies along the cooperation-competition spectrum, forming three groups: cooperative, intermediate, and competitive. Despite the behavioral complexity, our computational model, which incorporated travel path minimization, sensorimotor communication, and recent choice history, predicted dyadic decisions with 87% accuracy, and linked prediction certainty with ensuing dynamics of spatiotemporal coordination. Further modeling revealed how sensorimotor factors, such as movement speed and skill, shape distinct strategies and payoffs. Crucially, we quantify the cost of cooperation, demonstrating that in many dyads prosocial tendencies outweigh the individual benefits of exploiting skill advantages. Our versatile framework provides a predictive, mechanistic account of how social and embodied drivers promote the emergence of dynamic cooperation and competition, and offers rigorous metrics for investigating the neural basis of naturalistic social interactions, and for linking personality traits to distinct strategies.

neuroscience↗

Optic Ataxia in Patients with Thalamic Lesions

Lesions in parietal cortex can strongly impair visually guided reach-grasping behaviour. A specific reaching deficit termed Optic Ataxia (OA) occurs when eye and hand position are dissociated. Optic ataxia has typically been studied in patients with lesions in parietal cortex, neglecting potential thalamic contributions. We here examined 28 acute stroke patients (age 58.9 {+/-} 12.6 years) with circumscribed thalamic lesions for the presence of optic ataxia. We leveraged MRI-based lesion-symptom mapping to address the contributions of specific thalamic nuclei to visually-guided reaching deficits under foveal and peripheral viewing conditions. Based on the cortical literature, we hypothesized that lesions in thalamic nuclei with strong connections to the inferior and superior parietal cortex, such as the ventrolateral nucleus and pulvinar might lead to optic ataxia. In comparison with aged-matched healthy subjects (n = 40, age 60.6 {+/-} 9.1 years), we identified five thalamic patients with optic ataxia, most pronounced for reaches with the contralesional hand into the contralesional space. While motor and grasping deficits and optic ataxia occurred frequently together, they did not always co-occur, and visual attention deficits could not account for the optic ataxia either. Comparing the lesion maps of patients with and without optic ataxia, the critical lesion site for optic ataxia was not restricted to one circumscribed thalamic region within the Morel atlas. Instead, it encompassed several medial and lateral nuclei within and around the internal medullary laminar (IML) complex. Interestingly, this region matches the so-called central thalamus, a functionally defined thalamic region that is considered a higher-order nucleus complex. It receives afferent inputs from the cerebellum and brainstem regions and connects to fronto-parietal regions involved in eye movement control. Taken together, our results suggest the critical importance of thalamic nuclei for the spatial transformation from eye-into body-centered coordinates.

neuroscience↗

Fixation shifts in a novel 'no-report' binocular rivalry paradigm induce saccade-related perceptual switches

No-report paradigms help to avoid report-related confounds in conscious perception studies. A novel no-report binocular rivalry paradigm by Hesse and Tsao (2020) tracks conscious content using eye position as subjects follow fixation points linked to the rivaling stimuli. However, it remains unclear whether perceptual changes arise spontaneously or are induced by external factors such as fixation shifts and saccades. We found an increased probability of perceptual switches time-locked to fixation point shifts, indicating that some switches are externally driven. To disentangle the effects of visual fixation shifts and saccades, we implemented a two-factorial design and found that saccades play a larger role in eliciting perceptual changes. We estimate that 14% of saccades trigger a switch, accounting for 24% of all perceptual transitions. Our findings provide an analysis framework and guidelines for excluding externally driven perceptual switches, enabling a clearer focus on internally generated perceptual dynamics.

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↗

Dorsal pulvinar inactivation leads to spatial selection bias without perceptual deficit

The dorsal pulvinar has been implicated in visuospatial attentional and perceptual confidence processing. Pulvinar lesions in humans and monkeys lead to spatial neglect symptoms, including an overt spatial saccade bias during free choices. But it remains unclear whether disrupting the dorsal pulvinar during target selection that relies on a perceptual decision leads to a perceptual impairment or a more general spatial orienting and choice deficit. To address this question, we reversibly inactivated the unilateral dorsal pulvinar by injecting GABA-A agonist THIP while two macaque monkeys performed a color discrimination saccade task with varying perceptual difficulty. We used Signal Detection Theory and simulations to dissociate perceptual sensitivity (d-prime) and spatial selection bias (response criterion) effects. We expected a decrease in d-prime if dorsal pulvinar affects perceptual discrimination and a shift in response criterion if dorsal pulvinar is mainly involved in spatial orienting. After the inactivation, we observed response criterion shifts away from contralesional stimuli, especially when two competing stimuli in opposite hemifields were present. Notably, the d-prime and overall accuracy remained largely unaffected. Our results underline the critical contribution of the dorsal pulvinar to spatial orienting and action selection while showing it to be less important for visual perceptual discrimination.

neuroscience↗

Modality-specific and modality-general representations of reward value in frontal cortex

Standard neuroeconomics theories state that the value of different classes of stimuli, for instance the hedonic value of food versus music, is transformed to a common reference scale that is independent of their sensory properties. However, adaptive behaviour in a multimodal dynamic environment requires that our brain also encodes information about the sensory features of rewarding stimuli. How these two processes, i.e. deriving a common reference scale for valuation and maintaining sensitivity to the sensory contexts for goal-directed behaviour, are implemented in the brain remains inadequately understood. Here, we acquired fMRI data while human participants were engaged in a dynamic foraging task requiring them to integrate the reward history of auditory or visual choice options and update the subjective value assigned to each sensory modality. Univariate fMRI analysis revealed modality-specific and modality-general value representations in orbitofrontal cortex (OFC) and ventromedial prefrontal cortex (vmPFC), respectively. Crucially, modality-specific value representations were absent when the task involved instruction-based rather than value-based choices. The analysis of effective connectivity further demonstrated that the modality-specific value representations emerged as a result of selective bidirectional interactions across the auditory and visual sensory cortices, the corresponding OFC clusters and the vmPFC. These results show how a valuation process that is sensitive to the sensory context of rewarding stimuli is enabled in the brain.

neuroscience↗

Egocentric Bias in Effort Comparison Tasks Is Driven by Sensory Asymmetries, Not Attribution Bias

When comparing themselves with others, people often perceive their own actions and behaviour favourably. This phenomenon is often categorised as a bias of attribution, with favourable self-evaluation resulting from differing explanations of ones own behaviour and that of others. However, studies on availability biases offer an alternative explanation, ascribing egocentric biases to the inherent sensory asymmetries between performing an action and merely observing it. In this study, we used a paradigm that allowed us to directly compare these two distinct sources of bias. Participants perceived the tasks they performed to be harder than the tasks they observed, but demonstrated no bias driven by favourable self-evaluation. Furthermore, the degree of overestimation of the difficulty of performed tasks was magnified as overall task difficulty increased. These findings suggest that egocentric biases are in part derived from sensory asymmetries inherent to the first-person perspective.

animal behavior and cognition↗

Decision-making processes in perceptual learning depend on effectors

Visual perceptual learning is traditionally thought to arise in visual cortex. However, typical perceptual learning tasks also involve systematic mapping of visual information onto motor actions. Because the motor system contains both effector-specific and effector-unspecific representations, the question arises whether visual perceptual learning is effector-specific itself, or not. Here, we study this question in an orientation discrimination task. Subjects learn to indicate their choices either with joystick movements or with manual reaches. After training, we challenge them to perform the same task with eye movements. We dissect the decision-making process using the drift diffusion model. We find that learning effects on the rate of evidence accumulation depend on effectors, albeit not fully. This suggests that during perceptual learning, visual information is mapped onto effector-specific integrators. Overlap of the populations of neurons encoding motor plans for these effectors may explain partial generalization. Taken together, visual perceptual learning is not limited to visual cortex, but also affects sensorimotor mapping at the interface of visual processing and decision making.

neuroscience↗

Visual, delay and oculomotor timing and tuning in macaque dorsal pulvinar during instructed and free choice memory saccades

Causal perturbations suggest that the primate dorsal pulvinar (dPul) plays a crucial role in target selection and saccade planning, but its basic visuomotor neuronal properties are unclear. While some functional aspects of dPul and interconnected frontoparietal areas - e.g. ipsilesional choice bias after inactivation - are similar, it is unknown if dPul shares oculomotor properties of the cortical circuitry, in particular the delay and choice-related activity. We investigated such properties in macaque dPul during instructed and free-choice memory saccades. Most recorded units showed visual (16%), visuomotor (29%) or motor-related (35%) responses. Visual responses were mainly contralateral; motor-related responses were predominantly post-saccadic (64%) and showed weak contralateral bias. Pre-saccadic enhancement was infrequent (9-15%) - instead, activity was often suppressed during saccade planning (30%) and execution (19%). Surprisingly, only few units exhibited classical visuomotor patterns combining cue and continuous delay activity until the saccade or pre-saccadic ramping, and most spatially-selective neurons did not encode the upcoming decision during free-choice delay. Thus, in absence of a visible goal, the dorsal pulvinar has a limited role in prospective saccade planning, with patterns partially complementing its frontoparietal partners. Conversely, prevalent cue and post-saccadic responses imply the participation in integrating spatial goals with processing across saccades.

neuroscience↗

Effective connectivity and spatial selectivity-dependent fMRI changes elicited by microstimulation of pulvinar and LIP

The thalamic pulvinar and the lateral intraparietal area (LIP) share reciprocal anatomical connections and are part of an extensive cortical and subcortical network involved in spatial attention and oculomotor processing. The goal of this study was to compare the effective connectivity of dorsal pulvinar (dPul) and LIP and to probe the dependency of microstimulation effects on task demands and spatial tuning properties of a given brain region. To this end, we applied unilateral electrical microstimulation in the dPul (mainly medial pulvinar) and LIP in combination with event-related BOLD fMRI in monkeys performing fixation and memory-guided saccade tasks. Microstimulation in both dPul and LIP enhanced task-related activity in monosynaptically-connected fronto-parietal cortex and along the superior temporal sulcus (STS) including putative face patch locations, as well as in extrastriate cortex. LIP microstimulation elicited strong activity in the opposite homotopic LIP while no homotopic activation was found with dPul stimulation. Both dPul and LIP stimulation also elicited activity in several heterotopic cortical areas in the opposite hemisphere, implying polysynaptic propagation of excitation. Despite extensive activation along the intraparietal sulcus evoked by LIP stimulation, there was a difference in frontal and occipital connectivity elicited by posterior and anterior LIP stimulation sites. Comparison of dPul stimulation with the adjacent but functionally dissimilar ventral pulvinar also showed distinct connectivity. On the level of single trial timecourses within each region of interest (ROI), most ROIs did not show task-dependence of stimulation-elicited response modulation. Across ROIs, however, there was an interaction between task and stimulation, and task-specific correlations between the initial spatial selectivity and the magnitude of stimulation effect were observed. Consequently, stimulation-elicited modulation of task-related activity was best fitted by an additive model scaled down by the initial response amplitude. In summary, we identified overlapping and distinct patterns of thalamocortical and corticocortical connectivity of pulvinar and LIP, highlighting the dorsal bank and fundus of STS as a prominent node of shared circuitry. Spatial task-specific and partly polysynaptic modulations of cue and saccade planning delay period activity in both hemispheres exerted by unilateral pulvinar and parietal stimulation provide insight into the distributed interhemispheric processing underlying spatial behavior. HighlightsO_LIElectrical stimulation of pulvinar and LIP was used to study fMRI effective connectivity C_LIO_LIBoth regions activated prefrontal cortex and the dorsal bank of superior temporal sulcus C_LIO_LIActivations within and across hemispheres suggest polysynaptic propagation C_LIO_LIStimulation effects show interactions between task- and spatial selectivity C_LIO_LIStimulation effects are best fitted by an additive model scaled by the initial response C_LI

neuroscience↗

Deep Active Inference and Scene Construction

Adaptive agents must act in intrinsically uncertain environments with complex latent structure. Here, we elaborate a model of visual foraging - in a hierarchical context - wherein agents infer a higher-order visual pattern (a scene) by sequentially sampling ambiguous cues. Inspired by previous models of scene construction - that cast perception and action as consequences of approximate Bayesian inference - we use active inference to simulate decisions of agents categorizing a scene in a hierarchically-structured setting. Under active inference, agents develop probabilistic beliefs about their environment, while actively sampling it to maximise the evidence for their internal generative model. This approximate evidence maximization (i.e. self-evidencing) comprises drives to both maximise rewards and resolve uncertainty about hidden states. This is realised via minimization of a free energy functional of posterior beliefs about both the world as well as the actions used to sample or perturb it, corresponding to perception and action, respectively. We show that active inference, in the context of hierarchical scene construction, gives rise to many empirical evidence accumulation phenomena, such as noise-sensitive reaction times and epistemic saccades. We explain these behaviours in terms of the principled drives that constitute the expected free energy, the key quantity for evaluating policies under active inference. In addition, we report novel behaviours exhibited by these active inference agents that furnish new predictions for research on evidence accumulation and perceptual decision-making. We discuss the implications of this hierarchical active inference scheme for tasks that require planned sequences of information-gathering actions to infer compositional latent structure (such as visual scene construction and sentence comprehension). Finally, we propose experiments to contextualise active inference in relation to other formulations of evidence accumulation (e.g. drift-diffusion models) in tasks that require planning in uncertain environments with higher-order structure.

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↗

Eye position signals in the dorsal pulvinar during fixation and goal-directed saccades

Most sensorimotor cortical areas contain eye position information thought to ensure perceptual stability across saccades and underlie spatial transformations supporting goal-directed actions. One pathway by which eye position signals could be relayed to and across cortical areas is via the dorsal pulvinar. Several studies demonstrated saccade-related activity in the dorsal pulvinar and we have recently shown that many neurons exhibit post-saccadic spatial preference long after the saccade execution. In addition, dorsal pulvinar lesions lead to gaze-holding deficits expressed as nystagmus or ipsilesional gaze bias, prompting us to investigate the effects of eye position. We tested three starting eye positions (-15{degrees}/0{degrees}/15{degrees}) in monkeys performing a visually-cued memory saccade task. We found two main types of gaze dependence. First, [~]50% of neurons showed an effect of static gaze direction during initial and post-saccadic fixation. Eccentric gaze preference was more common than straight ahead. Some of these neurons were not visually-responsive and might be primarily signaling the position of the eyes in the orbit, or coding foveal targets in a head/body/world-centered reference frame. Second, many neurons showed a combination of eye-centered and gaze-dependent modulation of visual, memory and saccadic responses to a peripheral target. A small subset showed effects consistent with eye position-dependent gain modulation. Analysis of reference frames across task epochs from visual cue to post-saccadic target fixation indicated a transition from predominantly eye-centered encoding to representation of final gaze or foveated locations in non-retinocentric coordinates. These results show that dorsal pulvinar neurons carry information about eye position, which could contribute to steady gaze during postural changes and to reference frame transformations for visually-guided eye and limb movements.\n\nNew & NoteworthyWork on the pulvinar focused on eye-centered visuospatial representations, but position of the eyes in the orbit is also an important factor that needs to be taken into account during spatial orienting and goal-directed reaching. Here we show that dorsal pulvinar neurons are influenced by eye position. Gaze direction modulated ongoing firing during stable fixation, as well as visual and saccade responses to peripheral targets, suggesting involvement of the dorsal pulvinar in spatial coordinate transformations.

neuroscience↗

Emergence and suppression of cooperation by action visibility in transparent games

Real-world agents, such as humans, animals and robots, observe each other during interactions and choose their own actions taking the partners ongoing behaviour into account. Yet, classical game theory assumes that players act either strictly sequentially or strictly simultaneously (without knowing the choices of each other). To account for action visibility and provide a more realistic model of interactions under time constraints, we introduce a new game-theoretic setting called transparent game, where each player has a certain probability to observe the choice of the partner before deciding on its own action. Using evolutionary simulations, we demonstrate that even a small probability of seeing the partners choice before ones own decision substantially changes evolutionary successful strategies. Action visibility enhances cooperation in a Bach-or-Stravinsky game, but disrupts cooperation in a more competitive iterated Prisoners Dilemma. In both games, strategies based on the "Win-stay, lose-shift" and "Tit-for-tat" principles are predominant for moderate transparency, while for high transparency strategies of "Leader-Follower" type emerge. Our results have implications for studies of human and animal social behaviour, especially for the analysis of dyadic and group interactions.

evolutionary biology↗

Post-decision wagering after perceptual judgments reveals bi-directional certainty readouts

Humans and other animals constantly evaluate their decisions in order to learn and behave adaptively. Experimentally, such evaluation processes are accessed using metacognitive reports made after decisions, typically using verbally formulated confidence scales. When subjects report high confidence, it reflects a high certainty of being correct, but a low confidence might signify either low certainty about the outcome, or a high certainty of being incorrect. Hence, metacognitive reports might reflect not only different levels of decision certainty, but also two certainty directions (certainty of being correct and certainty of being incorrect). It is important to test if such bi-directional processing can be measured because, for decision-making under uncertainty, information about being incorrect is as important as information about being correct for guidance of subsequent behavior. We were able to capture implicit bi-directional certainty readouts by asking subjects to bet money on their perceptual decision accuracy using a six-grade wager scale (post-decision wagering, PDW). To isolate trial-specific aspects of metacognitive judgments, we used pre-decision wagering (wagering before the perceptual decision) to subtract, from PDW trials, influences resulting from non-trial-specific assessment of expected difficulty and psychological biases. This novel design allowed independent quantification of certainty of being correct and certainty of being incorrect, showing that subjects were able to read out certainty in a bi-directional manner. Certainty readouts about being incorrect were particularly associated with metacognitive sensitivity exceeding perceptual sensitivity (i.e. meta-d' > d'), suggesting that such enhanced metacognitive efficiency is driven by information about incorrect decisions. Readouts of certainty in both directions increased on easier trials, and both certainty directions were also associated with faster metacognitive reaction times, indicating that certainty of being incorrect was not confounded with low certainty. Finally, both readouts influenced the amount of money subjects earned through PDW, suggesting that bi-directional readouts are important for planning future actions when feedback about previous decisions is unavailable.

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↗