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Item Open Access A cerebellar learning model of vestibulo-ocular reflex adaptation in wild-type and mutant mice.(The Journal of neuroscience : the official journal of the Society for Neuroscience, 2014-05) Clopath, Claudia; Badura, Aleksandra; De Zeeuw, Chris I; Brunel, NicolasMechanisms of cerebellar motor learning are still poorly understood. The standard Marr-Albus-Ito theory posits that learning involves plasticity at the parallel fiber to Purkinje cell synapses under control of the climbing fiber input, which provides an error signal as in classical supervised learning paradigms. However, a growing body of evidence challenges this theory, in that additional sites of plasticity appear to contribute to motor adaptation. Here, we consider phase-reversal training of the vestibulo-ocular reflex (VOR), a simple form of motor learning for which a large body of experimental data is available in wild-type and mutant mice, in which the excitability of granule cells or inhibition of Purkinje cells was affected in a cell-specific fashion. We present novel electrophysiological recordings of Purkinje cell activity measured in naive wild-type mice subjected to this VOR adaptation task. We then introduce a minimal model that consists of learning at the parallel fibers to Purkinje cells with the help of the climbing fibers. Although the minimal model reproduces the behavior of the wild-type animals and is analytically tractable, it fails at reproducing the behavior of mutant mice and the electrophysiology data. Therefore, we build a detailed model involving plasticity at the parallel fibers to Purkinje cells' synapse guided by climbing fibers, feedforward inhibition of Purkinje cells, and plasticity at the mossy fiber to vestibular nuclei neuron synapse. The detailed model reproduces both the behavioral and electrophysiological data of both the wild-type and mutant mice and allows for experimentally testable predictions.Item Open Access A framework for integrating the songbird brain.(J Comp Physiol A Neuroethol Sens Neural Behav Physiol, 2002-12) Jarvis, ED; Smith, VA; Wada, K; Rivas, MV; McElroy, M; Smulders, TV; Carninci, P; Hayashizaki, Y; Dietrich, F; Wu, X; McConnell, P; Yu, J; Wang, PP; Hartemink, AJ; Lin, SBiological systems by default involve complex components with complex relationships. To decipher how biological systems work, we assume that one needs to integrate information over multiple levels of complexity. The songbird vocal communication system is ideal for such integration due to many years of ethological investigation and a discreet dedicated brain network. Here we announce the beginnings of a songbird brain integrative project that involves high-throughput, molecular, anatomical, electrophysiological and behavioral levels of analysis. We first formed a rationale for inclusion of specific biological levels of analysis, then developed high-throughput molecular technologies on songbird brains, developed technologies for combined analysis of electrophysiological activity and gene regulation in awake behaving animals, and developed bioinformatic tools that predict causal interactions within and between biological levels of organization. This integrative brain project is fitting for the interdisciplinary approaches taken in the current songbird issue of the Journal of Comparative Physiology A and is expected to be conducive to deciphering how brains generate and perceive complex behaviors.Item Open Access Adaptive Behavior and Learning(2010) Staddon, JERItem Open Access Adult age differences in frontostriatal representation of prediction error but not reward outcome.(Cogn Affect Behav Neurosci, 2014-06) Samanez-Larkin, Gregory R; Worthy, Darrell A; Mata, Rui; McClure, Samuel M; Knutson, BrianEmerging evidence from decision neuroscience suggests that although younger and older adults show similar frontostriatal representations of reward magnitude, older adults often show deficits in feedback-driven reinforcement learning. In the present study, healthy adults completed reward-based tasks that did or did not depend on probabilistic learning, while undergoing functional neuroimaging. We observed reductions in the frontostriatal representation of prediction errors during probabilistic learning in older adults. In contrast, we found evidence for stability across adulthood in the representation of reward outcome in a task that did not require learning. Together, the results identify changes across adulthood in the dynamic coding of relational representations of feedback, in spite of preserved reward sensitivity in old age. Overall, the results suggest that the neural representation of prediction error, but not reward outcome, is reduced in old age. These findings reveal a potential dissociation between cognition and motivation with age and identify a potential mechanism for explaining changes in learning-dependent decision making in old adulthood.Item Open Access Advances in understanding mechanisms of thalamic relays in cognition and behavior.(J Neurosci, 2014-11-12) Mitchell, Anna S; Sherman, S Murray; Sommer, Marc A; Mair, Robert G; Vertes, Robert P; Chudasama, YogitaThe main impetus for a mini-symposium on corticothalamic interrelationships was the recent number of studies highlighting the role of the thalamus in aspects of cognition beyond sensory processing. The thalamus contributes to a range of basic cognitive behaviors that include learning and memory, inhibitory control, decision-making, and the control of visual orienting responses. Its functions are deeply intertwined with those of the better studied cortex, although the principles governing its coordination with the cortex remain opaque, particularly in higher-level aspects of cognition. How should the thalamus be viewed in the context of the rest of the brain? Although its role extends well beyond relaying of sensory information from the periphery, the main function of many of its subdivisions does appear to be that of a relay station, transmitting neural signals primarily to the cerebral cortex from a number of brain areas. In cognition, its main contribution may thus be to coordinate signals between diverse regions of the telencephalon, including the neocortex, hippocampus, amygdala, and striatum. This central coordination is further subject to considerable extrinsic control, for example, inhibition from the basal ganglia, zona incerta, and pretectal regions, and chemical modulation from ascending neurotransmitter systems. What follows is a brief review on the role of the thalamus in aspects of cognition and behavior, focusing on a summary of the topics covered in a mini-symposium held at the Society for Neuroscience meeting, 2014.Item Open Access Attentional Biases in Value-Based Decision-Making(2014) San Martin Ulloa, ReneHumans make decisions in highly complex physical, economic and social environments. In order to adaptively choose, the human brain has to learn about- and attend to- sensory cues that provide information about the potential outcome of different courses of action. Here I present three event-related potential (ERP) studies, in which I evaluated the role of the interactions between attention and reward learning in economic decision-making. I focused my analyses on three ERP components (Chap. 1): (1) the N2pc, an early lateralized ERP response reflecting the lateralized focus of visual; (2) the feedback-related negativity (FRN), which reflects the process by which the brain extracts utility from feedback; and (3) the P300 (P3), which reflects the amount of attention devoted to feedback-processing. I found that learned stimulus-reward associations can influence the rapid allocation of attention (N2pc) towards outcome-predicting cues, and that differences in this attention allocation process are associated with individual differences in economic decision performance (Chap. 2). Such individual differences were also linked to differences in neural responses reflecting the amount of attention devoted to processing monetary outcomes (P3) (Chap. 3). Finally, the relative amount of attention devoted to processing rewards for oneself versus others (as reflected by the P3) predicted both charitable giving and self-reported engagement in real-life altruistic behaviors across individuals (Chap. 4). Overall, these findings indicate that attention and reward processing interact and can influence each other in the brain. Moreover, they indicate that individual differences in economic choice behavior are associated both with biases in the manner in which attention is drawn towards sensory cues that inform subsequent choices, and with biases in the way that attention is allocated to learn from the outcomes of recent choices.
Item Open Access Attractor Dynamics in Networks with Learning Rules Inferred from In Vivo Data.(Neuron, 2018-07) Pereira, Ulises; Brunel, NicolasThe attractor neural network scenario is a popular scenario for memory storage in the association cortex, but there is still a large gap between models based on this scenario and experimental data. We study a recurrent network model in which both learning rules and distribution of stored patterns are inferred from distributions of visual responses for novel and familiar images in the inferior temporal cortex (ITC). Unlike classical attractor neural network models, our model exhibits graded activity in retrieval states, with distributions of firing rates that are close to lognormal. Inferred learning rules are close to maximizing the number of stored patterns within a family of unsupervised Hebbian learning rules, suggesting that learning rules in ITC are optimized to store a large number of attractor states. Finally, we show that there exist two types of retrieval states: one in which firing rates are constant in time and another in which firing rates fluctuate chaotically.Item Open Access Basal ganglia function, stuttering, sequencing, and repair in adult songbirds.(Sci Rep, 2014-10-13) Kubikova, Lubica; Bosikova, Eva; Cvikova, Martina; Lukacova, Kristina; Scharff, Constance; Jarvis, Erich DA pallial-basal-ganglia-thalamic-pallial loop in songbirds is involved in vocal motor learning. Damage to its basal ganglia part, Area X, in adult zebra finches has been noted to have no strong effects on song and its function is unclear. Here we report that neurotoxic damage to adult Area X induced changes in singing tempo and global syllable sequencing in all animals, and considerably increased syllable repetition in birds whose song motifs ended with minor repetitions before lesioning. This stuttering-like behavior started at one month, and improved over six months. Unexpectedly, the lesioned region showed considerable recovery, including immigration of newly generated or repaired neurons that became active during singing. The timing of the recovery and stuttering suggest that immature recovering activity of the circuit might be associated with stuttering. These findings indicate that even after juvenile learning is complete, the adult striatum plays a role in higher level organization of learned vocalizations.Item Open Access Cerebellar learning using perturbations.(eLife, 2018-11-12) Bouvier, Guy; Aljadeff, Johnatan; Clopath, Claudia; Bimbard, Célian; Ranft, Jonas; Blot, Antonin; Nadal, Jean-Pierre; Brunel, Nicolas; Hakim, Vincent; Barbour, BorisThe cerebellum aids the learning of fast, coordinated movements. According to current consensus, erroneously active parallel fibre synapses are depressed by complex spikes signalling movement errors. However, this theory cannot solve the credit assignment problem of processing a global movement evaluation into multiple cell-specific error signals. We identify a possible implementation of an algorithm solving this problem, whereby spontaneous complex spikes perturb ongoing movements, create eligibility traces and signal error changes guiding plasticity. Error changes are extracted by adaptively cancelling the average error. This framework, stochastic gradient descent with estimated global errors (SGDEGE), predicts synaptic plasticity rules that apparently contradict the current consensus but were supported by plasticity experiments in slices from mice under conditions designed to be physiological, highlighting the sensitivity of plasticity studies to experimental conditions. We analyse the algorithm's convergence and capacity. Finally, we suggest SGDEGE may also operate in the basal ganglia.Item Open Access Characteristics of sequential activity in networks with temporally asymmetric Hebbian learning.(Proceedings of the National Academy of Sciences of the United States of America, 2020-11-11) Gillett, Maxwell; Pereira, Ulises; Brunel, NicolasSequential activity has been observed in multiple neuronal circuits across species, neural structures, and behaviors. It has been hypothesized that sequences could arise from learning processes. However, it is still unclear whether biologically plausible synaptic plasticity rules can organize neuronal activity to form sequences whose statistics match experimental observations. Here, we investigate temporally asymmetric Hebbian rules in sparsely connected recurrent rate networks and develop a theory of the transient sequential activity observed after learning. These rules transform a sequence of random input patterns into synaptic weight updates. After learning, recalled sequential activity is reflected in the transient correlation of network activity with each of the stored input patterns. Using mean-field theory, we derive a low-dimensional description of the network dynamics and compute the storage capacity of these networks. Multiple temporal characteristics of the recalled sequential activity are consistent with experimental observations. We find that the degree of sparseness of the recalled sequences can be controlled by nonlinearities in the learning rule. Furthermore, sequences maintain robust decoding, but display highly labile dynamics, when synaptic connectivity is continuously modified due to noise or storage of other patterns, similar to recent observations in hippocampus and parietal cortex. Finally, we demonstrate that our results also hold in recurrent networks of spiking neurons with separate excitatory and inhibitory populations.Item Open Access Comparative genomics reveals molecular features unique to the songbird lineage.(BMC Genomics, 2014-12-13) Wirthlin, Morgan; Lovell, Peter V; Jarvis, Erich D; Mello, Claudio VBACKGROUND: Songbirds (oscine Passeriformes) are among the most diverse and successful vertebrate groups, comprising almost half of all known bird species. Identifying the genomic innovations that might be associated with this success, as well as with characteristic songbird traits such as vocal learning and the brain circuits that underlie this behavior, has proven difficult, in part due to the small number of avian genomes available until recently. Here we performed a comparative analysis of 48 avian genomes to identify genomic features that are unique to songbirds, as well as an initial assessment of function by investigating their tissue distribution and predicted protein domain structure. RESULTS: Using BLAT alignments and gene synteny analysis, we curated a large set of Ensembl gene models that were annotated as novel or duplicated in the most commonly studied songbird, the Zebra finch (Taeniopygia guttata), and then extended this analysis to 47 additional avian and 4 non-avian genomes. We identified 10 novel genes uniquely present in songbird genomes. A refined map of chromosomal synteny disruptions in the Zebra finch genome revealed that the majority of these novel genes localized to regions of genomic instability associated with apparent chromosomal breakpoints. Analyses of in situ hybridization and RNA-seq data revealed that a subset of songbird-unique genes is expressed in the brain and/or other tissues, and that 2 of these (YTHDC2L1 and TMRA) are highly differentially expressed in vocal learning-associated nuclei relative to the rest of the brain. CONCLUSIONS: Our study reveals novel genes unique to songbirds, including some that may subserve their unique vocal control system, substantially improves the quality of Zebra finch genome annotations, and contributes to a better understanding of how genomic features may have evolved in conjunction with the emergence of the songbird lineage.Item Open Access Convergent differential regulation of parvalbumin in the brains of vocal learners.(PLoS One, 2012) Hara, Erina; Rivas, Miriam V; Ward, James M; Okanoya, Kazuo; Jarvis, Erich DSpoken language and learned song are complex communication behaviors found in only a few species, including humans and three groups of distantly related birds--songbirds, parrots, and hummingbirds. Despite their large phylogenetic distances, these vocal learners show convergent behaviors and associated brain pathways for vocal communication. However, it is not clear whether this behavioral and anatomical convergence is associated with molecular convergence. Here we used oligo microarrays to screen for genes differentially regulated in brain nuclei necessary for producing learned vocalizations relative to adjacent brain areas that control other behaviors in avian vocal learners versus vocal non-learners. A top candidate gene in our screen was a calcium-binding protein, parvalbumin (PV). In situ hybridization verification revealed that PV was expressed significantly higher throughout the song motor pathway, including brainstem vocal motor neurons relative to the surrounding brain regions of all distantly related avian vocal learners. This differential expression was specific to PV and vocal learners, as it was not found in avian vocal non-learners nor for control genes in learners and non-learners. Similar to the vocal learning birds, higher PV up-regulation was found in the brainstem tongue motor neurons used for speech production in humans relative to a non-human primate, macaques. These results suggest repeated convergent evolution of differential PV up-regulation in the brains of vocal learners separated by more than 65-300 million years from a common ancestor and that the specialized behaviors of learned song and speech may require extra calcium buffering and signaling.Item Open Access Convergent differential regulation of SLIT-ROBO axon guidance genes in the brains of vocal learners.(J Comp Neurol, 2015-04-15) Wang, Rui; Chen, Chun-Chun; Hara, Erina; Rivas, Miriam V; Roulhac, Petra L; Howard, Jason T; Chakraborty, Mukta; Audet, Jean-Nicolas; Jarvis, Erich DOnly a few distantly related mammals and birds have the trait of complex vocal learning, which is the ability to imitate novel sounds. This ability is critical for speech acquisition and production in humans, and is attributed to specialized forebrain vocal control circuits that have several unique connections relative to adjacent brain circuits. As a result, it has been hypothesized that there could exist convergent changes in genes involved in neural connectivity of vocal learning circuits. In support of this hypothesis, expanding on our related study (Pfenning et al. [2014] Science 346: 1256846), here we show that the forebrain part of this circuit that makes a relatively rare direct connection to brainstem vocal motor neurons in independent lineages of vocal learning birds (songbird, parrot, and hummingbird) has specialized regulation of axon guidance genes from the SLIT-ROBO molecular pathway. The SLIT1 ligand was differentially downregulated in the motor song output nucleus that makes the direct projection, whereas its receptor ROBO1 was developmentally upregulated during critical periods for vocal learning. Vocal nonlearning bird species and male mice, which have much more limited vocal plasticity and associated circuits, did not show comparable specialized regulation of SLIT-ROBO genes in their nonvocal motor cortical regions. These findings are consistent with SLIT and ROBO gene dysfunctions associated with autism, dyslexia, and speech sound language disorders and suggest that convergent evolution of vocal learning was associated with convergent changes in the SLIT-ROBO axon guidance pathway.Item Open Access Convergent transcriptional specializations in the brains of humans and song-learning birds.(Science, 2014-12-12) Pfenning, Andreas R; Hara, Erina; Whitney, Osceola; Rivas, Miriam V; Wang, Rui; Roulhac, Petra L; Howard, Jason T; Wirthlin, Morgan; Lovell, Peter V; Ganapathy, Ganeshkumar; Mouncastle, Jacquelyn; Moseley, M Arthur; Thompson, J Will; Soderblom, Erik J; Iriki, Atsushi; Kato, Masaki; Gilbert, M Thomas P; Zhang, Guojie; Bakken, Trygve; Bongaarts, Angie; Bernard, Amy; Lein, Ed; Mello, Claudio V; Hartemink, Alexander J; Jarvis, Erich DSong-learning birds and humans share independently evolved similarities in brain pathways for vocal learning that are essential for song and speech and are not found in most other species. Comparisons of brain transcriptomes of song-learning birds and humans relative to vocal nonlearners identified convergent gene expression specializations in specific song and speech brain regions of avian vocal learners and humans. The strongest shared profiles relate bird motor and striatal song-learning nuclei, respectively, with human laryngeal motor cortex and parts of the striatum that control speech production and learning. Most of the associated genes function in motor control and brain connectivity. Thus, convergent behavior and neural connectivity for a complex trait are associated with convergent specialized expression of multiple genes.Item Open Access Core and Shell Song Systems Unique to the Parrot Brain.(PLoS One, 2015) Chakraborty, M; Walløe, S; Nedergaard, S; Fridel, EE; Dabelsteen, T; Pakkenberg, B; Bertelsen, MF; Dorrestein, GM; Brauth, SE; Durand, SE; Jarvis, EDThe ability to imitate complex sounds is rare, and among birds has been found only in parrots, songbirds, and hummingbirds. Parrots exhibit the most advanced vocal mimicry among non-human animals. A few studies have noted differences in connectivity, brain position and shape in the vocal learning systems of parrots relative to songbirds and hummingbirds. However, only one parrot species, the budgerigar, has been examined and no differences in the presence of song system structures were found with other avian vocal learners. Motivated by questions of whether there are important differences in the vocal systems of parrots relative to other vocal learners, we used specialized constitutive gene expression, singing-driven gene expression, and neural connectivity tracing experiments to further characterize the song system of budgerigars and/or other parrots. We found that the parrot brain uniquely contains a song system within a song system. The parrot "core" song system is similar to the song systems of songbirds and hummingbirds, whereas the "shell" song system is unique to parrots. The core with only rudimentary shell regions were found in the New Zealand kea, representing one of the only living species at a basal divergence with all other parrots, implying that parrots evolved vocal learning systems at least 29 million years ago. Relative size differences in the core and shell regions occur among species, which we suggest could be related to species differences in vocal and cognitive abilities.Item Open Access Cultural conformity generates extremely stable traditions in bird song.(Nature communications, 2018-06) Lachlan, Robert F; Ratmann, Oliver; Nowicki, StephenCultural traditions have been observed in a wide variety of animal species. It remains unclear, however, what is required for social learning to give rise to stable traditions: what level of precision and what learning strategies are required. We address these questions by fitting models of cultural evolution to learned bird song. We recorded 615 swamp sparrow (Melospiza georgiana) song repertoires, and compared syllable frequency distributions to the output of individual-based simulations. We find that syllables are learned with an estimated error rate of 1.85% and with a conformist bias in learning. This bias is consistent with a simple mechanism of overproduction and selective attrition. Finally, we estimate that syllable types could frequently persist for more than 500 years. Our results demonstrate conformist bias in natural animal behaviour and show that this, along with moderately precise learning, may support traditions whose stability rivals those of humans.Item Open Access Culture From Infrahumans to Humans: Essays in the Philosophy of Biology(2007-05-07T19:07:23Z) Ramsey, Grant AaronIt has become increasingly common to explain the behavior of animals—from sperm whales to songbirds—in terms of culture. But what is animal culture, what is its relationship to other biological concepts and to human culture, and what impact does culture have on a species’ evolution and ecology? My dissertation is an attempt to answer these questions. After an introductory chapter, the dissertation begins (Chapter 2) with a proposal for a novel concept of culture and a critique of the existing ways in which culture has been characterized. These characterizations include views from cultural anthropology as well as attempts to apply the concept of culture to animals. The existing concepts are problematic in a number of ways, such as a priori excluding infrahumans from being candidates for possessing culture, or mistaking what culture is for its measure. In this chapter I offer a way to understand culture that avoids these and other problems. With a concept of culture in hand, the next chapter of my dissertation (Chapter 3) examines and criticizes one key way of understanding the concept of culture, meme theory. In Chapter 4 I turn to the question of how cultural systems can arise in nature, how they can be adaptive, and how the evolution and ecology of species is impacted by the possession of a cultural system. In order to answer these questions I introduce a general constraint on cultural systems—what I am calling the Fundamental Constraint—that has to be satisfied in order for cultural systems to be adaptive. In the final chapter I develop a concept of innovation and draw out the conceptual and empirical implications of this concept.Item Open Access Data-Driven Analysis of Zebra Finch Song Copying and Learning(2021) Brudner, Samuel NavickasChildren learn crucial skills like speech by imitating the behavior of skilled adults. Similarly, juvenile zebra finches learn to sing by learning to imitate adults. This song learning process enables laboratory study of juvenile imitative learning. But it also poses behavioral quantification challenges. Zebra finches produce hundreds of thousands of complex vocalizations during vocal development. These undergo learned changes with respect to acoustic features that are relevant to the animal but experimentally unknown \textit{a priori}. Recent developments in machine learning provide tools to reduce the dimensionality of complex behaviors, plausibly simplifying this inference challenge. These tools have not been validated on or applied to song learning problems.
Here, I validate the use of an autoencoder to extract copying-relevant features from zebra finch song. Then, I develop tools to quantify developmental song change with respect to extracted features. In particular, I generate forward models that quantify developmental changes in syllable acoustic distributions. I also develop a method to score syllable maturity on a rendition-by-rendition basis. Both these techniques reveal circadian behavioral patterns that differ between normally developing and untutored juveniles, suggesting that tutoring not only sets target song acoustics; it directly affects intrinsic features of practice behavior. Critically, these tools enable making concrete predictions from otherwise abstract song learning theories.
Item Open Access Design thinking teaching and learning in higher education: Experiences across four universities.(PloS one, 2022-01) McLaughlin, Jacqueline E; Chen, Elizabeth; Lake, Danielle; Guo, Wen; Skywark, Emily Rose; Chernik, Aria; Liu, TsailuA growing body of literature highlights the increasing demand on college graduates to possess the problem finding, problem framing, and problem-solving skills necessary to address complex real-world challenges. Design thinking (DT) is an iterative, human-centered approach to problem solving that synthesizes what is desirable, equitable, technologically feasible, and sustainable. As universities expand efforts to train students with DT mindsets and skills, we must assess faculty and student DT practices and outcomes to better understand DT course experiences. Understanding how DT is taught and experienced within higher education can help schools promote student learning and align their training programs with professional, personal, and civic needs. In this study, surveys were completed by 19 faculty and 196 students from 23 courses at four universities. DT teaching and learning was characterized by three DT practices and five outcomes. Statistically significant differences were found by discipline of study and student type (i.e., graduate vs undergraduate), but not by gender or race/ethnicity. These results can be used to inform the development of classroom-based DT teaching and learning strategies across higher education institutions and disciplines.Item Open Access Differences in the early cognitive development of children and great apes.(Dev Psychobiol, 2014-04) Wobber, Victoria; Herrmann, Esther; Hare, Brian; Wrangham, Richard; Tomasello, MichaelThere is very little research comparing great ape and human cognition developmentally. In the current studies we compared a cross-sectional sample of 2- to 4-year-old human children (n=48) with a large sample of chimpanzees and bonobos in the same age range (n=42, hereafter: apes) on a broad array of cognitive tasks. We then followed a group of juvenile apes (n=44) longitudinally over 3 years to track their cognitive development in greater detail. In skills of physical cognition (space, causality, quantities), children and apes performed comparably at 2 years of age, but by 4 years of age children were more advanced (whereas apes stayed at their 2-year-old performance levels). In skills of social cognition (communication, social learning, theory of mind), children out-performed apes already at 2 years, and increased this difference even more by 4 years. Patterns of development differed more between children and apes in the social domain than the physical domain, with support for these patterns present in both the cross-sectional and longitudinal ape data sets. These results indicate key differences in the pattern and pace of cognitive development between humans and other apes, particularly in the early emergence of specific social cognitive capacities in humans.
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