Competitive Disinhibition Mediates Behavioral Choice and Sequences in Drosophila.

Even a simple sensory stimulus can elicit distinct innate behaviors and sequences. During sensorimotor decisions, competitive interactions among neurons that promote distinct behaviors must ensure the selection and maintenance of one behavior, while suppressing others. The circuit implementation of these competitive interactions is still an open question. By combining comprehensive electron microscopy reconstruction of inhibitory interneuron networks, modeling, electrophysiology, and behavioral studies, we determined the circuit mechanisms that contribute to the Drosophila larval sensorimotor decision to startle, explore, or perform a sequence of the two in response to a mechanosensory stimulus. Together, these studies reveal that, early in sensory processing, (1) reciprocally connected feedforward inhibitory interneurons implement behavioral choice, (2) local feedback disinhibition provides positive feedback that consolidates and maintains the chosen behavior, and (3) lateral disinhibition promotes sequence transitions. The combination of these interconnected circuit motifs can implement both behavior selection and the serial organization of behaviors into a sequence.

Abstract task sequence initiation deficit dissociates anxiety disorders from obsessive-compulsive disorder and healthy controls.

In everyday life, humans perform sequences of tasks. These tasks may be disrupted in people with obsessive-compulsive disorder (OCD). Symptoms, such as compulsions, can be considered sequential and often cause repetitions of tasks that disrupt daily living (e.g., checking the stove while cooking). Motor sequences have been used to study behavioral deficits in OCD. However, not all sequences are motor sequences. Some are more "abstract" in that they are composed of a series of tasks (e.g., chopping and stirring) rather than being dependent on individual actions or stimuli. These abstract task sequences require cognitive control mechanisms for their execution. Although theory has proposed deficits in these sequences in OCD as well, they have not been directly investigated. We tested the hypotheses that OCD participants exhibit deficits in the control mechanisms specific to abstract task sequences and more general flexible behavior (measured with task switching within the sequences), relative to health controls (HCs) and clinical controls (participants with anxiety disorders [ANX]). A total of 112 participants completed abstract task sequences consisting of simple categorization tasks. Surprisingly, participants with OCD did not perform worse than HCs or ANX. However, ANX participants showed impairments specific to sequential control that did not extend to more general flexible control. Thus, we showed a novel behavioral dissociation between OCD and ANX specific to abstract task sequential control. These results also implicate deficits in specific frontal sequential control neural circuitry in ANX and not in OCD, where implicit sequential deficits may more closely align with striatal circuits.

Comparative analysis of optional hunting behavior in Cricetinae hamsters using the data compression approach.

Research into the hunting behavior in members of the Cricetidae family offers an opportunity to reveal what changes in the predatory behavioral sequences occur when a rodent species shifts from an omnivorous to a predatory lifestyle. The study tests the following hypotheses: are there phylogenetic differences in the divergence of species' predatory lifestyles in hamsters or do ecological factors lead to shaping their hunting behavior? We applied the data compression approach for performing comparative analysis of hunting patterns as biological "texts." The study presents a comparative analysis of hunting behaviors in five Cricetinae species, focusing on the new data obtained for the desert hamster Phodopus roborovskii whose behavior has never been studied before. The hunting behavior of P. roborovskii appeared to be the most variable one. In contrast, behavioral sequences in P. campbelli and Allocricetulus curtatus display more significant order and predictability of behavior during hunting. Optional hunting behavior in the most ancient species P. roborovskii displayed similarities with obligate patterns in "young" Allocricetulus species. It thus turned out to be the most advanced hunter among members of the Phodopus genus. Differences in hunting sequences among Phodopus representatives suggest that the hunting behavior of these species, despite its optional mode, was subject to selection during species splitting within the genus. These results did not reveal the role played by phylogenetic differences in the divergence of species' predatory lifestyles. They suggested that ecological conditions are the main factors in speciation of the hunting behavior in hamsters.

Looking for complexity in quantitative semiology of frontal and temporal lobe seizures using neuroethology and graph theory.

Epileptic syndromes and seizures are the expression of complex brain systems. Because no analysis of complexity has been applied to epileptic seizure semiology, our goal was to apply neuroethology and graph analysis to the study of the complexity of behavioral manifestations of epileptic seizures in human frontal lobe epilepsy (FLE) and temporal lobe epilepsy (TLE). We analyzed the video recordings of 120 seizures of 18 patients with FLE and 28 seizures of 28 patients with TLE. All patients were seizure-free >1 year after surgery (Engel Class I). All patients' behavioral sequences were analyzed by means of a glossary containing all behaviors and analyzed for neuroethology (Ethomatic software). The same series were used for graph analysis (CYTOSCAPE). Behaviors, displayed as nodes, were connected by edges to other nodes according to their temporal sequence of appearance. Using neuroethology analysis, we confirmed data in the literature such as in FLE: brief/frequent seizures, complex motor behaviors, head and eye version, unilateral/bilateral tonic posturing, speech arrest, vocalization, and rapid postictal recovery and in the case of TLE: presence of epigastric aura, lateralized dystonias, impairment of consciousness/speech during ictal and postictal periods, and development of secondary generalization. Using graph analysis metrics of FLE and TLE confirmed data from flowcharts. However, because of the algorithms we used, they highlighted more powerfully the connectivity and complex associations among behaviors in a quite selective manner, depending on the origin of the seizures. The algorithms we used are commonly employed to track brain connectivity from EEG and MRI sources, which makes our study very promising for future studies of complexity in this field.

Courtship behavior of the castniid palm borer, Paysandisia archon: potential roles of male scents and visual cues in a day-flying moth.

The castniid palm borer, Paysandisia archon (Burmeister) (Lepidoptera: Castniidae), is a South American moth that in the last ten years has become a major pest of palm trees in the Mediterranean region. Current knowledge on the reproductive behavior of this diurnal moth suggests the importance of both visual and chemical cues, in particular the production of a male pheromone emitted during a specific scratching behavior. Male-produced scents have diverse functions in lepidopteran sexual communication but generally act during courtship behavior, leading to complex, stereotyped courtship sequences. As a first step to understand the cues involved in mating behavior and the role of male scents in male mating success, we quantified sequences of P. archon courtship behavior using video filming. To distinguish behaviors leading to an approach of both partners from those involved in short-range courtship, sequences were divided into "approach" and "interaction" phases. Quantifications and analyses were first made by NPMANOVA analysis of behavioral event frequencies, followed by flowchart construction using transition matrix probabilities. In 90% of the observations, courting activities led to copulation, but successful sequences were highly variable and could be divided into two categories, "rapid" and "prolonged" courtship sequences. In both categories, approaches were performed by males but depended strongly on female movements, especially on female flights. The significant behavioral differences were observed after the first contact (i.e., interaction phase) where, in rapid sequences, males generally acceded to copulation without displaying scratching behavior. Conversely, in prolonged sequences, the female expressed evading behavior and male scratching frequency increased. The possible roles of male scent emission in female mate choice and the importance of visual cues in the mating behavior of P. archon are discussed.

Feedback inhibition by a descending GABAergic neuron regulates timing of escape behavior in Drosophila larvae.

Escape behaviors help animals avoid harm from predators and other threats in the environment. Successful escape relies on integrating information from multiple stimulus modalities (of external or internal origin) to compute trajectories toward safe locations, choose between actions that satisfy competing motivations, and execute other strategies that ensure survival. To this end, escape behaviors must be adaptive. When a Drosophila melanogaster larva encounters a noxious stimulus, such as the focal pressure a parasitic wasp applies to the larval cuticle via its ovipositor, it initiates a characteristic escape response. The escape sequence consists of an initial abrupt bending, lateral rolling, and finally rapid crawling. Previous work has shown that the detection of noxious stimuli primarily relies on class IV multi-dendritic arborization neurons (Class IV neurons) located beneath the body wall, and more recent studies have identified several important components in the nociceptive neural circuitry involved in rolling. However, the neural mechanisms that underlie the rolling-escape sequence remain unclear. Here, we present both functional and anatomical evidence suggesting that bilateral descending neurons within the subesophageal zone of D. melanogaster larva play a crucial role in regulating the termination of rolling and subsequent transition to escape crawling. We demonstrate that these descending neurons (designated SeIN128) are inhibitory and receive inputs from a second-order interneuron upstream (Basin-2) and an ascending neuron downstream of Basin-2 (A00c). Together with optogenetic experiments showing that co-activation of SeIN128 neurons and Basin-2 influence the temporal dynamics of rolling, our findings collectively suggest that the ensemble of SeIN128, Basin-2, and A00c neurons forms a GABAergic feedback loop onto Basin-2, which inhibits rolling and thereby facilitates the shift to escape crawling.

Approximations of algorithmic and structural complexity validate cognitive-behavioral experimental results.

Being able to objectively characterize the intrinsic complexity of behavioral patterns resulting from human or animal decisions is fundamental for deconvolving cognition and designing autonomous artificial intelligence systems. Yet complexity is difficult in practice, particularly when strings are short. By numerically approximating algorithmic (Kolmogorov) complexity (K), we establish an objective tool to characterize behavioral complexity. Next, we approximate structural (Bennett's Logical Depth) complexity (LD) to assess the amount of computation required for generating a behavioral string. We apply our toolbox to three landmark studies of animal behavior of increasing sophistication and degree of environmental influence, including studies of foraging communication by ants, flight patterns of fruit flies, and tactical deception and competition (e.g., predator-prey) strategies. We find that ants harness the environmental condition in their internal decision process, modulating their behavioral complexity accordingly. Our analysis of flight (fruit flies) invalidated the common hypothesis that animals navigating in an environment devoid of stimuli adopt a random strategy. Fruit flies exposed to a featureless environment deviated the most from Levy flight, suggesting an algorithmic bias in their attempt to devise a useful (navigation) strategy. Similarly, a logical depth analysis of rats revealed that the structural complexity of the rat always ends up matching the structural complexity of the competitor, with the rats' behavior simulating algorithmic randomness. Finally, we discuss how experiments on how humans perceive randomness suggest the existence of an algorithmic bias in our reasoning and decision processes, in line with our analysis of the animal experiments. This contrasts with the view of the mind as performing faulty computations when presented with randomized items. In summary, our formal toolbox objectively characterizes external constraints on putative models of the "internal" decision process in humans and animals.

Deconstructing Hunting Behavior Reveals a Tightly Coupled Stimulus-Response Loop.

Animal behavior often forms sequences, built from simple stereotyped actions and shaped by environmental cues. A comprehensive characterization of the interplay between an animal's movements and its environment is necessary to understand the sensorimotor transformations performed by the brain. Here, we use unsupervised methods to study behavioral sequences in zebrafish larvae. We generate a map of swim bouts, revealing that fish modulate their tail movements along a continuum. During prey capture, larvae produce stereotyped sequences using a subset of bouts from a broader behavioral repertoire. These sequences exhibit low-order transition dynamics and immediately respond to changes in visual cues. Chaining of prey capture bouts is disrupted in visually impaired (lakritz and blumenkohl) mutants, and removing the prey stimulus during ongoing behavior in closed-loop virtual reality causes larvae to immediately abort the hunting sequence. These results suggest that the continuous integration of sensory information is necessary to structure the behavior. This stimulus-response loop serves to bring prey into the anterior dorsal visual field of the larvae. Fish then release a capture strike maneuver comprising a stereotyped jaw movement and tail movements fine-tuned to the distance of the prey. Fish with only one intact eye fail to correctly position the prey in the strike zone, but are able to produce the strike itself. Our analysis shows that short-term integration of binocular visual cues shapes the behavioral dynamics of hunting, thus uncovering the temporal organization of a goal-directed behavior in a vertebrate.

Recurring sequences of multimodal non-verbal and verbal communication during a human psycho-social stress test: A temporal pattern analysis.

BACKGROUND: The Trier Social Stress Test (TSST) is a widely used protocol to study human psycho-social stress responses. Quantitative reports of non-verbal behaviors have been carried out by means of the Ethological Coding System for Interviews (ECSI). However, no data have described whether and how non-verbal and verbal behaviors take part in the composition of multimodal sequences of communication during the test. METHOD: Five non-verbal ECSI categories and four verbal behaviors related with communication were included in the Ethogram. A focal sampling was employed to ensure a high temporal resolution of the behavioral annotation. T-Pattern Analysis was employed to detect statistically-grounded behavioral sequences. RESULTS: As a first step, frequency, overall duration and mean time length were reported for each component of the Ethogram. Besides, T-Pattern Analysis revealed that communication during TSST is organized according to a complex temporal patterning. We found 51 different sequences (T-patterns): 8 T-patterns included exclusively non-verbal behaviors; 17 T-patterns included verbal behaviors and 26 T-patterns encompassed mixed non-verbal and verbal behaviors. T-patterns were discussed depending on their putative functional meaning since non-verbal behaviors almost did not overlap within patterns. CONCLUSIONS: The implementation of an Ethogram including non-verbal and verbal components highlights the multimodal human communication in TSST. T-Pattern Analysis unveils the real-time interplay among these components. In this study results are discussed according to Jakobson's six constitutive factors of communication.

Nucleus Isthmi Is Required to Sustain Target Pursuit during Visually Guided Prey-Catching.

Animals must frequently perform a sequence of behaviors to achieve a specific goal. However, the neural mechanisms that promote the continuation and completion of such action sequences are not well understood. Here, we characterize the anatomy, physiology, and function of the nucleus isthmi (NI), a cholinergic nucleus thought to modulate tectal-dependent, goal-directed behaviors. We find that the larval zebrafish NI establishes reciprocal connectivity with the optic tectum and identify two distinct types of isthmic projection neuron that either connect ipsilaterally to retinorecipient laminae of the tectum and pretectum or bilaterally to both tectal hemispheres. Laser ablation of NI caused highly specific deficits in tectally mediated loom-avoidance and prey-catching behavior. In the context of hunting, NI ablation did not affect prey detection or hunting initiation but resulted in larvae failing to sustain prey-tracking sequences and aborting their hunting routines. Moreover, calcium imaging revealed elevated neural activity in NI following onset of hunting behavior. We propose a model in which NI provides state-dependent feedback facilitation to the optic tectum and pretectum to potentiate neural activity and increase the probability of consecutive prey-tracking maneuvers during hunting sequences.

T-pattern analysis for the study of temporal structure of animal and human behavior: a comprehensive review.

A basic tenet in the realm of modern behavioral sciences is that behavior consists of patterns in time. For this reason, investigations of behavior deal with sequences that are not easily perceivable by the unaided observer. This problem calls for improved means of detection, data handling and analysis. This review focuses on the analysis of the temporal structure of behavior carried out by means of a multivariate approach known as T-pattern analysis. Using this technique, recurring sequences of behavioral events, usually hard to detect, can be unveiled and carefully described. T-pattern analysis has been successfully applied in the study of various aspects of human or animal behavior such as behavioral modifications in neuro-psychiatric diseases, route-tracing stereotypy in mice, interaction between human subjects and animal or artificial agents, hormonal-behavioral interactions, patterns of behavior associated with emesis and, in our laboratories, exploration and anxiety-related behaviors in rodents. After describing the theory and concepts of T-pattern analysis, this review will focus on the application of the analysis to the study of the temporal characteristics of behavior in different species from rodents to human beings. This work could represent a useful background for researchers who intend to employ such a refined multivariate approach to the study of behavior.

Les Sequences De Remplacement Chez Ctenodactylus gundi: Competition Ou Cooperation?

Ctenodactylus gundi, a colonial rodent inhabiting saharian Atlas, is often seen standing at the top of the rocks. At more or less regular intervals, another conspecific is taking the place of the "resident" animal. This relief impues only amicable reliationships and is to be considered as a kind of cooperation. The function of the resident, as a specific element against predation, is discussed.