A neural hub for holistic courtship displays.

Courtship displays often involve the concerted production of several distinct courtship behaviors. The neural circuits that enable the concerted production of the component behaviors of a courtship display are not well understood. Here, we identify a midbrain cell group (A11) that enables male zebra finches to produce their learned songs in concert with various other behaviors, including female-directed orientation, pursuit, and calling. Anatomical mapping reveals that A11 is at the center of a complex network including the song premotor nucleus HVC as well as brainstem regions crucial to calling and locomotion. Notably, lesioning A11 terminals in HVC blocked female-directed singing but did not interfere with female-directed calling, orientation, or pursuit. In contrast, lesioning A11 cell bodies strongly reduced and often abolished all female-directed courtship behaviors. However, males with either type of lesion still produced songs when in social isolation. Lastly, imaging calcium-related activity in A11 terminals in HVC showed that during courtship, A11 signals HVC about female-directed calls and during female-directed singing, about the transition from simpler introductory notes to the acoustically more complex syllables that depend intimately on HVC for their production. These results show how a brain region important to reproduction in both birds and mammals enables holistic courtship displays in male zebra finches, which include learning songs, calls, and other non-vocal behaviors.

Spatial cognition in birds.

Finding the kitchen refrigerator in the middle of a sleepless night or arriving at the home parking lot at the end of a daily drive are things that we mostly take for granted. However, such feats rely on complex brain computations that integrate multiple environmental and internal cues. Together these computations mediate the process referred to as spatial cognition, the study of which has been one of the most active research fields in modern neuroscience. In the early 1970s, John O'Keefe recorded the activity of individual cells in the hippocampus of a freely moving rat: he found cells that fired action potentials when the rat passed through a specific place in the environment. Examining the activity pattern of such 'place cells', he concluded that the hippocampus may contain a 'cognitive map' that represents the animal's location in its proximate environment. Since O'Keefe's seminal discovery about half a century ago, extensive research has led to a detailed characterization of hippocampal space processing in rats and other mammalian species.

What pops out for you pops out for fish: Four common visual features.

Visual search is the ability to detect a target of interest against a background of distracting objects. For many animals, performing this task fast and accurately is crucial for survival. Typically, visual-search performance is measured by the time it takes the observer to detect a target against a backdrop of distractors. The efficiency of a visual search depends fundamentally on the features of the target, the distractors, and the interaction between them. Substantial efforts have been devoted to investigating the influence of different visual features on visual-search performance in humans. In particular, it has been demonstrated that color, size, orientation, and motion are efficient visual features to guide attention in humans. However, little is known about which features are efficient and which are not in other vertebrates. Given earlier observations that moving targets elicit pop-out and parallel search in the archerfish during visual-search tasks, here we investigate and confirm that all four of these visual features also facilitate efficient search in the archerfish in a manner comparable to humans. In conjunction with results reported for other species, these finding suggest universality in the way visual search is carried out by animals despite very different brain anatomies and living environments.

What a predator can teach us about visual processing: a lesson from the archerfish.

The archerfish is a predator with highly unusual visually guided behavior. It is most famous for its ability to hunt by shooting water jets at static or dynamic insect prey, up to two meters above the water's surface. In the lab, the archerfish can learn to distinguish and shoot at artificial targets presented on a computer screen, thus enabling well-controlled experiments. In recent years, these capacities have turned the archerfish into a model animal for studying a variety of visual functions, from visual saliency and visual search, through fast visually guided prediction, and all the way to higher level visual processing such as face recognition. Here we review these recent developments and show how they fall into two emerging lines of research on this animal model. The first is ethologically motivated and emphasizes how the natural environment and habitat of the archerfish interact with its visual processing during predation. The second is driven by parallels to the primate brain and aims to determine whether the latter's characteristic visual information processing capacities can also be found in the qualitatively different fish brain, thereby underscoring the functional universality of certain visual processes. We discuss the differences between these two lines of research and possible future directions.

Coding Schemes in the Archerfish Optic Tectum.

Many studies have yielded valuable knowledge on the early visual system but it is biased since the studies have focused on terrestrial mammals alone. Here, to better account for visual systems in different environments and animal classes, we studied the structure of early visual processing in the archerfish which harnesses its extreme visual ability to hunt by shooting water jets at prey hanging on vegetation above the water. Thus, the archerfish provides a unique opportunity to study visual processing in a vertebrate which is an expert vision-guided predator with a very different brain structure than mammals. The receptive field structures in the archerfish (both sexes) optic tectum, the main visual processing region in the fish brain, were measured and linear non-linear cascades were used to analyze their properties. The findings indicate that the spatial receptive field structures lie on a continuum between circular and elliptical shapes. In addition, the cells' functional properties display a richness of response characteristics, since many cells could be captured by more than a single linear filter. Finally, the non-linear response functions that link linear filters and neuronal responses were found to be similar to the non-linear functions of models that describe terrestrial mammalian single cell activity. Overall our results help to better understand the early visual processing system across vertebrates.

Pop-out in visual search of moving targets in the archer fish.

Pop-out in visual search reflects the capacity of observers to rapidly detect visual targets independent of the number of distracting objects in the background. Although it may be beneficial to most animals, pop-out behaviour has been observed only in mammals, where neural correlates are found in primary visual cortex as contextually modulated neurons that encode aspects of saliency. Here we show that archer fish can also utilize this important search mechanism by exhibiting pop-out of moving targets. We explore neural correlates of this behaviour and report the presence of contextually modulated neurons in the optic tectum that may constitute the neural substrate for a saliency map. Furthermore, we find that both behaving fish and neural responses exhibit additive responses to multiple visual features. These findings suggest that similar neural computations underlie pop-out behaviour in mammals and fish, and that pop-out may be a universal search mechanism across all vertebrates.

Decorrelation of retinal response to natural scenes by fixational eye movements.

Under natural viewing conditions the input to the retina is a complex spatiotemporal signal that depends on both the scene and the way the observer moves. It is commonly assumed that the retina processes this input signal efficiently by taking into account the statistics of the natural world. It has recently been argued that incessant microscopic eye movements contribute to this process by decorrelating the input to the retina. Here we tested this theory by measuring the responses of the salamander retina to stimuli replicating the natural input signals experienced by the retina in the presence and absence of fixational eye movements. Contrary to the predictions of classic theories of efficient encoding that do not take behavior into account, we show that the response characteristics of retinal ganglion cells are not sufficient in themselves to disrupt the broad correlations of natural scenes. Specifically, retinal ganglion cells exhibited strong and extensive spatial correlations in the absence of fixational eye movements. However, the levels of correlation in the neural responses dropped in the presence of fixational eye movements, resulting in effective decorrelation of the channels streaming information to the brain. These observations confirm the predictions that microscopic eye movements act to reduce correlations in retinal responses and contribute to visual information processing.

Visual receptive field properties of cells in the optic tectum of the archer fish.

The archer fish is well known for its extreme visual behavior in shooting water jets at prey hanging on vegetation above water. This fish is a promising model in the study of visual system function because it can be trained to respond to artificial targets and thus to provide valuable psychophysical data. Although much behavioral data have indeed been collected over the past two decades, little is known about the functional organization of the main visual area supporting this visual behavior, namely, the fish optic tectum. In this article we focus on a fundamental aspect of this functional organization and provide a detailed analysis of receptive field properties of cells in the archer fish optic tectum. Using extracellular measurements to record activities of single cells, we first measure their retinotectal mapping. We then determine their receptive field properties such as size, selectivity for stimulus direction and orientation, tuning for spatial frequency, and tuning for temporal frequency. Finally, on the basis of all these measurements, we demonstrate that optic tectum cells can be classified into three categories: orientation-tuned cells, direction-tuned cells, and direction-agnostic cells. Our results provide an essential basis for future investigations of information processing in the archer fish visual system.

Visual acuity in the archerfish: behavior, anatomy, and neurophysiology.

Archerfish are known for their remarkable behavior of shooting water jets at prey hanging on vegetation above water. Motivated by the fish's capacity to knock down small prey as high as two meters above water level, we studied the role of the retina in facilitating their excellent visual acuity. First, we show behaviorally that archerfish (Toxotes jaculatrix) can detect visual structures with a minimum angle of resolution in the range of 0.075°-0.15°. Then, combining eye movement measurements with a ray tracing method, we show that the image of a target on the retina coincides with the area centralis at the ventro-temporal retina. Moving down to retinal neural circuits, we then examine the ratio by which retinal ganglion cells multiplex visual information from the photoreceptors. Measuring the anatomical densities of both cell types in the area centralis, we found photoreceptor spacing to be 5.8 µm, which supports a minimum angle of resolution as low as 0.073°. Similarly, the average spacing of the ganglion cells was 5.7 µm. Based on electrophysiological measurements we found the smallest receptive fields of ganglion cells in that area to be in the range of 8-16 µm, which translates to an angular width of 0.1°-0.2°. These findings indicate that retinal ganglion cells in the area centralis stream information to the brain at a comparable resolution with which it is sampled by the photoreceptors. Thus, the archerfish can be used as an animal model for studying how visual details are streamed to the brain by retinal output.

The effects of rhythmicity and amplitude on transfer of motor learning.

We perform rhythmic and discrete arm movements on a daily basis, yet the motor control literature is not conclusive regarding the mechanisms controlling these movements; does a single mechanism generate both movement types, or are they controlled by separate mechanisms? A recent study reported partial asymmetric transfer of learning from discrete movements to rhythmic movements. Other studies have shown transfer of learning between large-amplitude to small-amplitude movements. The goal of this study is to explore which aspect is important for learning to be transferred from one type of movement to another: rhythmicity, amplitude or both. We propose two hypotheses: (1) Rhythmic and discrete movements are generated by different mechanisms; therefore we expect to see a partial or no transfer of learning between the two types of movements; (2) Within each movement type (rhythmic/discrete), there will be asymmetric transition of learning from larger movements to smaller ones. We used a learning-transfer paradigm, in which 70 participants performed flexion/extension movements with their forearm, and switched between types of movement, which differed in amplitude and/or rhythmicity. We found partial transfer of learning between discrete and rhythmic movements, and an asymmetric transfer of learning from larger movements to smaller movements (within the same type of movement). Our findings suggest that there are two different mechanisms underlying the generation of rhythmic and discrete arm movements, and that practicing on larger movements helps perform smaller movements; the latter finding might have implications for rehabilitation.