Automated Segmentation of the Mouse Body Language to Study Stimulus-Evoked Emotional Behaviors.

Understanding the neural basis of emotions is a critical step to uncover the biological substrates of neuropsychiatric disorders. To study this aspect in freely behaving mice, neuroscientists have relied on the observation of ethologically relevant bodily cues to infer the affective content of the subject, both in neutral conditions or in response to a stimulus. The best example of that is the widespread assessment of freezing in experiments testing both conditioned and unconditioned fear responses. While robust and powerful, these approaches come at a cost: they are usually confined within selected time windows, accounting for only a limited portion of the complexity of emotional fluctuation. Moreover, they often rely on visual inspection and subjective judgment, resulting in inconsistency across experiments and questionable result interpretations. To overcome these limitations, novel tools are arising, fostering a new avenue in the study of the mouse naturalistic behavior. In this work we developed a computational tool [stimulus-evoked behavioral tracking in 3D for rodents (SEB3R)] to automate and standardize an ethologically driven observation of freely moving mice. Using a combination of machine learning-based behavioral tracking and unsupervised cluster analysis, we identified statistically meaningful postures that could be used for empirical inference on a subsecond scale. We validated the efficacy of this tool in a stimulus-driven test, the whisker nuisance (WN) task, where mice are challenged with a prolonged and invasive whisker stimulation, showing that identified postures can be reliably used as a proxy for stimulus-driven fearful and explorative behaviors.

Hippocampus and medial striatum dissociation during goal navigation by geometry or features in the domestic chick: An immediate early gene study.

We employed a standard reference memory task to study the involvement of the hippocampal formation (HF) of domestic chicks that used the boundary geometry of a test environment to orient to and locate a reward. Using the immediate early gene product c-Fos as a neuronal activity marker, we found enhanced HF activation in chicks that learned to locate rewarded corners using the shape of a rectangular arena compared to chicks trained to solve the task by discriminating local features in a square-shaped arena. We also analyzed neuronal activity in the medial part of the medial striatum (mMSt). Surprisingly, in mMSt we observed a reverse pattern, with higher activity in the chicks that were trained to locate the goal by local features. Our results identify two seemingly parallel, memory systems in chicks, with HF central to the processing of spatial-geometrical information and mMSt important in supporting local feature discrimination.

Visual hierarchical processing and lateralization of cognitive functions through domestic chicks' eyes.

Hierarchical stimuli have proven effective for investigating principles of visual organization in humans. A large body of evidence suggests that the analysis of the global forms precedes the analysis of the local forms in our species. Studies on lateralization also indicate that analytic and holistic encoding strategies are separated between the two hemispheres of the brain. This raises the question of whether precedence effects may reflect the activation of lateralized functions within the brain. Non-human animals have perceptual organization and functional lateralization that are comparable to that of humans. Here we trained the domestic chick in a concurrent discrimination task involving hierarchical stimuli. Then, we evaluated the animals for analytic and holistic encoding strategies in a series of transformational tests by relying on a monocular occlusion technique. A local precedence emerged in both the left and the right hemisphere, adding further evidence in favour of analytic processing in non-human animals.

Spatial reorientation by geometry with freestanding objects and extended surfaces: a unifying view.

The macroscopic, three-dimensional surface layout geometry of an enclosure apparently provides a different contribution for spatial reorientation than the geometric cues associated with freestanding objects arranged in arrays with similar geometric shape. Here, we showed that a unitary spatial representation can account for the capability of animals to reorient both by extended surfaces and discrete objects in a small-scale spatial task. We trained domestic chicks to locate a food-reward from an opening on isolated cylinders arranged either in a geometrically uninformative (square-shaped) or informative (rectangular-shaped) arrays. The arrays were located centrally within a rectangular-shaped enclosure. Chicks trained to access the reward from a fixed position of openings proved able to reorient according to the geometric cues specified by the shape of the enclosure in all conditions. Chicks trained in a fixed position of opening with geometric cues provided both by the arena and the array proved able to reorient according to each shape separately. However, chicks trained to access the reward from a variable position of openings failed to reorient. The results suggest that the physical constrains associated with the presence of obstacles in a scene, rather than their apparent visual extension, are crucial for spatial reorientation.

From natural geometry to spatial cognition.

A review of selected works on spatial memory in animals and humans is presented, and some ideas about the encoding of geometry and its role in evolution are presented, based on recently accumulated evidence from psychology, ethology and the neurosciences. It is argued that comparative analyses at the level of both spatial navigation behaviors and their underlying neural mechanisms may provide a solid foundation for the biological origins of organisms' spontaneous ability in dealing with geometric concepts. To this aim, the representations of space underlying memory tasks involving discrete (i.e., landmark arrays) or continuous elements (i.e., enclosed environments) are evaluated and compared as regards the impact of their geometric arrangement.

Stable panoramic views facilitate snap-shot like memories for spatial reorientation in homing pigeons.

Following spatial disorientation, animals can reorient themselves by relying on geometric cues (metric and sense) specified both by the macroscopic surface layout of an enclosed space and prominent visual landmarks in arrays. Whether spatial reorientation in arrays of landmarks is based on explicit representation of the geometric cues is a matter of debate. Here we trained homing pigeons (Columba livia) to locate a food-reward in a rectangular array of four identical or differently coloured pipes provided with four openings, only one of which allowed the birds to have access to the reward. Pigeons were trained either with a stable or a variable position of the opening on pipes, so that they could view the array either from the same or a variable perspective. Explicit mapping of configural geometry would predict successful reorientation irrespective of access condition. In contrast, we found that a stable view of the array facilitated spatial learning in homing pigeons, likely through the formation of snapshot-like memories.

Olfactory lateralization in homing pigeons: a GPS study on birds released with unilateral olfactory inputs.

A large body of evidence has shown that pigeons rely on an olfactory-based navigational map when homing from unfamiliar locations. Previous studies on pigeons released with one nostril occluded highlighted an asymmetry in favour of the right nostril, particularly concerning the initial orientation performance of naïve birds. Nevertheless, all pigeons experiencing only unilateral olfactory input showed impaired homing, regardless of the side of the occluded nostril. So far this phenomenon has been documented only by observing the birds' vanishing bearings. In the present work we recorded the flight tracks of pigeons with previous homing experience equipped with a GPS data logger and released from an unfamiliar location with the right or the left nostril occluded. The analysis of the tracks revealed that the flight path of the birds with the right nostril occluded was more tortuous than that of unmanipulated controls. Moreover, the pigeons smelling with the left nostril interrupted their journey significantly more frequently and displayed more exploratory activity than the control birds, e.g. during flights around a stopover site. These data suggest a more important involvement of the right olfactory system in processing the olfactory information needed for the operation of the navigational map.

View-based strategy for reorientation by geometry.

Human and non-human animals can use geometric information (metric information and left-right discrimination sense) to reorient themselves in an environment. The hypothesis that in so doing they rely on allocentric (map-like) representations has received wide consensus. However, theoretical models suggest that egocentric representations may represent efficient strategies for visuo-spatial navigation. Here, we provide, for the first time, evidence that a view-based strategy is effectively used by animals to reorient themselves in an array of landmarks. Domestic chicks were trained to locate a food-reward in a rectangular array of either four indistinguishable or distinctive pipes. In the key experimental series, the pipes had four openings, only one of which allowed the chicks to access the reward. The direction of the open access relative to the array was either maintained stable or it was changed throughout training. The relative position of the pipes in the array was maintained stable in both training conditions. Chicks reoriented according to configural geometry as long as the open access pointed in the same direction during training but failed when the positions of the openings was changed throughout training. When the correct pipe was characterized by a distinctive featural cue, chicks learnt to locate the reward irrespective of the stability of the direction to openings, indicating that place-navigation was dissociated from non-spatial learning. These findings provide evidence that view-based strategies to reorient by geometry could be used by animals.

Reorienting strategies in a rectangular array of landmarks by domestic chicks (Gallus gallus).

Spatial reorientation in a rectangular array of four landmarks located in the center of a circular enclosure was investigated in domestic chicks (Gallus gallus). One of the landmark possessed unique visual features, indicating the location of a food reward. After training, chicks were tested (a) with the same array as during the training; (b) with four identical landmarks of the type previously nonrewarded, of the type previously rewarded, or of a new type; (c) after having transformed one of the landmarks located at the geometric incorrect location into the type of landmark previously rewarded; or (d) with a fifth landmark of the rewarded type at a new location. Chicks encoded information provided by local featural cues but not the geometric information provided by the shape of the array. Moreover, when trained in a rectangular array of identical landmarks chicks failed to reorient. In a second series of experiments, the array was located in correspondence to the corners of a rectangular enclosure. This time chicks successfully learned to locate the reward using geometric information. However, when the rectangular array was located in the center of a larger rectangular enclosure, chicks failed to reorient, indicating that the geometric information given by the macroscopic layout of arena surfaces was not used to specify different locations. These results suggest that chicks reorient on the basis of a local representation of single landmarks and that encoding of the global aspects of geometry only occurs with respect to the large, extended surfaces of an enclosure.

Olfactory lateralization in homing pigeons: initial orientation of birds receiving a unilateral olfactory input.

It has been shown that homing pigeons (Columba livia) rely on olfactory cues to navigate from unfamiliar locations. In fact, the integrity of the olfactory system, from the olfactory mucosa to the piriform cortex, is required for pigeons to navigate over unfamiliar areas. Recently it has been shown that there is a functional asymmetry in the piriform cortex, with the left piriform cortex more involved in the use of the olfactory navigational map than the right piriform cortex. To investigate further the lateralization of the olfactory system in relation to navigational processes in carrier pigeons, we compared their homing performance after either their left or the right nostril was plugged. Contrary to our expectations, we observed an impairment in the initial orientation of the pigeons with their right nostril plugged. However, both groups released with one nostril plugged tended to be poorer than control pigeons in their homing performance. The observed asymmetry in favour of the right nostril might be due to projections from the olfactory bulbs to the contralateral globus pallidum, a structure involved in motor responses.

Functional asymmetry of left and right avian piriform cortex in homing pigeons' navigation.

It has been shown that homing pigeons rely on olfactory cues to navigate over unfamiliar areas and that any kind of olfactory impairment produces a dramatic reduction of navigational performance from unfamiliar sites. The avian piriform cortex is the main projection field of olfactory bulbs and it is supposed to process olfactory information; not surprisingly bilateral lesions to this telencephalic region disrupt homing pigeon navigation. In the present study, we attempted to assess whether the left and right piriform cortex are differentially involved in the use of the olfactory navigational map. Therefore, we released from unfamiliar locations pigeons subjected, when adult, to unilateral ablation of the piriform cortex. After being released, the pigeons lesioned to the right piriform cortex orientated similarly to the intact controls. On the contrary, the left lesioned birds were significantly more scattered than controls, showing a crucial role of the left piriform cortex in processing the olfactory cues needed for determining the direction of displacement. However, both lesioned groups were significantly slower than controls in flying back to the home loft, showing that the integrity of both sides of the piriform cortex is necessary to accomplish the whole homing process.