Home, head direction stability, and grid cell distortion

The home is a unique location in the life of humans and animals. In rats, home presents itself as a multicompartmental space that involves integrating navigation through subspaces. Here we embedded the laboratory rat’s home cage in the arena, while recording neurons in the animal’s parasubiculum and medial entorhinal cortex, two brain areas encoding the animal’s location and head direction. We found that head direction signals were unaffected by home cage presence or translocation. Head direction cells remain globally stable and have similar properties inside and outside the embedded home. We did not observe egocentric bearing encoding of the home cage. However, grid cells were distorted in the presence of the home cage. While they did not globally remap, single firing fields were translocated toward the home. These effects appeared to be geometrical in nature rather than a home-specific distortion and were not dependent on explicit behavioral use of the home cage during a hoarding task. Our work suggests that medial entorhinal cortex and parasubiculum do not remap after embedding the home, but local changes in grid cell activity overrepresent the embedded space location and might contribute to navigation in complex environments

Unsupervised discovery of behaviorally relevant brain states in rats playing hide-and-seek

In classical neuroscience experiments, neural activity is measured across many identical trials of animals performing simple tasks and is then analyzed, associating neural responses to pre-defined experimental parameters. This type of analysis is not suitable for patterns of behavior that unfold freely, such as play behavior. Here, we attempt an alternative approach for exploratory data analysis on a single-trial level, applicable in more complex and naturalistic behavioral settings in which no two trials are identical. We analyze neural population activity in the prefrontal cortex (PFC) of rats playing hide-and-seek and show that it is possible to discover what aspects of the task are reflected in the recorded activity with a limited number of simultaneously recorded cells (% 31). Using hidden Markov models, we cluster population activity in the PFC into a set of neural states, each associated with a pattern of neural activity. Despite high variability in behavior, relating the inferred states to the events of the hide-and-seek game reveals neural states that consistently appear at the same phases of the game. Furthermore, we show that by applying the segmentation inferred from neural data to the animals’ behavior, we can explore and discover novel correlations between neural activity and behavior. Finally, we replicate the results in a second dataset and show that population activity in the PFC displays distinct sets of states during playing hide-and-seek and observing others play the game. Overall, our results reveal robust, state-like representations in the rat PFC during unrestrained playful behavior and showcase the applicability of population analyses in naturalistic neuroscience

Play, but not observing play, engages rat medial prefrontal cortex

Rats have elaborate cognitive capacities for playing Hide & Seek. Playing Hide & Seek strongly engages medial prefrontal cortex and the activity of prefrontal cortex neurons reflects the structure of the game. We wondered if prefrontal neurons would also show a mirroring of play‐related neural activity. Specifically, we asked how does the activity in the rat medial prefrontal cortex differ when the animal plays itself versus when it observes others playing. Consistent with our previous work, when the animal plays itself we observed medial prefrontal cortex activity that was sharply locked to game events. Observing play, however, did not lead to a comparable activation of rat medial prefrontal cortex. Firing rates during observing play were lower than during real play. The modulation of responses in medial prefrontal cortex by game events was strong during playing Hide & Seek, but weak during observing Hide & Seek. We conclude the rat prefrontal cortex does not mirror play events under our experimental conditions.Peer Reviewe

Motor patterns during active electrosensory acquisition

Hofmann V, Geurten B, Sanguinetti-Scheck JI, Gomez-Senna L, Engelmann J. Motor patterns during active electrosensory acquisition. Frontiers in Behavioral Neuroscience. 2014;8:186.Motor patterns displayed during active electrosensory acquisition of information seem to be an essential part of a sensory strategy by which weakly electric fish actively generate and shape sensory flow. These active sensing strategies are expected to adaptively optimize ongoing behavior with respect to either motor efficiency or sensory information gained. The tight link between the motor domain and sensory perception in active electrolocation make weakly electric fish like Gnathonemus petersii an ideal system for studying sensory-motor interactions in the form of active sensing strategies. Analyzing the movements and electric signals of solitary fish during unrestrained exploration of objects in the dark, we here present the first formal quantification of motor patterns used by fish during electrolocation. Based on a cluster analysis of the kinematic values we categorized the basic units of motion. These were then analyzed for their associative grouping to identify and extract short coherent chains of behavior. This enabled the description of sensory behavior on different levels of complexity: from single movements, over short behaviors to more complex behavioral sequences during which the kinematics alter between different behaviors. We present detailed data for three classified patterns and provide evidence that these can be considered as motor components of active sensing strategies. In accordance with the idea of active sensing strategies, we found categorical motor patterns to be modified by the sensory context. In addition these motor patterns were linked with changes in the temporal sampling in form of differing electric organ discharge frequencies and differing spatial distributions. The ability to detect such strategies quantitatively will allow future research to investigate the impact of such behaviors on sensing

Two pup vocalization types are genetically and functionally separable in deer mice

Vocalization is a widespread vertebrate social behavior that is essential for fitness in the wild. While many vocal behaviors are highly conserved, heritable features of specific vocalization types can vary both within and between species, raising the questions of why and how some vocal behaviors evolve. Here, using new computational tools to automatically detect and cluster vocalizations into distinct acoustic categories, we compare pup isolation calls across neonatal development in eight taxa of deer mice (genusPeromyscus) and compare them to laboratory mice (C57Bl6/j strain) and free-living, wild house mice (Mus musculus musculus). Whereas bothPeromyscusandMuspups produce ultrasonic vocalizations (USVs),Peromyscuspups also produce a second call type with acoustic features, temporal rhythms, and developmental trajectories that are distinct from those of USVs. In deer mice, these tonal and low frequency “cries” are predominantly emitted in postnatal days one through nine, while USVs are primarily made after day nine. Using playback assays, we show that cries result in a more rapid approach byPeromyscusmothers than USVs, suggesting a role for cries in eliciting parental care early in neonatal development. Using genetic crosses between two sister species of deer mice exhibiting large, innate differences in the acoustic structure of cries and USVs, we find that variation in vocalization rate, duration, and pitch display different degrees of genetic dominance and that cry and USV features can be uncoupled in second-generation hybrids. Taken together, this work shows that vocal behavior can evolve quickly between closely related rodent species in which vocalization types, likely serving distinct functions in communication, are controlled by distinct genetic loci

Fish Geometry and Electric Organ Discharge Determine Functional Organization of the Electrosensory Epithelium

Active electroreception in Gymnotus omarorum is a sensory modality that perceives the changes that nearby objects cause in a self generated electric field. The field is emitted as repetitive stereotyped pulses that stimulate skin electroreceptors. Differently from mormyriformes electric fish, gymnotiformes have an electric organ distributed along a large portion of the body, which fires sequentially. As a consequence shape and amplitude of both, the electric field generated and the image of objects, change during the electric pulse. To study how G. omarorum constructs a perceptual representation, we developed a computational model that allows the determination of the self-generated field and the electric image. We verify and use the model as a tool to explore image formation in diverse experimental circumstances. We show how the electric images of objects change in shape as a function of time and position, relative to the fish's body. We propose a theoretical framework about the organization of the different perceptive tasks made by electroreception: 1) At the head region, where the electrosensory mosaic presents an electric fovea, the field polarizing nearby objects is coherent and collimated. This favors the high resolution sampling of images of small objects and perception of electric color. Besides, the high sensitivity of the fovea allows the detection and tracking of large faraway objects in rostral regions. 2) In the trunk and tail region a multiplicity of sources illuminate different regions of the object, allowing the characterization of the shape and position of a large object. In this region, electroreceptors are of a unique type and capacitive detection should be based in the pattern of the afferents response. 3) Far from the fish, active electroreception is not possible but the collimated field is suitable to be used for electrocommunication and detection of large objects at the sides and caudally

Neural bases of navigation in foraging and play

Für die meisten Säugetiere ist Navigation eine essentielle kognitive Fähigkeit. Im Bereich der Neurowissenschaften gab es immense Fortschritte im Verständnis neuronaler Grundlagen von Navigation. Diese Dissertation beschäftigt sich mit der neuronalen Grundlage von Navigation im Hinblick auf Hirnstruktur (d.h. Parasubikulum) und ethologisch relevante Verhaltensweisen (d.h. Heimkehr und Spielverhalten). Im ersten Kapitel konzentriere ich mich auf das Verhältnis von Struktur und Funktion im Parasubikulum. Wir postulieren, dass das Parasubikulum durch seine selektive Vernetzung mit dem entorhinalen Kortex, durch seine starke interne Konnektivität, sowie wegen dem hohen Grad räumlich selektiver Aktivitätsmuster seiner Neurone im Bezug auf die Kontrolle von Gitterzellaktivität und räumlicher Navigation eine herausragende Stellung einnimmt. Im zweiten Kapitel untersuche ich die neuronale Grundlage von Heimkehr. Wir nutzen die starke Verbundenheit von Laborratten zu ihrem Zuhause. Wir zeigen, dass das Parasubikulum und der entorhinale Kortex keinen expliziten Heimvektor besitzen und dass die Präsenz des Zuhauses keine globale Veränderung der neuralen Repräsentation des Raums hervorruft. Allerdings führte die Präsenz des Zuhauses oder anderer geometrischer Objekte zu einer Verzerrung von Gitterzellen. Im dritten Kapitel unteruche ich Navigation im Hinblick auf Spielverhalten. Ratten erlernen das Versteckspiel schnell und verhalten sich erstaunlich regelkonform. Zeigen Ratten spielspezifische Vokalisationen. Gleichzeitige Ableitungen neuronaler Aktivität im medialen präfrontalen Kortex offenbarten starke und spezifische Antworten der meisten Nervenzellen auf verschiedene Phasen des Spiels des spezifischen Spielkontextes wiederspiegeln. Diese Arbeit liefert durch ihren ethologischen Ansatz und durch Verhaltensanalysen von sich frei verhaltenden Tieren einen wichtigen Beitrag zum besseren Verständnis neuronaler Grundlagen von Navigation im Säugetiergehirn.Navigation is an essential cognitive skill in the life of most animals. Animals move along space to procure the advantages of different places in the environment, and to adapt to ever changing resources, dangers and needs. This thesis addresses the neural bases of navigation in the context of brain structure (i.e. the parasubiculum) and ethologically relevant behaviors (i.e. homing and playing). In the first chapter I focus on the structure function relation of the parasubiculum: an understudied area of the rat’s parahippocampal cortex. We performed the most comprehensive study of the parasubiculum up to date and propose that, because of its selective connectivity with the medial entorhinal cortex, its internal connectivity, and the high spatial and head directional tuning of its neurons, the parasubiculum sits in remarkable position to control grid cell activity and navigation. In the second chapter, I study the neural bases of homing. We use the lab-rat' s strong attachment to its home cage to study whether brains maintain an online home vector. We show, that the parasubiculum and medial entorhinal cortex do not have an explicit home vector representation, and that the presence of home did not affect global encoding of space. However, we do find that grid cells are distorted by the home or other geometrical features affecting the internal environment. In the third chapter, I study navigation in an interspecies role-playing game. We played 'Hide and Seek' with rats and found that they acquired the game easily and played by the rules. Rats were strategic and developed game specific vocalizations patterns. We recorded from the medial prefrontal cortex and found that neurons respond sharply to different phases of the game, and may encode as well the context in which this events take place. By emphasizing ethological approaches and free behaviors this thesis contributes to an increased understanding of the neural underpinnings of navigation in the mammalian brain

Electrorrecepción activa :Formación de imágenes, claves sensoriales y esquemas sensorio-motores

Tribunal: Dr. Omar Macadar, Dr. Kirsty Grant, Dr. Eduardo Mizraji.Orientador: Dr. Leonel Gómez-Sen

Sensory flow as a basis for a novel distance cue in freely behaving electric fish

Hofmann V, Sanguinetti-Scheck JI, Gómez-Sena L, Engelmann J. Sensory flow as a basis for a novel distance cue in freely behaving electric fish. The Journal of neuroscience : the official journal of the Society for Neuroscience. 2017;37(2):302-312.The sensory input that an animal receives is directly linked to its motor activity. Behavior thus enables animals to influence their sensory input, a concept referred to as active sensing. How such behavior can serve as a scaffold for generating sensory information is of general scientific interest. In this article, we investigate how behavior can shape sensory information by using some unique features of the sensorimotor system of the weakly electric fish.Based on quantitative behavioral characterizations and computational reconstruction of sensory input, we show how electrosensory flow is actively created during highly patterned, spontaneous behavior in Gnathonemus petersii The spatiotemporal structure of the sensory input provides information for the computation of a novel distance cue, which allows for a continuous estimation of distance. This has significant advantages over previously known non-dynamic distance estimators as determined from electric image blur.Our investigation of the sensorimotor interactions in pulsatile electrolocation show, for the first time, that the electrosensory flow contains behaviorally relevant information only accessible through active behavior. As patterned sensory behaviors are a shared feature of (active) sensory systems, our results have general implications for the understanding of (active) sensing, with the proposed sensory flow based-measure being potentially pertinent to a broad range of sensory modalities. SIGNIFICANCE STATEMENT: Acquisition of sensory information depends on motion, as either an animal or its sensors move. Behavior can thus actively influence the sensory flow, and in this way, behavior can be seen as a manifestation of the brain's integrative functions. The properties of the active pulsatile electrolocation system in Gnathonemus petersii allow for the sensory input to be computationally reconstructed, enabling us to link the informational content of spatiotemporal sensory dynamics to behavior. Our study reveals a novel sensory cue for estimating depth that is actively generated by the fishes' behavior. The physical and behavioral similarities between electrolocation and other active sensory systems suggest that this may be a mechanism shared by (active) sensory systems. Copyright 2016 the authors