Dynamic representation of 3D auditory space in the midbrain of the free-flying echolocating bat

Abstract

Essential to spatial orientation in the natural environment is a dynamic representation of direction and distance to objects. Despite the importance of 3D spatial localization to parse objects in the environment and to guide movement, most neurophysiological investigations of sensory mapping have been limited to studies of restrained subjects, tested with 2D, artificial stimuli. Here, we show for the first time that sensory neurons in the midbrain superior colliculus (SC) of the free-flying echolocating bat encode 3D egocentric space, and that the bat's inspection of objects in the physical environment sharpens tuning of single neurons, and shifts peak responses to represent closer distances. These findings emerged from wireless neural recordings in free-flying bats, in combination with an echo model that computes the animal's instantaneous stimulus space. Our research reveals dynamic 3D space coding in a freely moving mammal engaged in a real-world navigation task.

Natural switches in behaviour rapidly modulate hippocampal coding

“…therefore, had to be attentive to avoid collision between one another. To measure the bats' attention, we recorded their echolocation clicks (sonar signals), because many bat species have been shown to increase echolocation click rate when attention is needed; thus, echolocation provides an index of the bat's moment-to-moment attention [1][2][3][4][5][6][7][8][9] . Indeed, we found that, during cross-overs, the bats increased their echolocation click rate by around fourfold and click amplitude by around twofold (Fig.…”

“…1d-f and Extended Data Fig. 2), which suggests that they are attending to the other bat at these distances [1][2][3][4][5][6][7][8][9][38][39][40][41] ; to enable the analysis of an extra baseline, we considered a larger and symmetrical distance window of ±40 m, which enabled us to detect neuronal modulations and their return to baseline activity. Cross-overs that occurred less than 8 m from the landing balls were excluded from the analysis to avoid effects of landing and take-off (see the light grey vertical rectangles in Fig.…”

“…To test how attention modulates the distance tuning curves and firing rates of the neurons during cross-overs, we used the increase in echolocation click rate as an index of attention [1][2][3][4][5][6][7][8][9][38][39][40][41] . For 1D distance cells that were recorded simultaneously with audio (which was performed in one bat), we divided the cross-over flights into two equally sized groups according to the click rate (median bisection).…”

“…Here we tested this question using an ethological setting: two bats flew together in a long 135 m tunnel, and switched between navigation when flying alone (solo) and collision avoidance as they flew past each other (cross-over). Bats increased their echolocation click rate before each cross-over, indicating attention to the other bat [1][2][3][4][5][6][7][8][9] . Hippocampal CA1 neurons represented the bat's own position when flying alone (place coding [10][11][12][13][14] ).…”

Motor Control: Three-Dimensional Metric of Head Movements in the Mouse Brain

“…The absence of strong roll representation by head-motion and head-direction cells across species might relate to the fact that roll does not define the heading direction in threedimensional space, and thus might be less ethologically relevant for orienting behavior and navigation [16]. Notably, recent recordings in the superior colliculus of echolocating bats revealed neurons tuned to object position in egocentric threedimensional space [17]. The distance tuning of these neurons became shorter when bats actively inspected objects in the environment, suggesting that multidimensional neural representations in the superior colliculus could be modulated dynamically according to the behavioral needs of the animal.…”