A circuit for heading direction estimation in the zebrafish anterior hindbrain

Petrucco, Luigi (2022): A circuit for heading direction estimation in the zebrafish anterior hindbrain. Dissertation, LMU München: Graduate School of Systemic Neurosciences (GSN)

Abstract

To successfully navigate their environment, animals may generate an inter- nal representation of the environment that can be updated based on sensory cues or internally generated motor commands. Head-direction cells, neu- rons that fire when the animal faces a particular direction in space have been recorded in various areas of the vertebrate brain. The dynamics of heading direction circuits are well by described by ring attractor networks, where a ring attractor organizes the activity of the circuit and positions along the ring represent the heading direction. Although this model has found remarkable validation in the invertebrate central complex, the anatomical dissection of a ring attractor circuit has been elusive in the vertebrate brain. Here, I report experimental observations in the larval zebrafish that high- light a possible role of the interpenducular nucleus (IPN) and a connected area, the anterior hindbrain, in generating heading direction-related signals. The internal organization of the interpeduncular nucleus is poorly un- derstood. In the first part of this thesis, I will present anatomical recon- structions that provide crucial insights in the organization of this struc- ture in the larval zebrafish. I will show that 1) the internal circuitry of the ventral IPN is organized in a fix number of glomeruli, domains of neuropil that receive dense and segregated dendritic and axonal arborizations and exhaustively tile the ventral IPN; and that 2) neurons in the anterior hind- brain dorsal from the interpeduncular nucleus contribute many dendritic and axonal projections to the IPN neuropil. In the second part of the thesis, I will describe a population of r1π neu- rons in the anterior hindbrain that exhibit a highly constrained dynamics lying on a ring manifold in the phase space of the network. Intriguingly, clock- and counterclock-wise shifts along this manifold correspond to left and right movements of the fish, so that the network state can keep track of current heading direction. The dynamics of the network full-fills several criteria that define a head-direction network: 1) There is a sustained and unique bump of activity that translates across the network (uniqueness); 2) the activity shifts in opposite directions when the animal perform leftward and rightward movements (integration); 3) activation of the network is sta- ble over tens of seconds in the absence of motion (persistence). Finally, I will turn back to the anatomy of r1π neurons and show how they could connect with each other in the IPN according to their proximity in activity space, and I will conclude by proposing a mechanistic model for the organization of the ring network dynamics. Together, these data repre- sent the first observation of a head-direction network with an anatomical organization in the vertebrate brain.

• Dokumententyp: Dissertationen (Dissertation, LMU München)
• Keywords: neuroscience, zebrafish, imaging, navigation, ring attractor, electron microscopy, anatomy, hindbrain, interpeduncular
• Themengebiete: 500 Naturwissenschaften und Mathematik ; 500 Naturwissenschaften und Mathematik > 570 Biowissenschaften, Biologie
• Fakultäten: Graduate School of Systemic Neurosciences (GSN)
• Sprache der Hochschulschrift: Englisch
• Datum der mündlichen Prüfung: 1. Juli 2022
• 1. Bericht­erstatter:in: Portugues, Ruben