Toric spines at a site of learning

Abstract

We discovered a new type of dendritic spine. It is found on space-specific neurons in the barn owl inferior colliculus, a site of experience-dependent plasticity. Connectomic analysis revealed dendritic protrusions of unusual morphology including topological holes, hence termed ‘toric’ spines (n = 76). More significantly, presynaptic terminals converging onto individual toric spines displayed numerous active zones (up to 49) derived from multiple axons (up to 11) with incoming trajectories distributed widely throughout 3D space. This arrangement is suited to integrate input sources. Dense reconstruction of two toric spines revealed that they were unconnected with the majority (∼84%) of intertwined axons, implying a high capacity for information storage. We developed an ex vivo slice preparation and provide the first published data on space-specific neuron intrinsic properties, including cellular subtypes with and without toric-like spines. We propose that toric spines are a cellular locus of sensory integration and behavioral learning.

Significance statement The majority of excitatory synapses in the brain are formed onto dendritic spines, which typically act to isolate the action of individual synapses. We discovered a new type of spine which in contrast receives convergent input from many different axons. These ‘toric’ spines, named for their topological holes, are found on space-specific neurons in the barn owl auditory system. We used a combination of in vivo electrophysiology, super-resolution optical microscopy and serial block electron microscopy to characterize the ultrastructure and wiring of toric spines, and ex vivo patch clamp recording to elucidate the cells’ electrical properties. These data lead us to propose that toric spines serve as microanatomical hubs for neuronal computation, plasticity and learning.