Integration of Olfactory Bulb Output in the Zebrafish Telencephalon analyzed by Electrophysiology and 2-Photon Ca2+ - Imaging

To understand how the brain generates representations of the external world it is crucial to analyze the processing of sensory information between early processing centers and higher brain regions. In the first olfactory relay, the olfactory bulb (OB), odors are represented by dynamic patterns of activity across the population of principal neurons, the mitral cells. During an odor response, subsets of mitral cells synchronize their action potentials and convey information that is different from the information contained in non-synchronized firing patterns. It is, however, poorly understood how these combinatorial representations are further processed in higher brain areas. I used a small vertebrate model system, the zebrafish, to examine how neurons in the dorsal posterior telencephalon (Dp), a direct target of OB output that is homologous to olfactory cortex, extract information from OB output activity patterns. Using 2-photon Ca2+ - imaging and whole-cell patch-clamp recordings, I found that individual Dp neurons receive input from diverse sets of mitral cells. Unlike in mitral cells, responses of Dp neurons to binary mixtures of odors could not be predicted from their responses to the components. Electrophysiological and pharmacological results demonstrated that suprathreshold responses are controlled by the convergence of excitatory and inhibitory pathways in single Dp neurons. I next analyzed the temporal integration properties of neurons and neuronal circuits to examine whether neurons in Dp may selectively extract the information contained in synchronized mitral cells spikes. No evidence for coincidence detection mechanisms was found; rather, action potential firing is controlled primarily by a slow membrane depolarization. In conclusion, the readout of information in Dp is determined by a balance of slow excitatory and inhibitory inputs that allows Dp neurons to detect defined patterns of excitation and inhibition across the population of mitral cells in the olfactory bulb. This mechanism does not depend on the synchronization of inputs and mediates the association of information about multiple molecular features of an odor stimulus. Together, these data suggest that neurons in Dp form synthetic representations of olfactory objects