Mammalian octopus cells are direction selective to frequency sweeps by excitatory synaptic sequence detection

Octopus cells are remarkable projection neurons of the mammalian cochlear nucleus, with extremely fast membranes and wide-frequency tuning. They are considered prime examples of coincidence detectors but are poorly characterized in vivo. We discover that octopus cells are selective to frequency sweep direction, a feature that is absent in their auditory nerve inputs. In vivo intracellular recordings reveal that direction selectivity does not derive from across-frequency coincidence detection but hinges on the amplitudes and activation sequence of auditory nerve inputs tuned to clusters of hot spot frequencies. A simple biophysical octopus cell model excited with real nerve spike trains recreates direction selectivity through interaction of intrinsic membrane conductances with the activation sequence of clustered excitatory inputs. We conclude that octopus cells are sequence detectors, sensitive to temporal patterns across cochlear frequency channels. The detection of sequences rather than coincidences is a much simpler but powerful operation to extract temporal information.

Automated summary

Octopus cells in the mammalian cochlear nucleus are remarkable neurons that have fast membranes and wide-frequency tuning. They exhibit direction selectivity in response to frequency sweeps, which is not present in their auditory nerve inputs. The selectivity is achieved through the interaction between the activation sequence of auditory nerve inputs and intrinsic membrane conductances. This finding suggests that octopus cells are sequence detectors, sensitive to temporal patterns across different cochlear frequency channels.