Neuronal dendrites are electrically excitable: they can generate regenerative events such as dendritic spikes in response to sufficiently strong synaptic input1,2,3. Although such events have been observed in many neuronal types4,5,6,7,8,9, it is not well understood how active dendrites contribute to the tuning of neuronal output in vivo. Here we show that dendritic spikes increase the selectivity of neuronal responses to the orientation of a visual stimulus (orientation tuning). We performed direct patch-clamp recordings from the dendrites of pyramidal neurons in the primary visual cortex of lightly anaesthetized and awake mice, during sensory processing. Visual stimulation triggered regenerative local dendritic spikes that were distinct from back-propagating action potentials. These events were orientation tuned and were suppressed by either hyperpolarization of membrane potential or intracellular blockade of NMDA (N-methyl-d-aspartate) receptors. Both of these manipulations also decreased the selectivity of subthreshold orientation tuning measured at the soma, thus linking dendritic regenerative events to somatic orientation tuning. Together, our results suggest that dendritic spikes that are triggered by visual input contribute to a fundamental cortical computation: enhancing orientation selectivity in the visual cortex. Thus, dendritic excitability is an essential component of behaviourally relevant computations in neurons.
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We are grateful to B. Clark, P. Latham, M. London, D. Ringach, A. Roth, C. Schmidt-Hieber and C. Wilms for discussions and comments on the manuscript. This work was supported by the following: a Long-Term Fellowship and a Career Development Award from the Human Frontier Science Program and a Klingenstein Fellowship (S.L.S.); a Helen Lyng White Fellowship (I.T.S.); a Wellcome Trust and Royal Society Fellowship and MRC Programme Leader Track (T.B.); and by grants from the Wellcome Trust, ERC and Gatsby Charitable Foundation (M.H.).
Extended data figures
Background input was continuously active, and signal synapses were activated at 8 Hz for 200 ms (100 ms after the start of the trace). The traces show the local voltage at the indicated dendrites, together with the somatic voltage. During the period of high synaptic input local dendritic spikes are elicited in multiple regions of the dendritic tree, and eventually lead to a somatic action potential the backpropagates globally. Note how all of the global spikes are preceded by at least one dendritic spike in a region of the dendritic tree.
Note that the first two global spikes are immediately preceded by local spikes in this dendrite, and that while the last dendritic spike does not directly trigger a somatic action potential it leads to a significant charge build up in the soma that facilitates the subsequent somatic firing.
Note that dendrite 1 fires bursts of spikes at frequencies >50 Hz.