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The Journal of Neuroscience, February 14, 2007, 27(7):1552-1565; doi:10.1523/JNEUROSCI.5302-06.2007

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Behavioral/Systems/Cognitive
Central Control of Dendritic Spikes Shapes the Responses of Purkinje-Like Cells through Spike Timing-Dependent Synaptic Plasticity

Nathaniel B. Sawtell, Alan Williams, and Curtis C. Bell

Neurological Sciences Institute, Oregon Health and Sciences University, Beaverton, Oregon 97006

Correspondence should be addressed to Nathaniel B. Sawtell, Neurological Sciences Institute, Oregon Health and Sciences University, Beaverton, OR 97006. Email: sawtelln{at}ohsu.edu

Cerebellum-like structures process peripheral sensory information in combination with parallel fiber inputs that convey information about sensory and motor contexts. Activity-dependent changes in the strength of parallel fiber synapses act as an adaptive filter, removing predictable features of the sensory input. In the electrosensory lobe (ELL) of mormyrid fish, a main cellular site for this adaptive processing is the Purkinje-like medium ganglion (MG) cell. MG cells exhibit two types of spikes: narrow axon spikes (N spikes) and broad dendritic spikes (B spikes). N spikes shape ELL output by inhibiting efferent cells, whereas B spikes drive plasticity at parallel fiber synapses. Despite their critical role in plasticity, little is known about the relative importance of various classes of MG cell inputs in driving B spikes or to what extent B spikes can be controlled independently of N spikes. Using in vivo intracellular recordings, measurements of synaptic conductance, and pharmacological blockade of inhibition, we provide evidence for corollary discharge-evoked inhibition that exerts potent control over the timing and probability of B spikes with little apparent effect on N spikes. The timing of this inhibition corresponds to the period during which repeated occurrence of B spikes causes depression of corollary discharge-evoked synaptic responses and a reduction in N spikes. B spikes occurring before or after the period of inhibition lead to increases in corollary discharge-evoked excitation. Thus, by controlling the timing of B spikes, central inhibition shapes the output of MG cells through spike timing-dependent synaptic plasticity. Our findings are consistent with a model of ELL function in which feedback guides adaptive processing by regulating B spikes.

Key words: inhibition; synaptic plasticity; spike timing; corollary discharge; electric fish; cerebellum

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Received Dec. 7, 2006; revised Jan. 8, 2007; accepted Jan. 9, 2007.

Correspondence should be addressed to Nathaniel B. Sawtell, Neurological Sciences Institute, Oregon Health and Sciences University, Beaverton, OR 97006. Email: sawtelln{at}ohsu.edu

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