Central control of dendritic spikes shapes the responses of Purkinje-like cells through spike timing-dependent synaptic plasticity.
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.
Sawtell
Nathaniel B
NB
Neurological Sciences Institute, Oregon Health and Sciences University, Beaverton, Oregon 97006, USA. sawtelln@ohsu.edu
Williams
Alan
A
Bell
Curtis C
CC
D000200:Action Potentials / Q000502:physiology*; D000818:Animals; D001640:Bicuculline / Q000031:analogs & derivatives / Q000494:pharmacology; D003712:Dendrites / Q000502:physiology*; D004553:Electric Conductivity; D004555:Electric Fish; D004557:Electric Organ / Q000166:cytology*; D004558:Electric Stimulation / Q000379:methods; D005071:Evoked Potentials / Q000187:drug effects / Q000502:physiology / Q000528:radiation effects; D018756:GABA Antagonists / Q000494:pharmacology; D009433:Neural Inhibition / Q000187:drug effects / Q000502:physiology / Q000528:radiation effects; D016571:Neural Networks, Computer; D011689:Purkinje Cells / Q000166:cytology* / Q000502:physiology*; D011930:Reaction Time / Q000502:physiology; D012867:Skin / Q000294:innervation; D013569:Synapses / Q000502:physiology*; D009435:Synaptic Transmission / Q000187:drug effects / Q000502:physiology / Q000528:radiation effects
D018756:GABA Antagonists; C017069:bicuculline methiodide; D001640:Bicuculline