The complex dynamics of the membrane potential endows neurons with a wide behavioral repertoire. Even the least complex feature, the steady state membrane potential, can attain two distinct values, which is indicative of bistable dynamics. For this bistability to be of functional significance, a control mechanism that transforms the cell's membrane potential from one state to the other is required. Here we show that a bistable neuron, a Purkinje cell (PC), behaves like a toggle switch, where a single synaptic input is the lever that shifts between the two states. We demonstrate that PC bistability, which is typically attributed to in-vitro conditions, is retained in anaesthetized guinea pigs and that the same climbing fibre input switches the cells between the two states in both directions. We propose a general dynamic mechanism to explain this toggling effect, and discuss its possible computational role.

Simple cells in layer 4 of the primary visual cortex are the first neurons in the visual pathway showing orientation and direction selective responses. The precise role of intracortical excitatory and inhibitory connections in generating these properties is still unclear. Intracortical inhibitory processes have been shown to be crucial to the generation of direction selective responses. In vivo, excitatory and inhibitory layer 4 cells differ in their receptive field properties: excitatory (regular spiking) neurons are orientation- and direction-selective whereas inhibitory (fast spiking) neurons are orientation, but poorly direction tuned. This difference in direction tuning could be due to differences in intracortical inhibitory synaptic input patterns. To address this question we have optically recorded orientation and direction maps from ferret primary visual cortex (n=11, age: postnatal days 37 - 41). Subsequently the imaged brain region was removed and tangential slices (400 mm thickness) prepared. Whole cell patch clamp recordings from individual layer 4 neurons were done and synaptic inputs were scanned by local photolysis of Nmoc-caged glutamate (1 mM). Postsynaptic cells were filled with biocytin and histological sections were aligned with the synaptic input maps and the optical images obtained in vivo to determine the spatial distribution of presynaptic inputs. We recorded from n = 12 spiny (excitatory) and n = 10 aspiny (inhibitory) stellate cells. The majority (68 %) of excitatory inputs to both spiny (excitatory) and aspiny (inhibitory) stellate cells originated from cortical regions preferring the same orientation and direction as the postsynaptic cell. However, the inhibitory input patterns were significantly different for the two cell populations: excitatory layer 4 cells received two populations of inhibitory inputs, about 50 % originated in iso-direction domains whereas the remaining inputs originated in cortical regions preferring the opposite direction of stimulus motion. Inhibitory layer 4 neurons did not receive inhibitory synaptic inputs tuned to the opposite direction. This indicates that specific inhibitory connections originating in regions tuned to the opposite direction are important for direction tuning of cortical neurons and that differences in response properties in different populations of cortical neurons might be explained by their different intracortical connectivity patterns.