In neocortical circuits, repetitively active neurons evoke unitary
postsynaptic potentials (PSPs) whose peak amplitudes either increase (facilitate)
or decrease (depress) progressively. To examine the basis for these different
synaptic responses, we made simultaneous recordings from three classes of
neurons in cortical layer 2/3. We induced repetitive action potentials in
pyramidal cells and recorded the evoked unitary excitatory (E)PSPs in two
classes of GABAergic neurons. We observed facilitation of EPSPs in bitufted
GABAergic interneurons, many of which expressed somatostatin immunoreactivity.
EPSPs recorded from multipolar interneurons, however, showed depression. Some
of these neurons were immunopositive for parvalbumin. Unitary inhibitory (I)PSPs
evoked by repetitive stimulation of a bitufted neuron also showed a less pronounced
but significant difference between the two target neurons. Facilitation and
depression involve presynaptic mechanisms, and because a single neuron can
express both behaviors simultaneously, we infer that local differences in
the molecular structure of presynaptic nerve terminals are induced by retrograde
signals from different classes of target neurons. Because bitufted and multipolar
neurons both formed reciprocal inhibitory connections with pyramidal cells,
the results imply that the balance of activation between two recurrent inhibitory
pathways in the neocortex depends on the frequency of action potentials in
pyramidal cells.
