Activity-dependent regulation of receptive field properties of cat area 17 by supervised Hebbian learning

Most algorithms currently used to model synaptic plasticity in self-organizing cortical networks suppose that the change in synaptic efficacy is governed by the same structuring factor, i.e., the temporal correlation of activity between pre- and postsynaptic neurons. Functional predictions generated by such algorithms have been tested electrophysiologically in the visual cortex of anesthetized and paralyzed cats. Supervised learning procedures were applied at the cellular level to change receptive field (RF) properties during the time of recording of an individual functionally identified cell. The protocols were devised as cellular analogs of the plasticity of RF properties, which is normally expressed during a critical period of postnatal development. We summarize here evidence demonstrating that changes in covariance between afferent input and postsynaptic response imposed during extracellular and intracellular conditioning can acutely induce selective long-lasting up- and down-regulations of visual responses. The functional properties that could be modified in 40% of cells submitted to differential pairing protocols include ocular dominance, orientation selectivity and orientation preference, interocular orientation disparity, and the relative dominance of ON and OFF responses. Since changes in RF properties can be induced in the adult as well, our findings also suggest that similar activity-dependent processes may occur during development and during active phases of learning under the supervision of behavioral attention or contextual signals. Such potential for plasticity in primary visual cortical neurons suggests the existence of a hidden connectivity expressing a wider functional competence than the one revealed at the spiking level. In particular, in the spatial domain the sensory synaptic integration field is larger than the classical discharge field. It can be shaped by supervised learning and its subthreshold extent can be unmasked by the pharmacological blockade of intracortical inhibition.