Intracortical mechanism of stimulus-timing-dependent plasticity in visual cortical orientation tuning

Abstract

Visual stimuli are known to induce various changes in the receptive field properties of adult cortical neurons, but the underlying mechanisms are not well understood. Repetitive pairing of stimuli at two orientations can induce a shift in cortical orientation tuning, with the direction and magnitude of the shift depending on the temporal order and interval between the pair. Although the temporal specificity of the effect on the order of tens of milliseconds strongly suggests spike-timing-dependent synaptic plasticity (STDP) as the underlying mechanism, it remains unclear whether the modification occurs within the cortex or at earlier stages of the visual pathway. In the present study, we examined the involvement of an intracortical mechanism in this functional modification. First, we measured interocular transfer of the shift induced by monocular conditioning. We found complete transfer of the effect at both the physiological and psychophysical levels, indicating that the modification occurs largely in the cortex. Second, we analyzed the spike timing of cortical neurons during conditioning and found it commensurate with the requirement of STDP. Finally, we compared the measured shift in orientation tuning with the prediction of a model circuit that exhibits STDP at intracortical connections. This model can account for not only the temporal specificity of the effect but also the dependence of the shift on both orientations in the conditioning pair. These results indicate that modification of intracortical connections is a key mechanism in the stimulustiming-dependent plasticity in orientation tuning.V isual stimuli are known to induce various changes in adult cortical circuits. For example, in contrast adaptation, a few seconds of visual stimulation can cause a marked reduction in the response amplitude of cortical neurons (1) along with changes in their spatial frequency tuning (2), orientation tuning (3, 4), and direction selectivity (5). These effects may be caused by a reduction in neuronal excitability (6, 7) or by short-term synaptic depression (8). Concurrent visual stimulation and iontophoretic activation of cortical neurons can induce changes in their orientation selectivity and ocular dominance (9-11). The dependence of these effects on the coincidence between visual and iontophoretic stimulation is consistent with Hebb's rule for synaptic modification. Similarly, synchronous stimulation of the receptive field (RF) center and part of the surround can induce an RF expansion toward the costimulated surround (12), which is also likely mediated by Hebbian synaptic modification. Together, these studies indicate a high degree of plasticity of adult cortical circuits. In this study, we focused on a form of cortical modification that is likely mediated by spike-timing-dependent synaptic plasticity (STDP) of synaptic connections.In STDP, the direction and magnitude of synaptic modification depend on the order and interval between the pre-and postsynaptic spikes: Presynaptic spiking within tens of milliseconds be...

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