Cellular analogs of visual cortical epigenesis. I. Plasticity of orientation selectivity

Abstract

A differential pairing procedure was applied in vivo to individual neurons in the primary visual cortex of anesthetized paralyzed cats, in order to produce changes in their relative orientation preference. While we recorded from a single cell, its visual response to a light bar was driven iontophoretically to a "high" level when stimulating with an initially nonpreferred orientation (S+), and alternately reduced to a "low" level when stimulating with the preferred orientation (S). This associative procedure was devised to test the possible role of neuronal coactivity in controlling the plasticity of orientation selectivity. Among 87 cells tested, 35 (40%) showed significant long-lasting changes, either in the relative orientation preference for the two "paired" stimuli S+ and S-, in the global orientation tuning profile, or in both. Measurements of relative orientation preference demonstrated significant effects in 27 cells (31%), all in favor of the positively reinforced orientation (S+). Modifications of orientation selectivity (studied over the entire orientation spectrum in 45 of the conditioned cells) usually consisted (21 out of 25 modified cells) of a competitive reorganization of the orientation tuning curve: the preferred orientation shifted toward S+, and a loss of relative visual responsiveness was observed for orientations close to the negatively reinforced orientation (S-). The largest changes were found in deprived kittens at the peak of the critical period, although the probability of inducing a significant change studied during the first year of postnatal life was independent of age. These functional modifications demonstrated at the cellular level are analogous to those induced by a global manipulation of the visual environment, when only a restricted spectrum of orientations is experienced during the critical period. Our results support the hypothesis that covariance levels between pre- and postsynaptic activity determine the sign and the amplitude of the modification of efficacy of cortical synapses.

A synaptic basis for memory storage in the cerebral cortex

“…It is possible to manipulate receptive field properties in visual cortex by pairing visual stimulation with various imposed patterns of postsynaptic activity (53,54). The modifications of receptive fields observed in these studies conform well with theoretical predictions.…”

The brain decade in debate: VI. Sensory and motor maps: dynamics and plasticity

“…Aniruddha Das: Eliane, Yves Fregnac and colleagues (46,47) have shown a whole range of similar effects in V1 -where you get a change in the orientation tuning by pairing a particular orientation with stimulation (they used extracellular electrical stimulation, for example), again, you get a shift in the peak orientation tuning but not a bodily shift in orientation tuning, similar to Norman Weinberger's results.…”

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

“…For example, visual adaptation to a nonoptimal orientation can induce a shift in orientation tuning away from the adapted orientation (3,55), which may be mediated by short-term plasticity of intracortical connections (56). Pairing of visual and iontophoretic activation of cortical neurons can also induce a shift in orientation tuning, which is likely mediated by intracortical synaptic modifications that depend on coincident pre-and postsynaptic activity (9)(10)(11). In the present study, dependence of the effect on the order and interval between the conditioning pair strongly indicates the involvement of STDP of intracortical connections, which has been shown to be a robust phenomenon in visual cortical slices (22,23).…”

“…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)(10)(11). The dependence of these effects on the coincidence between visual and iontophoretic stimulation is consistent with Hebb's rule for synaptic modification.…”