Rapid plasticity of visually evoked responses in rat monocular visual cortex

Abstract

Sensory cortical circuits are shaped by experience during sensitive periods in development. In the primary visual cortex (V1) altered visual experience results in changes in visual responsiveness of cortical neurons. The experience-dependent refinement of the circuit in V1 is thought to rely on competitive interactions between feedforward circuits driven by the two eyes. However, recent data have provided evidence for an additional role of cortico-cortical circuits in this process. Indeed, experience-dependent changes in intracortical circuits can be induced rapidly and may result in rapid-onset functional changes. Unilateral occlusion of vision rapidly alters visual responsiveness, synaptic strength and connectivity of local circuits in the binocular region of V1 (V1b), where the inputs from the two eyes converge. In the monocular region of rodent V1 (V1m), where feedforward inputs from the ipsilateral eye are virtually absent, visual deprivation induces rapid plasticity in local circuits; however, functional changes seem to occur only after long periods of deprivation. In V1m there is currently no evidence for functional changes occurring within a time window compatible with that of local circuit plasticity. Here, we probed the visual responsiveness of neurons in rat V1m and assessed the effect of one day unilateral eye lid suture on single neuron visual responses. We report a novel form of plasticity within V1m that occurs on a timescale consistent with the earliest known changes in synaptic strength. Our data provide new insights into how sensory experience can rapidly modulate neuronal responses, even in the absence of direct competition between feedforward thalamocortical inputs.

Fig 1. Whole-cell recordings of V1 neurons.

(A) Recovered L4 V1m pyramidal neuron with representative morphology. The electrode track is visible next to the recovered cell. (B) Representative current injection/firing relationship of a V1 neuron in response to 1s sequential current injections (in pA: -250, 0, 250, 500). (C) Five representative, overlapped responses of a V1 neuron to stimulation of the contralateral eye. Arrow: stimulus onset.

Fig 2. Delayed onset ipsilateral responses in V1m.

(A) 10 overlapped membrane potential responses (black) to contralateral (top) and ipsilateral (bottom) eye stimuli recorded from a V1m neuron. The mean of the absolute value of the derivative of the action potentials (red) and the response latencies (purple) are superimposed. Arrow: stimulus onset. (B) Same as A, except traces are from a V1b neuron. (C) Response latencies of flash-evoked responses recorded in V1m and V1b. *p < 0.05, ANOVA on Ranks and post hoc pairwise multiple comparisons by Dunn’s Method. (D) Injection site of cholera toxin B in V1m. (E) Retrograde labeling specifically in the monocular region of the LGN confirms that the site of injection shown in D is in V1m. (F) Retrogradely labeled neurons in V1b of the injected hemisphere. The site of injection has been blanked to selectively show V1b labeled neurons. (G) Retrogradely labeled neurons in V1b of the hemisphere opposite to the injection site. For all images, insets show an enlarged portion of region of interest. Magenta: cholera toxin B; cyan: Hoechst. The boundaries between V1m and V1b were reconstructed based on the rat brain atlas [23].

Fig 3. Rapid interocular bias plasticity in V1m.

(A) Ten overlapped responses to contralateral (top) and ipsilateral (bottom) eye stimuli from a representative Control V1m neuron (recorded from V1m of the hemisphere contralateral to the open eye). (B) Ten overlapped responses to stimulation of the contralateral (top) and ipsilateral (bottom) eye of the Deprived hemisphere (recorded from V1m of the hemisphere contralateral to the closed eye). Note the large ipsilateral response. For (A) and (B), arrow: stimulus onset. Top bar: post-response bin. (C) auROC-IBI for V1m neurons recorded in the Control and Deprived hemispheres. *p = 0.037, Wilcoxon rank-sum test. (D) Responses to contralateral eye stimuli for V1m neurons from Control and Deprived hemispheres. p = 0.86, Wilcoxon rank-sum test. (E) Responses to ipsilateral eye stimuli for V1m neurons recorded in Control and Deprived hemispheres. *p = 0.041, Wilcoxon rank-sum test.