Top-down inputs enhance orientation selectivity in neurons of the primary visual cortex during perceptual learning.

Perceptual learning has been used to probe the mechanisms of cortical plasticity in the adult brain. Feedback projections are ubiquitous in the cortex, but little is known about their role in cortical plasticity. Here we explore the hypothesis that learning visual orientation discrimination involves learning-dependent plasticity of top-down feedback inputs from higher cortical areas, serving a different function from plasticity due to changes in recurrent connections within a cortical area. In a Hodgkin-Huxley-based spiking neural network model of visual cortex, we show that modulation of feedback inputs to V1 from higher cortical areas results in shunting inhibition in V1 neurons, which changes the response properties of V1 neurons. The orientation selectivity of V1 neurons is enhanced without changing orientation preference, preserving the topographic organizations in V1. These results provide new insights to the mechanisms of plasticity in the adult brain, reconciling apparently inconsistent experiments and providing a new hypothesis for a functional role of the feedback connections

Feedback stabilizes propagation of synchronous spiking in cortical neural networks

Precisely timed action potentials related to stimuli and behavior have been observed in the cerebral cortex. However, information carried by the precise spike timing has to propagate through many cortical areas, and noise could disrupt millisecond precision during the transmission. Previous studies have demonstrated that only strong stimuli that evoke a large number of spikes with small dispersion of spike times can propagate through multilayer networks without degrading the temporal precision. Here we show that feedback projections can increase the number of spikes in spike volleys without degrading their temporal precision. Feedback also increased the range of spike volleys that can propagate through multilayer networks. Our work suggests that feedback projections could be responsible for the reliable propagation of information encoded in spike times through cortex, and thus could serve as an attentional mechanism to regulate the flow of information in the cortex. Feedback projections may also participate in generating spike synchronization that is engaged in cognitive behaviors by the same mechanisms described here for spike propagation

Effect of feedbacks on population response in V1.

<p><b>A.</b> Population response in V1 to a stimulus before training, with (black) and without (grey) recurrent connections among V1 neurons. <b>B.</b> Input-output function in V1 neurons, with (black) and without (grey) recurrent connections among V1 neurons. <b>C.</b> Population response in V1 to the trained stimulus (preferred stimulus for neuron <b><i>A</i></b>) before and after training. <b>D.</b> Responses of neurons <b><i>A</i></b> and <b><i>B</i></b> to the trained stimulus (preferred for neuron <b><i>A</i></b>) changed due to feedback. Black line indicates input-output relation in V1. Blue arrows indicate the strength of feedback inputs. Black and grey filled circles represent neural response of neurons <b><i>A</i></b> and <b><i>B</i></b> to the trained stimulus before and after training. <b>E.</b> Population response in V1 to a novel stimulus (preferred for neuron <b><i>B</i></b>), before and after training with the stimulus preferred for neuron <b><i>A</i></b>. <b>F.</b> Responses of neurons <b><i>A</i></b> and <b><i>B</i></b> to the novel stimulus (preferred for neuron <b><i>B</i></b>) changed due to feedback. Black line indicates input-output relation in V1. Blue arrows indicate feedback inputs. Black and grey filled circles represent neural responses to stimulus preferred for neuron <b><i>B</i></b> before and after training.</p

Stimulus specificity of tuning curve changes.

<p><b>A.</b> Training the model with stimulus <b><i>A</i></b> strengthened the feedforward and feedback connections between stimulus-specific populations of V1 and V2 neurons. <b>B.</b> A test stimulus <b><i>B</i></b> (green) activated population of neurons in V1 and V2 that included some neurons with the modified synapses. The red circle shows where the trained stimulus <b><i>A</i></b> was presented to the model. <b>C.</b> Another test stimulus <b><i>C</i></b> (purple) activated populations of V1 and V2 neurons that did not include neurons with modified synapses. <b>D.</b> Before training, the strength of the feedback inputs was equal for any applied stimulus (grey dashed line). After training, the strength of feedback inputs depended on the applied stimulus (black solid line). <b>E.</b> Stimulus specificity of changes to tuning curves. Peaks of tuning curves did not change, but amplitudes and widths of the tuning curves changed depending on the distance from the trained orientation.</p