Abstract

The calcium ion (Ca2+) is an important messenger for signal transduction, and the intracellular Ca2+ concentration ([Ca2+]i) changes in response to an excitation of the cell. To reveal the spatiotemporal properties of the propagation of an excitatory signal with action potentials in the primary visual cortical circuit, we conducted a Ca2+ imaging study on slices of the mouse visual cortex. Electrical stimulation of layer 4 evoked [Ca2+]i transients around the stimulus electrode. Subsequently, the high [Ca2+]i region mainly propagated perpendicular to the cortical layer (vertical propagation), with horizontal propagation being restricted. When the excitatory synaptic transmission was blocked, only weak and concentric [Ca2+]i transients were observed. When the action potential was blocked, the [Ca2+]i transients disappeared almost completely. These results suggested that the action potential contributed to the induction of the [Ca2+]i transients, and that excitatory synaptic connections were involved in the propagation of the high [Ca2+]i region in the primary visual cortical circuit. To elucidate the involvement of inhibitory synaptic connections in signal propagation in the primary visual cortex, the GABAA receptor inhibitor bicuculline was applied. In this case, the evoked signal propagated from layer 4 to the entire field of view, and the prolonged [Ca2+]i transients were observed compared with the control condition. Our results suggest that excitatory neurons are widely connected to each other over the entire primary visual cortex with recurrent synapses, and inhibitory neurons play a fundamental role in the organization of functional sub-networks by restricting the propagation of excitation signals.

Highlights

  • A fundamental part of neuroscience is the characterization of neuronal circuits

  • P,0.0001; one-sample t-test), and 4.964.9% and 10.6610.6% in the case of the 200 mA stimuli (n = 4 slices; p,0.001 and p,0.005, respectively; one-sample t-test; note: only one slice exhibited small responses in the case of 200 mA stimulation). These results indicated that action potentials involved in the induction of the [Ca2+]i transients

  • Physiological implications of the [Ca2+]i transients In this paper, we demonstrated the spatiotemporal properties of the [Ca2+]i dynamics evoked by electrical stimulation in primary visual cortical slice preparations by means of Ca2+ imaging

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Summary

Introduction

A fundamental part of neuroscience is the characterization of neuronal circuits. The calcium ion (Ca2+) is an important messenger for signal transduction, and the intracellular Ca2+ concentration ([Ca2+]i) has been shown to change in response to the excitation of the cell [1,2,3,4,5]. An analysis of [Ca2+]i dynamics may help to better characterize the behavior of neuronal circuits. Understanding the behavior of a neuronal circuit based on single-site neuronal recordings is difficult. To understand signal processing in neuronal networks better, the activity of a large population of neurons should be simultaneously measured. As a direct approach to reveal circuit dynamics, multielectrode recordings have been conducted [11,12,13]. A multielectrode array can record the spikes or local field potentials from an ensemble of neurons simultaneously. This approach is not optimal, because it has the disadvantage of sampling only a small population of neurons [1], [2]

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