Signal Propagation Along Unidimensional Neuronal Networks

Abstract

Feinerman, Ofer, Menahem Segal, and Elisha Moses. Signal propagation along unidimensional neuronal networks. J Neurophysiol 94: [3406][3407][3408][3409][3410][3411][3412][3413][3414][3415][3416] 2005. First published July 27, 2005; doi:10.1152/jn.00264.2005. Dissociated neurons were cultured on lines of various lengths covered with adhesive material to obtain an experimental model system of linear signal transmission. The neuronal connectivity in the linear culture is characterized, and it is demonstrated that local spiking activity is relayed by synaptic transmission along the line of neurons to develop into a large-scale population burst. Formally, this can be treated as a onedimensional information channel. Directional propagation of both spontaneous and stimulated bursts along the line, imaged with the calcium indicator Fluo-4, revealed the existence of two different propagation velocities. Initially, a small number of neighboring neurons fire, leading to a slow, small and presumably asynchronous wave of activity. The signal then spontaneously develops to encompass much larger and further populations, and is characterized by fast propagation of high-amplitude activity, which is presumed to be synchronous. These results are well described by an existing theoretical framework for propagation based on an integrate-and-fire model.The advance of activity through a neural network reveals much about its underlying properties. In particular, the velocity in which a signal propagates may differentiate synchronous from asynchronous activity and can identify the limiting factors in transmission, whether they are synaptic or axonal. The dependency of velocities on the strength of the ␣-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) synapses has been experimentally demonstrated in bursts that propagate in slices (Golomb and Amitai 1997).In this report such questions are addressed using a novel experimental system in which dissociated hippocampal neurons are grown along one-dimensional (1-D) patterned lines. These networks (Chang et al. 2001;Segev et al. 2002) provide a bridge that can link the realistic experimental system to numerous theoretical modeling approaches, which often deal effectively with one dimension (Abeles 1991;Diesmann et al. 1999;Golomb and Amitai 1997;Litvak et al. 2003;Osan and Ermentrout 2002;Siegal and Read 2001). Viewed as simplified models of cortical structure, such theoretical networks were used to address questions concerning the possible cortical coding schemes (Abeles 1991;Diesmann et al. 1999;Litvak et al. 2003).The major advantage of using one-dimensional cultures to study propagation is that a signal has only a limited pathway. Two-dimensional (2-D) networks and slices exhibit similar activity, but may have a large number of possible paths connecting any two given points ( The first goal of the study reported herein is to characterize the culture and to demonstrate that it is indeed layered and directed along one dimension. This is done by applying pharmacological treatments an...

Local axon collaterals of area CA1 support spread of epileptiform discharges within CA1, but propagation is unidirectional

“…Nondecrementing (and sometimes broadening) population events spread through area CA3 at 0.15 m/s CA3 (Miles et al, 1988). This was similar to the rates reported for neocortex, 0.13-0.19 m/s neocortex (Golomb and Amitai, 1997), and disinhibited hippocampal neurons cultured on a line, 0.1 m/s (Feinerman et al, 2005). Lower rates were reported in other studies of neocortex, 0.074 m/s (Pinto et al, 2005), and in subiculum, 0.04 m/s subiculum (Harris and Stewart, 2001a).…”

Spatiotemporal order out of noise

“…This system can present inhibitory, excitable, and oscillatory behavior, depending on the synaptic strength between neurons, which is chemically controlled. Signal propagation and information transport have been studied by Feinerman et al ͑2005͒. Neural connectivity and the presence of a percolation transition in two-dimensional neural cultures have been examined by Breskin et al ͑2006͒.…”

BDNF and NT-3 Increase Velocity of Activity Front Propagation in Unidimensional Hippocampal Cultures

“…One-dimensional neural cultures have emerged in the last years as versatile culturing platforms to investigate the relation between neuronal connectivity, signal propagation, and information coding (Feinerman et al 2005;Golomb and Ermentrout 1999;Jacobi and Moses 2007;Osan and Ermentrout 2002). The key feature of 1D cultures is that the velocity of activity fronts depends on neural connectivity and specifically on both the synaptic strength and the number of connections.…”

“…The key feature of 1D cultures is that the velocity of activity fronts depends on neural connectivity and specifically on both the synaptic strength and the number of connections. Therefore the measurement of the propagation velocity under different experimental conditions provides valuable information of the interplay between neural connectivity and neural activity (Feinerman et al 2005;Golomb and Ermentrout 1999;Jacobi and Moses 2007;Osan and Ermentrout 2002).…”

“…The key feature of 1D cultures is that the velocity of activity fronts depends on neural connectivity and specifically on both the synaptic strength and the number of connections. Therefore the measurement of the propagation velocity under different experimental conditions provides valuable information of the interplay between neural connectivity and neural activity (Feinerman et al 2005;Golomb and Ermentrout 1999;Jacobi and Moses 2007;Osan and Ermentrout 2002).In this work, we combine our previous results regarding the effect of neurotrophins on bursting activity with velocity measurements of propagating fronts in 1D circuits. The results are studied within the framework of the model of Feinerman et al (2005), Golomb and Ermentrout (1999), Jacobi and Moses (2007), and Osan and Ermentrout (2002) that takes into account the role of synaptic delays in burst propagation, which is extended to include the probability of neural connection.…”