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Gating multiple signals through detailed balance of excitation and inhibition in spiking networks.

Vogels TP, Abbott LF - Nat. Neurosci. (2009)

Bottom Line: We illustrate gating through detailed balance in large networks of integrate-and-fire neurons.We show successful gating of multiple signals and study failure modes that produce effects reminiscent of clinically observed pathologies.Provided that the individual signals are detectable, detailed balance has a large capacity for gating multiple signals.

View Article: PubMed Central - PubMed

Affiliation: Center for Neurobiology and Behavior, Department of Physiology and Cellular Biophysics, Columbia University College of Physicians and Surgeons, New York, New York, USA.

ABSTRACT
Recent theoretical work has provided a basic understanding of signal propagation in networks of spiking neurons, but mechanisms for gating and controlling these signals have not been investigated previously. Here we introduce an idea for the gating of multiple signals in cortical networks that combines principles of signal propagation with aspects of balanced networks. Specifically, we studied networks in which incoming excitatory signals are normally cancelled by locally evoked inhibition, leaving the targeted layer unresponsive. Transmission can be gated 'on' by modulating excitatory and inhibitory gains to upset this detailed balance. We illustrate gating through detailed balance in large networks of integrate-and-fire neurons. We show successful gating of multiple signals and study failure modes that produce effects reminiscent of clinically observed pathologies. Provided that the individual signals are detectable, detailed balance has a large capacity for gating multiple signals.

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Response Analysisa) Firing rates of the excitatory receiver neurons as a function of different constant sender firing rates, in the balanced (solid trace) and unbalanced (dashed trace) states. b) Ratio of receiver to sender excitatory firing-rate oscillation amplitudes at different oscillation frequencies, in the balanced (solid trace) and unbalanced (dashed trace) states. c,d) Response to a random time filtered signal in the unbalanced (c) and balanced (d) states. Red trace: average firing rate of the excitatory receiver neurons. Black histogram: rates of the sender neurons. Deviations from the signal in c) and from the average background rate in d) are colored grey. e) Schematic of an input step. Step size (*) and step duration (**) are varied independently. f) Average responses of the excitatory receiver neurons in the balanced state to instantaneous steps of different sizes. g) Peak amplitude of the responses in these neurons to steps of different sizes (legend) and durations (horizontal axis).
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Figure 3: Response Analysisa) Firing rates of the excitatory receiver neurons as a function of different constant sender firing rates, in the balanced (solid trace) and unbalanced (dashed trace) states. b) Ratio of receiver to sender excitatory firing-rate oscillation amplitudes at different oscillation frequencies, in the balanced (solid trace) and unbalanced (dashed trace) states. c,d) Response to a random time filtered signal in the unbalanced (c) and balanced (d) states. Red trace: average firing rate of the excitatory receiver neurons. Black histogram: rates of the sender neurons. Deviations from the signal in c) and from the average background rate in d) are colored grey. e) Schematic of an input step. Step size (*) and step duration (**) are varied independently. f) Average responses of the excitatory receiver neurons in the balanced state to instantaneous steps of different sizes. g) Peak amplitude of the responses in these neurons to steps of different sizes (legend) and durations (horizontal axis).

Mentions: To further quantify the gating mechanism, we studied responses to different types of input (Fig. 3a & b). The firing rates of excitatory receiver neurons are relatively unaffected by constant input rates in the balanced gated-off state (solid trace in Fig. 3a) but rise sharply as a function of input rate when the pathway is gated on (dashed trace in Fig. 3a). The rise begins to saturate at high rates due to the residual inhibition produced locally, even at low gain. Gating is also evident in the amplitudes of firing-rate fluctuations for excitatory neurons in the receiver region when the input signal is oscillatory (Fig. 3b). In addition, gating occurs when filtered white noise (with a 50 ms time constant12) is used as the input signal (Fig. 3c, d). In the gated-on state, this complex, irregular signal is transmitted with similarity values12,14 (defined in the methods) of ~90%, sufficient to propagate the signal across several layers14. In the balanced, gated-off state (Fig. 3d), the output of the excitatory receiver group is greatly decreased in amplitude, and the similarity between input and output is reduced to ~25%.


Gating multiple signals through detailed balance of excitation and inhibition in spiking networks.

Vogels TP, Abbott LF - Nat. Neurosci. (2009)

Response Analysisa) Firing rates of the excitatory receiver neurons as a function of different constant sender firing rates, in the balanced (solid trace) and unbalanced (dashed trace) states. b) Ratio of receiver to sender excitatory firing-rate oscillation amplitudes at different oscillation frequencies, in the balanced (solid trace) and unbalanced (dashed trace) states. c,d) Response to a random time filtered signal in the unbalanced (c) and balanced (d) states. Red trace: average firing rate of the excitatory receiver neurons. Black histogram: rates of the sender neurons. Deviations from the signal in c) and from the average background rate in d) are colored grey. e) Schematic of an input step. Step size (*) and step duration (**) are varied independently. f) Average responses of the excitatory receiver neurons in the balanced state to instantaneous steps of different sizes. g) Peak amplitude of the responses in these neurons to steps of different sizes (legend) and durations (horizontal axis).
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Figure 3: Response Analysisa) Firing rates of the excitatory receiver neurons as a function of different constant sender firing rates, in the balanced (solid trace) and unbalanced (dashed trace) states. b) Ratio of receiver to sender excitatory firing-rate oscillation amplitudes at different oscillation frequencies, in the balanced (solid trace) and unbalanced (dashed trace) states. c,d) Response to a random time filtered signal in the unbalanced (c) and balanced (d) states. Red trace: average firing rate of the excitatory receiver neurons. Black histogram: rates of the sender neurons. Deviations from the signal in c) and from the average background rate in d) are colored grey. e) Schematic of an input step. Step size (*) and step duration (**) are varied independently. f) Average responses of the excitatory receiver neurons in the balanced state to instantaneous steps of different sizes. g) Peak amplitude of the responses in these neurons to steps of different sizes (legend) and durations (horizontal axis).
Mentions: To further quantify the gating mechanism, we studied responses to different types of input (Fig. 3a & b). The firing rates of excitatory receiver neurons are relatively unaffected by constant input rates in the balanced gated-off state (solid trace in Fig. 3a) but rise sharply as a function of input rate when the pathway is gated on (dashed trace in Fig. 3a). The rise begins to saturate at high rates due to the residual inhibition produced locally, even at low gain. Gating is also evident in the amplitudes of firing-rate fluctuations for excitatory neurons in the receiver region when the input signal is oscillatory (Fig. 3b). In addition, gating occurs when filtered white noise (with a 50 ms time constant12) is used as the input signal (Fig. 3c, d). In the gated-on state, this complex, irregular signal is transmitted with similarity values12,14 (defined in the methods) of ~90%, sufficient to propagate the signal across several layers14. In the balanced, gated-off state (Fig. 3d), the output of the excitatory receiver group is greatly decreased in amplitude, and the similarity between input and output is reduced to ~25%.

Bottom Line: We illustrate gating through detailed balance in large networks of integrate-and-fire neurons.We show successful gating of multiple signals and study failure modes that produce effects reminiscent of clinically observed pathologies.Provided that the individual signals are detectable, detailed balance has a large capacity for gating multiple signals.

View Article: PubMed Central - PubMed

Affiliation: Center for Neurobiology and Behavior, Department of Physiology and Cellular Biophysics, Columbia University College of Physicians and Surgeons, New York, New York, USA.

ABSTRACT
Recent theoretical work has provided a basic understanding of signal propagation in networks of spiking neurons, but mechanisms for gating and controlling these signals have not been investigated previously. Here we introduce an idea for the gating of multiple signals in cortical networks that combines principles of signal propagation with aspects of balanced networks. Specifically, we studied networks in which incoming excitatory signals are normally cancelled by locally evoked inhibition, leaving the targeted layer unresponsive. Transmission can be gated 'on' by modulating excitatory and inhibitory gains to upset this detailed balance. We illustrate gating through detailed balance in large networks of integrate-and-fire neurons. We show successful gating of multiple signals and study failure modes that produce effects reminiscent of clinically observed pathologies. Provided that the individual signals are detectable, detailed balance has a large capacity for gating multiple signals.

Show MeSH
Related in: MedlinePlus