Shunting Inhibition Does Not Have a Divisive Effect on Firing Rates

By Gary R. Holt, Christof Koch. 1997

Shunting inhibition, a conductance increase with a reversal potential close to the resting potential of the cell, has been shown to have a divisive effect on subthreshold excitatory postsynaptic potential amplitudes. It has therefore been assumed to have the same divisive effect on firing rates. We show that shunting inhibition actually has a subtractive effecton the firing rate in most circumstances. Averaged over several interspike intervals, the spiking mechanism effectively clamps the somatic membrane potential to a value significantly above the resting potential, so that the current through the shunting conductance is approximately independent of the firing rate. This leads to a subtractive rather than a divisive effect. In addition, at distal synapses, shunting inhibition will also have an approximately subtractive effect if the excitatory conductance is not small compared to the inhibitory conductance. Therefore regulating a cell's passive membrane conductancefor instance, via massive feedbackis not an adequate mechanism for normalizing or scaling its output.

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Citations in the corpus

Normalization as a canonical neural computation (2011, background): “It is less obvious to see how conductance controls the gain of firing rate responses, because spiking itself introduces large, albeit brief, conductance increase”
Attentional modulation of visual processing. (2004, background): “This action has a divisive effect on subthreshold excitatory postsynaptic potential amplitudes, and the model assumes that this reduction has a divisive effect on firing rate (however, see Holt & Koch 1997).”
Tonically active GABA A receptors: modulating gain and maintaining the tone. (2004, result): “When excitation was mediated by a constant conductance, increasing tonic inhibition performed an almost perfect subtraction on the input–output relationship [41] (Figure 3a,b), as predicted from theory [ 46 ] and observed previously for step current injections [5].”
Shunting inhibition modulates neuronal gain during synaptic excitation. (2003, background): “This produced a current through the inhibitory conductanceare consistent with the findings of Holt and Koch (1997), (A) Spiking in a cerebellar granule cell evoked by injection of a step of 1 nS tonic excitatory conductance (Gexc) for control and with 1 nS of tonic inhibition.”
Synaptic Basis of Cortical Persistent Activity: the Importance of NMDA Receptors to Working Memory (1999, background): “However, as it was recently pointed out by Holt and Koch (1997), the situation is different when the cell is in a repetitively firing state.”
Asynchronous GABA release generates long-lasting inhibition at a hippocampal interneuron–principal neuron synapse (2005, background): “, whereas slow 'tonic' inhibition may set the gain or offset of the input-output relations of postsynaptic target cell”
Non-topographical contrast enhancement in the olfactory bulb (2006, background): “While this chloride-mediated shunt inhibition may often be insufficiently hyperpolarizing to evoke clearly visible ipsps, it is highly effective at blocking spike initiation by multiplicatively decrementing the cumulative effect of excitatory sensory input (Figure 4Avi–vii;[61,65]; see also [66]).”
How Inhibition Shapes Cortical Activity (2011, unknown): “Furthermore neuronal models provide a theoretical framework for these observations (Holt and Koch, 1997).”
Alternative to hand-tuning conductance-based models: construction and analysis of databases of model neurons. (2003, background): “conductance can affect the gain of the fI curve—such a conductance could be a target for gain modulation (Chance et al. 2002; Holt and Koch 1997; Smith et al. 2002).”
A Canonical Neural Circuit for Cortical Nonlinear Operations (2008, background): “(For a similar discussion, see Carandini & Heeger, 1994; Reichardt et al., 1983; Chance et al., 2002; Holt & Koch, 1997.)”