Regulation of Spatial Selectivity by Crossover Inhibition
authors: Jon Cafaro, Fred Rieke
doi: 10.1523/JNEUROSCI.4964-12.2013
CITATION
Cafaro, J., & Rieke, F. (2013). Regulation of Spatial Selectivity by Crossover Inhibition. The Journal of Neuroscience, 33(15), 6310–6320. https://doi.org/10.1523/JNEUROSCI.4964-12.2013
ABSTRACT
Signals throughout the nervous system diverge into parallel excitatory and inhibitory pathways that later converge on downstream neurons to control their spike output. Converging excitatory and inhibitory synaptic inputs can exhibit a variety of temporal relationships. A common motif is feedforward inhibition, in which an increase (decrease) in excitatory input precedes a corresponding increase (decrease) in inhibitory input. The delay of inhibitory input relative to excitatory input originates from an extra synapse in the circuit shaping inhibitory input. Another common motif is push-pull or “crossover” inhibition, in which increases (decreases) in excitatory input occur together with decreases (increases) in inhibitory input. Primate On midget ganglion cells receive primarily feedforward inhibition and On parasol cells receive primarily crossover inhibition; this difference provides an opportunity to study how each motif shapes the light responses of cell types that play a key role in visual perception. For full-field stimuli, feedforward inhibition abbreviated and attenuated responses of On midget cells, while crossover inhibition, though plentiful, had surprisingly little impact on the responses of On parasol cells. Spatially structured stimuli, however, could cause excitatory and inhibitory inputs to On parasol cells to increase together, adopting a temporal relation very much like that for feedforward inhibition. In this case, inhibitory inputs substantially abbreviated a cell’s spike output. Thus inhibitory input shapes the temporal stimulus selectivity of both midget and parasol ganglion cells, but its impact on responses of parasol cells depends strongly on the spatial structure of the light inputs.
fleeting notes
signals diverge into excitatory/inhibitory pathways. these converge later on.
feedforward inhibition
- an increase in excitatory input precedes a corresponding increase in inhibitory input
- and vice versa
push-pull inhibition (crossover inhibition) - increase in excitatory input occurs together with decrease in inhibitory input
feedforward inhibition - excitation and inhibition are positively correlated, just temporally delayed.
- the delay is an extra synapse in the circuit
feedforward inhibition limits neural responses to a brief time window
crossover inhibition can help define receptive field properties
delayed inhibition produced by feedforward circuit happens on super fast timescales (because it can be only a single synapse producing the effects)
crossover inhibition does not make predictions about timing of inputs
- can see near simultaneous changes in e/i inputs
midget ganglion responses without inhibitory input are stronger
parasol ganglion cells had similar spike responses with and without inhibition
therefore inhibition is really important for midget ganglion cell responses but dispensable for parasol responses
there are still nonlinearities in cell responses
spatially structured stimuli can cause positively correlated changes in excitatory and inhibitory synaptic inputs
inhibitory inputs may regulate a cells spike output
inhibitory mechanisms vary substantially. The minor different in timing of these inhibitory inputs changes the cell’s encoding of light inputs.
feedforward inhibition
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vision (this paper) among others
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primary auditory cortex
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pyramidal cells in hippocampus
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barrel cortex
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etc
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creates a temporally restricted window for excitatory input to drive spike output. precise correspondence between spike timing and synchronized input.
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feedforward inhibition likely creates transient responses. also changes how cells respond and integrate across space.
crossover inhibition
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proposed to shape receptive fields.
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extends range that ganglion cells encode light inputs
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can play a gatekeeper role — excitatory input can modulate spike output during times when inhibitory input is small