Key Points
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In vitro, precise and reliable spike trains are obtained in response to fluctuating current waveforms injected at the soma. For aperiodic currents this is called stimulus locking; for periodic currents it is called phase locking.
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Across trials, stimulus-locked spike trains contain multiple distinct spike patterns that can be uncovered using analysis procedures based on clustering.
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In vivo, output spike trains reflect the interaction that occurs between stimulus-locked inputs and oscillatory inputs that are generated internally. As a result, precise and reliable spike trains can sometimes be obtained in response to time-varying stimulus waveforms (when the spikes are aligned to stimulus onset), or in response to cortical oscillations (when the spikes are aligned to the oscillation phase).
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Stimulus or phase-locked spike trains across multiple neurons can lead to synchronous spike volleys, which can propagate efficiently through dendritic action potentials that pass through the different layers of the cortex. Inhibitory interneurons can coordinate synchronous volleys in pyramidal cells.
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Dynamically modulated oscillations can support a flexible system for communicating through spike volleys in parallel with neural codes based on firing rates. Slow cortical oscillations set the excitability of neurons and gate the amplitude of the fast oscillations, whereas fast inhibitory oscillations can gate spike volleys or shift their time.
Abstract
A train of action potentials (a spike train) can carry information in both the average firing rate and the pattern of spikes in the train. But can such a spike-pattern code be supported by cortical circuits? Neurons in vitro produce a spike pattern in response to the injection of a fluctuating current. However, cortical neurons in vivo are modulated by local oscillatory neuronal activity and by top-down inputs. In a cortical circuit, precise spike patterns thus reflect the interaction between internally generated activity and sensory information encoded by input spike trains. We review the evidence for precise and reliable spike timing in the cortex and discuss its computational role.
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Acknowledgements
We thank P. J. Thomas, S. Schreiber, D. Spencer, H. -P. Wang, J. V. Toups and J. V. José for their contributions to the research presented in this Review. This work was supported by the Human Frontier Science Program (P.T.), US National Institutes of Health grant R01 MH068481 (T.J.S. & P.T.) and the Howard Hughes Medical Institute (T.J.S.).
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FURTHER INFORMATION
Glossary
- Spike time
-
The time of occurrence of an action potential, relative to stimulus onset or another event.
- Spike volleys
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A set of spikes emitted at approximately the same time (typically with a temporal spread of between 1 and 10 ms) by a pool of neurons.
- Feedforward information
-
In the context of stimulus–response circuitry, feedforward information is information that is processed in a single direction — from sensory input through perceptual analysis to motor output — without involving feedback information flowing backwards from 'higher' centres to 'lower' centres.
- Top-down information
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The flow of information from 'higher' to 'lower' centres, conveying knowledge derived from previous experience rather than from sensory stimulation.
- Spike-time histogram
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A tool for resolving the behaviour of the firing rate as a function of time, by averaging across multiple trials or multiple neurons. Mathematically, it is obtained by counting the number of spikes in each time bin and normalizing the count by the bin width, the number of trials and/or the number of neurons.
- Event
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A time-point relative to the stimulus onset during which a spike is found on a significant fraction of the trials.
- Neuromodulator
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An endogenous chemical substance that changes the intrinsic properties of a neuron and the dynamics and strength of neurotransmission. Neuromodulators can modify neuronal responses to synaptic inputs on potentially long timescales.
- Afterhyperpolarization
-
The membrane hyperpolarization that follows the occurrence of one or several action potentials.
- Eye-cup preparation
-
A preparation in which the retina is extracted intact so that the neural responses to activation of the photoreceptors by a visual stimulus can be recorded.
- Local field potential
-
(LFP). The total electrical current in the vicinity of the recording electrode, reflecting the sum of events in the dendrites of a local neuronal population. It is often obtained by low-pass filtering (that is, removal of signals lower than 600 Hz ) of the recorded electrical signal.
- Compartmental model
-
A computer model that breaks a neuron down into small electrical compartments and can simulate the propagation of electrical signals inside the neuron and across its membrane surface.
- Cortical pyramidal cell
-
A class of neuron in the cerebral cortex with a pyramid-shaped cell body. These neurons have dendrites that extend locally and can project their axonal processes both locally and distally across many layers and brain areas.
- Caged glutamate
-
An inactive derivative of glutamate that can be transformed into the active transmitter, usually by photolysis. This technique provides an efficient means for achieving a spatially restricted application of glutamate.
- Dendritic action potential
-
(dAP). An action potential that is first generated in the dendrites and which then propagates towards the soma, often but not always eliciting a somatic action potential after a brief delay.
- Relay cell
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A type of cell in the thalamus that sends its axon to the cortex. Relay cells in the lateral geniculate nucleus receive inputs from the retina and project to spiny stellate cells in layer 4 of the primary visual cortex.
- Spiny stellate cells
-
(SSCs). An excitatory cell type that is common in layer 4 of the sensory cortex. SSCs have axons that have a local arborization pattern and have dendrites that are covered by spines.
- Basket cell
-
A type of interneuron that sends its axon to the cell body of the postsynaptic cell and surrounds it with a structure akin to a basket.
- Dynamic clamp
-
A technique by which the effect of opening ionic channels (a conductance change) is simulated by injecting into a real neuron a current that is proportional to the neuron's membrane potential.
- Network model
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A model comprised of neurons connected by synapses that is used to study the effects of synaptic coupling on the dynamics of neural activity.
- Selective attention
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A cognitive process that is involved in selecting stimuli based on their behavioural relevance.
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Tiesinga, P., Fellous, JM. & Sejnowski, T. Regulation of spike timing in visual cortical circuits. Nat Rev Neurosci 9, 97–107 (2008). https://doi.org/10.1038/nrn2315
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DOI: https://doi.org/10.1038/nrn2315
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