The meaning of spikes from the neuron's point of view: predictive homeostasis generates the appearance of randomness

Cited 13 time in webofscience Cited 0 time in scopus
  • Hit : 488
  • Download : 245
The conventional interpretation of spikes is from the perspective of an external observer with knowledge of a neuron's inputs and outputs who is ignorant of the contents of the "black box" that is the neuron. Here we consider a neuron to be an observer and we interpret spikes from the neuron's perspective. We propose both a descriptive hypothesis is that a neuron's membrane excitability is "known" and the amplitude of a future excitatory postsynaptic conductance (EPSG) is "unknown". Therefore excitability is an expectation of EPSG amplitude and a spike is generated only when EPSG amplitude exceeds its expectation ("prediction error"). Our prescriptive hypothesis is that a diversity of synaptic inputs and voltage-regulated ion channels implement "predictive homeostasis", working to insure that the expectation is accurate. The homeostatic ideal and optimal expectation would be achieved when an EPSP reaches precisely to spike threshold, so that spike output is exquisitely sensitive to small variations in EPSG input. To an external observer who knows neither EPSG amplitude nor membrane excitability, spikes would appear random if the neuron is making accurate predictions. We review experimental evidence that spike probabilities are indeed maintained near an average of 0.5 under natural conditions, and we suggest that the same principles may also explain why synaptic vesicle release appears to be "stochastic." Whereas the present hypothesis accords with principles of efficient coding dating back to Barlow (1961). it contradicts decades of assertions that neural activity is substantially "random" or "noisy". The apparent randomness is by design, and like many other examples of apparent randomness, it corresponds to the ignorance of external macroscopic observers about the detailed inner workings of a microscopic system.
Publisher
FRONTIERS RESEARCH FOUNDATION
Issue Date
2014-04
Language
English
Article Type
Article
Keywords

LATERAL GENICULATE-NUCLEUS; PROBABILISTIC POPULATION CODES; MEMBRANE-POTENTIAL SYNCHRONY; PRIMARY VISUAL-CORTEX; IN-VIVO; SYNAPTIC-TRANSMISSION; AUDITORY-CORTEX; SINGLE NEURONS; INFORMATION-TRANSMISSION; FEEDFORWARD INHIBITION

Citation

FRONTIERS IN COMPUTATIONAL NEUROSCIENCE, v.8, no.49

ISSN
1662-5188
DOI
10.3389/fncom.2014.00049
URI
http://hdl.handle.net/10203/189157
Appears in Collection
BiS-Journal Papers(저널논문)
Files in This Item
85719.pdf(1.03 MB)Download
This item is cited by other documents in WoS
⊙ Detail Information in WoSⓡ Click to see webofscience_button
⊙ Cited 13 items in WoS Click to see citing articles in records_button

qr_code

  • mendeley

    citeulike


rss_1.0 rss_2.0 atom_1.0