How Silent is the Brain: is There a "dark Matter" Problem in Neuroscience?

Overview

Journal J Comp Physiol A Neuroethol Sens Neural Behav Physiol

Publisher Springer

Specialties Neurology
Social Sciences

Date 2006 Mar 22

PMID 16550391

Citations 94

Authors

Shy Shoham

Daniel H OConnor

Ronen Segev

Affiliations

Soon will be listed here.

Abstract

Evidence from a variety of recording methods suggests that many areas of the brain are far more sparsely active than commonly thought. Here, we review experimental findings pointing to the existence of neurons which fire action potentials rarely or only to very specific stimuli. Because such neurons would be difficult to detect with the most common method of monitoring neural activity in vivo-extracellular electrode recording-they could be referred to as "dark neurons," in analogy to the astrophysical observation that much of the matter in the universe is undetectable, or dark. In addition to discussing the evidence for largely silent neurons, we review technical advances that will ultimately answer the question: how silent is the brain?

Citing Articles

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References

Stepanyants A, Hof P, Chklovskii D . Geometry and structural plasticity of synaptic connectivity. Neuron. 2002; 34(2):275-88. DOI: 10.1016/s0896-6273(02)00652-9. View

RALL W . Electrophysiology of a dendritic neuron model. Biophys J. 1962; 2(2 Pt 2):145-67. PMC: 1366481. DOI: 10.1016/s0006-3495(62)86953-7. View

BARLOW H . Single units and sensation: a neuron doctrine for perceptual psychology?. Perception. 1972; 1(4):371-94. DOI: 10.1068/p010371. View

Fiete I, Hahnloser R, Fee M, Seung H . Temporal sparseness of the premotor drive is important for rapid learning in a neural network model of birdsong. J Neurophysiol. 2004; 92(4):2274-82. DOI: 10.1152/jn.01133.2003. View

Chadderton P, Margrie T, Hausser M . Integration of quanta in cerebellar granule cells during sensory processing. Nature. 2004; 428(6985):856-60. DOI: 10.1038/nature02442. View

Swadlow H . Neocortical efferent neurons with very slowly conducting axons: strategies for reliable antidromic identification. J Neurosci Methods. 1998; 79(2):131-41. DOI: 10.1016/s0165-0270(97)00176-3. View

Heeger D, Huk A, Geisler W, Albrecht D . Spikes versus BOLD: what does neuroimaging tell us about neuronal activity?. Nat Neurosci. 2000; 3(7):631-3. DOI: 10.1038/76572. View

Gross C . Genealogy of the "grandmother cell". Neuroscientist. 2002; 8(5):512-8. DOI: 10.1177/107385802237175. View

Diamond M, Armstrong-James M, Ebner F . Experience-dependent plasticity in adult rat barrel cortex. Proc Natl Acad Sci U S A. 1993; 90(5):2082-6. PMC: 46025. DOI: 10.1073/pnas.90.5.2082. View

10.

Holt G, Koch C . Electrical interactions via the extracellular potential near cell bodies. J Comput Neurosci. 1999; 6(2):169-84. DOI: 10.1023/a:1008832702585. View

11.

Ohki K, Chung S, Chng Y, Kara P, Reid R . Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex. Nature. 2005; 433(7026):597-603. DOI: 10.1038/nature03274. View

12.

Wang J, Wong A, Flores J, Vosshall L, Axel R . Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell. 2003; 112(2):271-82. DOI: 10.1016/s0092-8674(03)00004-7. View

13.

Brecht M, Fee M, Garaschuk O, Helmchen F, Margrie T, Svoboda K . Novel approaches to monitor and manipulate single neurons in vivo. J Neurosci. 2004; 24(42):9223-7. PMC: 6730093. DOI: 10.1523/JNEUROSCI.3344-04.2004. View

14.

Segev R, Shapira Y, Benveniste M, Ben-Jacob E . Observations and modeling of synchronized bursting in two-dimensional neural networks. Phys Rev E Stat Nonlin Soft Matter Phys. 2001; 64(1 Pt 1):011920. DOI: 10.1103/PhysRevE.64.011920. View

15.

Georgopoulos A, Schwartz A, Kettner R . Neuronal population coding of movement direction. Science. 1986; 233(4771):1416-9. DOI: 10.1126/science.3749885. View

16.

Olshausen B, Field D . How close are we to understanding v1?. Neural Comput. 2005; 17(8):1665-99. DOI: 10.1162/0899766054026639. View

17.

Hubel D . Tungsten Microelectrode for Recording from Single Units. Science. 1957; 125(3247):549-50. DOI: 10.1126/science.125.3247.549. View

18.

Okeefe J, Dostrovsky J . The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 1971; 34(1):171-5. DOI: 10.1016/0006-8993(71)90358-1. View

19.

Song S, Sjostrom P, Reigl M, Nelson S, Chklovskii D . Highly nonrandom features of synaptic connectivity in local cortical circuits. PLoS Biol. 2005; 3(3):e68. PMC: 1054880. DOI: 10.1371/journal.pbio.0030068. View

20.

Brecht M, Roth A, Sakmann B . Dynamic receptive fields of reconstructed pyramidal cells in layers 3 and 2 of rat somatosensory barrel cortex. J Physiol. 2003; 553(Pt 1):243-65. PMC: 2343497. DOI: 10.1113/jphysiol.2003.044222. View