Neural oscillations

The concept of neural oscillations is close to the concept of brain waves. However, the latter usually refers to EEG recordings obtained from the skull, and the former refers to more invasive recording techniques such as single-unit recordings with extracellular electrodes, intracellular recordings of neuronal oscillatory potentials. Intracellularly this may be observed as subthreshold membrane potential oscillations (Llinas and Yarom 1986)). Extracellularly they may be recorded as local field potentials (LFPs) using electrodes directly contacting the brain. They occur at different frequency ranges, in different brain areas, and some type of oscillations have been related to particular behaviors. It is important to note that non-action potential oscillations, such as those in LFPs and EEGs, need not be based in neuronal activity or in action potential activity, but in extracellular currents in the neuropil.

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Visual system

Neuronal oscillations became a hot topic in neuroscience in the 1990s when the studies of the visual system of the brain by Gray, Singer and others appeared to support the neural binding hypothesis. According to this idea, synchronous oscillations in neuronal ensembles bind neurons representing different features of an object. For example, when a person looks at a tree, visual cortex neurons representing the tree trunk and those representing the branches of the same tree would oscillate in synchrony to form a single representation of the tree. Some scientists have questioned whether these oscillations are prominent, or relevant, in ensembles that consider only action potential activity^[1]. These oscillations are, however, prominent in differential LFP recordings taken between upper and lower cortical layers, which suggests a local current, but not action potential, basis for their origin^[2].

Olfactory System

In a series of papers beginning in 1994, Gilles Laurent and his colleagues at the California Institute of Technology showed that oscillations exist in the brain of the locust, that different odors lead to different subsets of neurons firing on different sets of oscillatory cycles (Wehr and Laurent, 1996), that the oscillations can be disrupted by GABA blocker picrotoxin (MacLeod and Laurent, 1996), that disruption of the oscillatory synchronization leads to impairment of behavioral discrimination of chemically similar odorants in bees (Stopfer et al., 1997) and to more similar responses across odors in downstream β-lobe neurons (MacLeod et al., 1998).

Motor system

Oscillations have been also reported in the motor system. Murthy and Fetz (1992) described motor cortical oscillations in monkey cortex when the monkeys performed motor acts that required significant attention (retrieval of raisins from unseen locations). Similar oscillations were observed in motor cortex during periods of immobility by the groups of John Donoghue and Roger Lemon.

Oscillating neurons have been also reported in somatosensory cortex (Mikhail Lebedev and Randall Nelson) and in premotor cortex (Mikhail Lebedev and Steven Wise). In these cortical areas, 20-40 Hz oscillations are often observed during periods of attentive immobility, and they typically disappear during movements. These oscillations may well be driven by the highly regular pattern of input activity from muscle spindles to somatosensory proprioceptive areas^[3].

Oscillatory rhythms at 10Hz have been recorded at the motor output (physiological tremor) of inferior olive and thalamic origin that seem to be central in motor timing (Rodolfo Llinas 1986)

Large-scale oscillations

Oscillations recorded from multiple cortical areas can become synchronized and form a large-scale network, whose dynamics and functional connectivity can be studied by means of spectral analyses and Granger causality (Andrea Brovelli, Steven L. Bressler and their colleagues, 2004) measures.

Brain-computer interface

Pesaran, Andersen and their colleagues suggested that neural oscillations can be used as a control signal for brain-computer interfaces because oscillatory pattern depends on the direction of movement that the monkey prepares to execute. Recent study of Rickert and colleagues (2005) supports this suggestion.

Oscillations and perception

Neural oscillations may have different functional roles in different brain areas, and their functional role continues to be a matter of debate. Neural oscillations have been hypothesized to be involved in the sense of time (Buhusi and Meck, 2005) and in somatosensory perception (Ahissar and Zacksenhouse, 2001) among other functions.

Neuronal mechanisms of oscillations

Neuronal mechanisms of oscillations are complex. Scientists suggest that both intrinsic neuronal properties, in particular subthreshold membrane potential oscillations (Rodolfo Llinas 1986 and Llinas and colleagues, 1991) and neural network properties are involved.

References

• Ahissar E, Zacksenhouse M (2001) Temporal and spatial coding in the rat vibrissal system. Prog Brain Res 130: 75-87.
• Engel AK, Konig P, Kreiter AK, Schillen TB, Singer W (1992) Temporal coding in the visual cortex: new vistas on integration in the nervous system. Trends Neurosci. 15: 218-226.
• Baker SN, Kilner JM, Pinches EM, Lemon RN (1999) The role of synchrony and oscillations in the motor output. Exp Brain Res. 128: 109-117.
• Brovelli A, Ding M, Ledberg A, Chen Y, Nakamura R, Bressler SL (2004). Beta oscillations in a large-scale sensorimotor cortical network: Directional influences revealed by Granger causality. Proceed. Natl. Acad. Sci. USA 101: 9849 – 9854.
• Buhusi CV, Meck WH (2005)What makes us tick? Functional and neural mechanisms of interval timing. Nat Rev Neurosci.
• Donoghue JP, Sanes JN, Hatsopoulos NG, Gaal G (1998) Neural discharge and local field potential oscillations in primate motor cortex during voluntary movements. J Neurophysiol 79: 159-173.
• Gray CM (1994) Synchronous oscillations in neuronal systems: mechanisms and functions. J Comput Neurosci. 1: 11-38.
• Lebedev, M.A., Wise, S.P. (2000) Oscillations in the premotor cortex: single-unit activity from awake, behaving monkeys. Exp. Brain Res., 130: 195-215.
• Lebedev, M.A., Nelson, R.J. (1999) Rhythmically firing neostriatal neurons in monkeys: activity patterns during reaction-time hand movements. J. Neurophysiol., 82: 1832-1842.
• Lebedev, M.A., Nelson, R.J. (1995) Rhythmically firing (20-50 Hz) neurons in monkey primary somatosensory cortex: activity patterns during initiation of vibratory-cued hand movements. J. Comput. Neurosci. 2: 313-334.
• Llinas RR. The Intrinsic electrophysiological properties of mammalian neurons: A new insight into CNS function. Science 242: 1654-1664, 1988
• Llinas RR, Grace AA, Yarom Y (1991) In vitro neurons in mammalian cortical layer 4 exhibit intrinsic oscillatory activity in the 10- to 50-Hz frequency range. Proc Natl Acad Sci U S A 88: 897-901.
• Llinas R. and Yarom, Y. Oscillatory properties of guinea-pig inferior olivary neurons and their pharmacological modulation: an in vitro study J. Physiol 376:163-182, 1986
• Murthy VN, Fetz EE (1992) Coherent 25- to 35-Hz oscillations in the sensorimotor cortex of awake behaving monkeys. Proc Natl Acad Sci U S A. 89: 5670-5674.
• Pesaran B, Pezaris JS, Sahani M, Mitra PP, Andersen RA (2002) Temporal structure in neuronal activity during working memory in macaque parietal cortex. Nat Neurosci. 5:805-811.
• Rickert J, Oliveira SC, Vaadia E, Aertsen A, Rotter S, Mehring C (2005) Encoding of movement direction in different frequency ranges of motor cortical local field potentials. J Neurosci. 25:8815-8824.