Attention modulates synchronized neuronal firing in primate somatosensory cortex (original) (raw)
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The role of neuronal synchronization in selective attention
Current Opinion in Neurobiology, 2007
Attention selectively enhances the influence of neuronal responses conveying information about relevant sensory attributes. Accumulating evidence suggests that this selective neuronal modulation relies on rhythmic synchronization at local and long-range spatial scales: attention selectively synchronizes the rhythmic responses of those neurons that are tuned to the spatial and featural attributes of the attended sensory input. The strength of synchronization is thereby functionally related to perceptual accuracy and behavioural efficiency. Complementing this synchronization at a local level, attention has recently been demonstrated to regulate which locally synchronized neuronal groups phase-synchronize their rhythmic activity across long-range connections. These results point to a general computational role for selective synchronization in dynamically controlling which neurons communicate information about sensory inputs effectively. Addresses Papers of particular interest, published within the period of review, have been highlighted as: of special interest of outstanding interest 1. Reynolds JH, Chelazzi L: Attentional modulation of visual processing. Annu Rev Neurosci 2004, 27:611-647. 2. Maunsell JH, Treue S: Feature-based attention in visual cortex. Trends Neurosci 2006, 29:317-322. 3. Miller BT, D'Esposito M: Searching for 'the top' in top-down control. Neuron 2005, 48:535-538. 4. Fries P: A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cogn Sci 2005, 9:474-480. 5. Fries P, Reynolds JH, Rorie AE, Desimone R: Modulation of oscillatory neuronal synchronization by selective visual attention. Science 2001, 291:1560-1563.
Journal of Neuroscience, 2008
In addition to the modulation of synchronization during visual stimulation, selective attention significantly changed the prestimulus pattern of synchronization. Attention inside the receptive field of the recorded neuronal population enhanced gamma-band synchronization and strongly reduced ␣-band (9 -11 Hz) synchronization in the prestimulus period. These results lend further support for a functional role of rhythmic neuronal synchronization in attentional stimulus selection.
Coincidence detection or temporal integration? What the neurons in somatosensory cortex are doing
The Journal of neuroscience : the official journal of the Society for Neuroscience, 2001
To assess the impact of thalamic synchronization on cortical responsiveness, we used conditional cross-correlation analysis to measure the probability of neuronal discharges in somatosensory cortex as a function of the time between discharges in pairs of simultaneously recorded neurons in the ventrobasal thalamus. Among 26 neuronal trios, we found that thalamocortical efficacy after synchronous thalamic activity was nearly twice as large as the efficacy rate obtained when pairs of thalamic neurons discharged asynchronously. Nearly half of these neuronal trios displayed cooperative effects in which the cortical discharge probability after synchronous thalamic events was larger than could be predicted from the efficacy rate of individual thalamic discharges. In these cases of heterosynaptic cooperativity, thalamocortical efficacy declined to asymptotic levels when the interspike intervals were >6-8 msec. These results indicate that thalamic synchronization has a significant impact ...
2012
35 The correlated discharges of cortical neurons in primary somatosensory cortex are 36 a potential source of information about somatosensory stimuli. One aspect of neuronal 37 correlations that has not been well studied is how the spatiotemporal properties of tactile 38 stimuli affect the presence and magnitude of correlations. We presented singleand dual39 point stimuli with varying spatiotemporal relationships to the hands of three anesthetized 40 owl monkeys and recorded neuronal activity from 100-electrode arrays implanted in 41 primary somatosensory cortex. Correlation magnitudes derived from joint peristimulus 42 time histogram (JPSTH) analysis of single neuron pairs were used to determine the level 43 of spike timing correlations under selected spatiotemporal stimulus conditions. 44 Correlated activities between neuron pairs were commonly observed, and the proportions 45 of correlated pairs tended to decrease with distance between the recorded neurons. 46 Distance between st...
Synchronization of Neuronal Responses in Primary Visual Cortex of Monkeys Viewing Natural Images
Journal of Neurophysiology, 2008
When inspecting visual scenes, primates perform on average four saccadic eye movements per second which implies that scene segmentation, feature binding and identification of image components is accomplished in less than 200ms. Thus, individual neurons can contribute only a small number of discharges for these complex computations, suggesting that information is encoded not only in the discharge rate but also in the timing of action potentials. While monkeys inspected natural scenes we registered with multi-electrodes from primary visual cortex, the discharges of simultaneously recorded neurons. Relating these signals to eye movements, revealed that discharge rates peaked around 90ms after fixation onset and then decreased to near baseline levels within 200ms. Unitary event analysis revealed that preceding this increase in firing, there was an episode of enhanced response synchronization during which discharges of spatially distributed cells coincided within 5ms windows significantly more often than predicted by the discharge rates. This episode started 30ms after fixation onset and ended by the time discharge rates had reached their maximum. When the animals scanned a blank screen a small change in firing rate but no excess synchronization was observed. The short latency of the stimulation related synchronization phenomena suggests a fast acting mechanism for the coordination of spike timing that may contribute to the basic operations of scene segmentation. T w 2 before the end of the trial. At each position of the window all the data within the window were analyzed for unitary events and the analysis was repeated sequentially for the next positions kh t t k + = 0 , with k being the index of the window positions. The results Bartlett JR, Doty RW, Lee BB, Sakakura H. Influence of saccadic eye movements on geniculostriate excitability in normal monkeys. Exp. Brain Res. 25:487-509, 1976 Buisseret P, Maffei L. Extraocular proprioceptive projections to the visual cortex. Exp. Brain Res. 28: 421-425, 1977. Burr DC, Morrone MC, Ross J. Selective suppression of the magnocellular visual pathway during saccadic eye movements. Nature 371: 511-513, 1994. Castelo-Branco M, Neuenschwander S, Singer W. Synchronization of visual responses between the cortex, lateral geniculate nucleus, and retina in the anesthetized cat. Fabre-Thorpe M, Delorme A, Marlot C, Thorpe S. A limit to the speed of processing in ultra-rapid visual categorization of novel natural scenes. J. Cogn. Neurosci. 13: 171-180, 2001. Friedman-Hill S, Maldonado PE, Gray CM. Dynamics of striate cortical activity in the alert macaque: I. Incidence and stimulus-dependence of gamma-band neuronal oscillations. Fries P, Reynolds JH, Rorie AE, Desimone R. Modulation of oscillatory neuronal synchronization by selective visual attention. Science 291: 1560-1563, 2001. Gerstein GL. Searching for significance in spatio-temporal firing patterns. Acta Neurobiol. Exp.(Wars.) 64: 203-207, 2004. Gray CM, Maldonado PE, Wilson M, McNaughton B. Tetrodes markedly improve the reliability and yield of multiple single-unit isolation from multi-unit recordings in cat striate cortex.
Attentional Stimulus Selection through Selective Synchronization between Monkey Visual Areas
Neuron, 2012
A central motif in neuronal networks is convergence, linking several input neurons to one target neuron. In visual cortex, convergence renders target neurons responsive to complex stimuli. Yet, convergence typically sends multiple stimuli to a target, and the behaviorally relevant stimulus must be selected. We used two stimuli, activating separate electrocorticographic V1 sites, and both activating an electrocorticographic V4 site equally strongly. When one of those stimuli activated one V1 site, it gamma synchronized (60-80 Hz) to V4. When the two stimuli activated two V1 sites, primarily the relevant one gamma synchronized to V4. Frequency bands of gamma activities showed substantial overlap containing the band of interareal coherence. The relevant V1 site had its gamma peak frequency 2-3 Hz higher than the irrelevant V1 site and 4-6 Hz higher than V4. Gamma-mediated interareal influences were predominantly directed from V1 to V4. We propose that selective synchronization renders relevant input effective, thereby modulating effective connectivity.
Journal of Neuroscience, 2006
Rhythms occur both in neuronal activity and in behavior. Behavioral rhythms abound at frequencies at or below 10 Hz. Neuronal rhythms cover a very wide frequency range, and the phase of neuronal low-frequency rhythms often rhythmically modulates the strength of higher-frequency rhythms, particularly of gamma-band synchronization (GBS). Here, we study stimulus-induced GBS in awake monkey areas V1 and V4 in relation to a specific form of spontaneous behavior, namely microsaccades (MSs), small fixational eye movements. We found that MSs occur rhythmically at a frequency of ϳ3.3 Hz. The rhythmic MSs were predicted by the phase of the 3.3 Hz rhythm in V1 and V4 local field potentials. In turn, the MSs modulated both visually induced GBS and the speed of visually triggered behavioral responses. Fast/slow responses were preceded by a specific temporal pattern of MSs. These MS patterns induced perturbations in GBS that in turn explained variability in behavioral response speed. We hypothesize that the 3.3 Hz rhythm structures the sampling and exploration of the environment through building and breaking neuronal ensembles synchronized in the gamma-frequency band to process sensory stimuli.
Journal of Neurophysiology, 2012
The correlated discharges of cortical neurons in primary somatosensory cortex are a potential source of information about somatosensory stimuli. One aspect of neuronal correlations that has not been well studied is how the spatiotemporal properties of tactile stimuli affect the presence and magnitude of correlations. We presented single- and dual-point stimuli with varying spatiotemporal relationships to the hands of three anesthetized owl monkeys and recorded neuronal activity from 100-electrode arrays implanted in primary somatosensory cortex. Correlation magnitudes derived from joint peristimulus time histogram (JPSTH) analysis of single neuron pairs were used to determine the level of spike timing correlations under selected spatiotemporal stimulus conditions. Correlated activities between neuron pairs were commonly observed, and the proportions of correlated pairs tended to decrease with distance between the recorded neurons. Distance between stimulus sites also affected correl...
Effects of stimulus-driven synchronization on sensory perception
Behavioral and Brain Functions, 2007
Background: A subject's ability to differentiate the loci of two points on the skin depends on the stimulus-evoked pericolumnar lateral inhibitory interactions which increase the spatial contrast between regions of SI cortex that are activated by stimulus-evoked afferent drive. Nevertheless, there is very little known about the impact that neuronal interactions -such as those evoked by mechanical skin stimuli that project to and coordinate synchronized activity in adjacent and/or near-adjacent cortical columns -could have on sensory information processing.