Thilo Womelsdorf | York University (original) (raw)

Papers by Thilo Womelsdorf

Research paper thumbnail of Comparison of Orientation Maps Obtained with Different Number of Stimulus Orientations

Neuroimage, 2001

The structure of orientation maps computed from a different number of stimulus orientations was s... more The structure of orientation maps computed from a different number of stimulus orientations was studied in visual cortical area 18 of the cat. Single condition maps (SCMs) were obtained to 16 stimulus orientations, of which angle maps were generated using 4, 8, and 16 SCMs corresponding to multiples of 45, 22.5, and 11.25°, respectively. The overall orientation distribution of the three types of maps was compared on a pixel-by-pixel basis. Twenty percent of the pixels of the 4-orientations maps differed by more than ؎17°f rom those produced by 16 orientations. Maps of 8 orientations differed by 6.4 and 5.8% from those of 4 and 16 orientations, respectively. Structural differences between the maps were mainly found at locations displaying high rate of change in orientation preference, i.e., orientation centers and adjoining short, fracture-like zones. These changes included lateral shifts up to 155 m (average: 38.7 m) in the position of orientation centers and appearance/disappearance of orientation centers when compared between different conditions. In general, these changes were three times more frequent between maps of 4/8 and 4/16 orientations than 8/16 orientations. It is concluded that orientation maps should be calculated from activity maps representing 8 or more stimulus orientations.

Research paper thumbnail of Selective Attention:Gamma-Range Synchronization between Sensoryand Executive Reconciling Coherent Oscillation with Modulationof Irregular Spiking Activity in

Buia CI, Tiesinga PH. Role of interneuron diversity in the cortical microcircuit for attention. f... more Buia CI, Tiesinga PH. Role of interneuron diversity in the cortical microcircuit for attention. fields of neurons in cortical area V4 are large enough to fit multiple stimuli, making V4 the ideal place to study the effects of selective attention at the single-neuron level. Experiments have revealed evidence for stimulus competition and have characterized the effect thereon of spatial and feature-based attention. We developed a biophysical model with spiking neurons and conductance-based synapses. To account for the comprehensive set of experimental results, it was necessary to include in the model, in addition to regular spiking excitatory (E) cells, two types of interneurons: feedforward interneurons (FFI) and top-down interneurons (TDI). Feature-based attention was mediated by a projection of the TDI to the FFI, stimulus competition was mediated by a cross-columnar excitatory connection to the FFI, whereas spatial attention was mediated by an increase in activity of the feedforward inputs from cortical area V2. The model predicts that spatial attention increases the FFI firing rate, whereas feature-based attention decreases the FFI firing rate and increases the TDI firing rate. During strong stimulus competition, the E cells were synchronous in the beta frequency range (15-35 Hz), but with featurebased attention, they became synchronous in the gamma frequency range (35)(36)(37)(38)(39)(40)(41)(42)(43)(44)(45)(46)(47)(48)(49)(50). We propose that the FFI correspond to fast-spiking, parvalbumin-positive basket cells and that the TDI correspond to cells with a double-bouquet morphology that are immunoreactive to calbindin or calretinin. Taken together, the model results provide an experimentally testable hypothesis for the behavior of two interneuron types under attentional modulation.

Research paper thumbnail of Modeling the influence of spatial attention on visual receptive fields

Frontiers in Computational Neuroscience, 1970

Research paper thumbnail of Predicting human perceptual decisions by decoding neuronal information profiles

Biological Cybernetics, 2008

Perception relies on the response of populations of neurons in sensory cortex. How the response p... more Perception relies on the response of populations of neurons in sensory cortex. How the response profile of a neuronal population gives rise to perception and perceptual discrimination has been conceptualized in various ways. Here we suggest that neuronal population responses represent information about our environment explicitly as Fisher information (FI), which is a local measure of the variance estimate of the sensory input. We show how this sensory information can be read out and combined to infer from the available information profile which stimulus value is perceived during a fine discrimination task. In particular, we propose that the perceived stimulus corresponds to the stimulus value that leads to the same information for each of the alternative directions, and compare the model prediction to standard models considered in the literature (population vector, maximum likelihood, maximum-a-posteriori Bayesian inference). The models are applied to human performance in a motion discrimination task that induces perceptual misjudgements of a target direction of motion by task irrelevant motion in the spatial surround of the target stimulus (motion repulsion). By using the neurophysiological insight that surround motion suppresses neuronal responses to the target motion in the center, all models predicted the pattern of perceptual misjudgements. The variation of discrimination thresholds (error on the perceived value) was also explained through the changes of the total FI content with varying surround motion directions. The proposed FI decoding scheme incorporates recent neurophysiological evidence from macaque visual cortex showing that perceptual decisions do not rely on the most active neurons, but rather on the most informative neuronal responses. We statistically compare the prediction capability of the FI decoding approach and the standard decoding models. Notably, all models reproduced the variation of the perceived stimulus values for different surrounds, but with different neuronal tuning characteristics underlying perception. Compared to the FI approach the prediction power of the standard models was based on neurons with far wider tuning width and stronger surround suppression. Our study demonstrates that perceptual misjudgements can be based on neuronal populations encoding explicitly the available sensory information, and provides testable neurophysiological predictions on neuronal tuning characteristics underlying human perceptual decisions.

Research paper thumbnail of Dynamic shifts of visual receptive fields in cortical area MT by spatial attention

Nature Neuroscience, 2006

Voluntary attention is the top-down selection process that focuses cortical processing resources ... more Voluntary attention is the top-down selection process that focuses cortical processing resources on the most relevant sensory information. Spatial attention-that is, selection based on stimulus position-alters neuronal responsiveness throughout primate visual cortex. It has been hypothesized that it also changes receptive field profiles by shifting their centers toward attended locations and by shrinking them around attended stimuli. Here we examined, at high resolution, receptive fields in cortical area MT of rhesus macaque monkeys when their attention was directed to different locations within and outside these receptive fields. We found a shift of receptive fields, even far from the current location of attention, accompanied by a small amount of shrinkage. Thus, already in early extrastriate cortex, receptive fields are not static entities but are highly modifiable, enabling the dynamic allocation of processing resources to attended locations and supporting enhanced perception within the focus of attention by effectively increasing the local cortical magnification.

Research paper thumbnail of Receptive Field Shift and Shrinkage in Macaque Middle Temporal Area through Attentional Gain Modulation

Journal of Neuroscience, 2008

Selective attention is the top-down mechanism to allocate neuronal processing resources to the mo... more Selective attention is the top-down mechanism to allocate neuronal processing resources to the most relevant subset of the information provided by an organism's sensors. Attentional selection of a spatial location modulates the spatial-tuning characteristics (i.e., the receptive fields of neurons in macaque visual cortex). These tuning changes include a shift of receptive field centers toward the focus of attention and a narrowing of the receptive field when the attentional focus is directed into the receptive field. Here, we report that when attention is directed into versus of receptive fields of neurons in the middle temporal visual area (area MT), the magnitude of the shift of the spatial-tuning functions is positively correlated with a narrowing of spatial tuning around the attentional focus. By developing and applying a general attentional gain model, we show that these nonmultiplicative attentional modulations of basic neuronal-tuning characteristics could be a direct consequence of a spatially distributed multiplicative interaction of a bell-shaped attentional spotlight with the spatially fined-grained sensory inputs of MT neurons. Additionally, the model lets us estimate the spatial spread of the attentional top-down signal impinging on visual cortex. Consistent with psychophysical reports, the estimated size of the "spotlight of attention" indicates a coarse spatial resolution of attention. These results illustrate how spatially specific nonmultiplicative attentional changes of neuronal-tuning functions can be the result of multiplicative gain modulation affecting sensory neurons in a widely distributed region in cortical space.

Research paper thumbnail of Feature-based attention influences contextual interactions during motion repulsion

Vision Research, 2006

Visual perception is strongly shaped by the spatial context in which stimuli are presented. Using... more Visual perception is strongly shaped by the spatial context in which stimuli are presented. Using center-surround configurations with oriented stimuli, recent studies suggest that voluntary attention critically determines which stimuli in the surround affect the percept of the central stimulus. However, evidence for attentional influences on center-surround interactions is restricted to the spatial selection of few among several surround stimuli of different orientations. Here, we extend these insights of center-surround interactions to the motion domain and show that the influence of surround information is critically shaped by feature-based attention. We used motion repulsion as an experimental test tool. When a central target motion was surrounded by a ring of motion, subjects misperceived the direction of the foveal target for particular center-surround direction differences (repulsion condition). Adding an appropriate second motion in the surround counterbalanced the effect, eliminating the repulsion. Introducing feature-based attention to one of the two superimposed directions of motion in the surround reinstated the strong contextual effects. The task relevance of the attended surround motion component effectively induced a strong motion repulsion on the foveally presented stimulus. In addition, the task relevance of the foveal stimulus also induced motion repulsion on the attended surround direction of motion. Our results show that feature-based attention to the surround strongly modulates the veridical perception of a foveally presented motion. The observed attentional effects reflect a feature-based mechanism affecting human perception, by modulating spatial interactions among sensory information and enhancing the attended direction of motion.

Research paper thumbnail of Theta-activity in anterior cingulate cortex predicts task rules and their adjustments following errors

Proceedings of The National Academy of Sciences, 2010

Accomplishing even simple tasks depend on neuronal circuits to configure how incoming sensory sti... more Accomplishing even simple tasks depend on neuronal circuits to configure how incoming sensory stimuli map onto responses. Controlling these stimulus-response (SR) mapping rules relies on a cognitive control network comprising the anterior cingulate cortex (ACC). Single neurons within the ACC convey information about currently relevant SR mapping rules and signal unexpected action outcomes, which can be used to optimize behavioral choices. However, its functional significance and the mechanistic means of interaction with other nodes of the cognitive control network remain elusive and poorly understood. Here, we report that core aspects of cognitive control are encoded by rhythmic theta-band activity within neuronal circuits in the ACC. Throughout task performance, theta-activity predicted which of two SR mapping rules will be established before processing visual target information. Task-selective theta-activity emerged particularly early during those trials, which required the adjustment of SR rules following an erroneous rule representation in the preceding trial. These findings demonstrate a functional correlation of cognitive control processes and oscillatory theta-band activity in macaque ACC. Moreover, we report that spike output of a subset of cells in ACC is synchronized to predictive theta-activity, suggesting that the theta-cycle could serve as a temporal reference for coordinating local task selective computations across a larger network of frontal areas and the hippocampus to optimize and adjust the processing routes of sensory and motor circuits to achieve efficient sensory-motor control.

Research paper thumbnail of Precise spike synchronization in the gamma band increases information gain in awake monkey V1

Frontiers in Systems Neuroscience, 2009

... in area V1 of three awake macaque monkeys performing a fixation task. During fixation, neuron... more ... in area V1 of three awake macaque monkeys performing a fixation task. During fixation, neuronal sites were stimulated with moving gratings of eight different orientations. For each orientation, we calculated the neuronal spiking responses as a function of the LFP gamma-band ...

Research paper thumbnail of Rhythmic Neuronal Synchronization Subserves Selective Attentional Processing

Selective attention relies on dynamic restructuring of cortical information flow to prioritize ne... more Selective attention relies on dynamic restructuring of cortical information flow to prioritize neuronal communication between those neuronal groups conveying information about behaviorally relevant information while reducing the influence from groups encoding irrelevant and distracting information. Electrophysiological evidence suggests that such selective neuronal communication is instantiated and sustained through selective neuronal synchronization of rhythmic gamma band activity within and between neuronal groups. Attentionally modulated synchronization patterns evolve rapidly, are evident even before sensory inputs arrive, follow closely subjective readiness to process information in time, can be sustained for prolonged time periods, and convey specific information about perceptually selected sensory features and motor plans. These functional implications of selective synchronization patterns are complemented by recent insights about the mechanistic origins of rhythmic synchronization at micro- and macro- scales of cortical neuronal processing, suggesting that selective attention is subserved by precise neuronal synchronization that is selective in space, time and frequency.

Research paper thumbnail of The pairwise phase consistency: A bias-free measure of rhythmic neuronal synchronization

Neuroimage, 2010

Oscillatory activity is a widespread phenomenon in nervous systems and has been implicated in num... more Oscillatory activity is a widespread phenomenon in nervous systems and has been implicated in numerous functions. Signals that are generated by two separate neuronal sources often demonstrate a consistent phase-relationship in a particular frequency-band, i.e., they demonstrate rhythmic neuronal synchronization. This consistency is conventionally measured by the PLV (phase-locking value) or the spectral coherence measure. Both statistical measures suffer from significant bias, in that their sample estimates overestimate the population statistics for finite sample sizes. This is a significant problem in the neurosciences where statistical comparisons are often made between conditions with a different number of trials or between neurons with a different number of spikes. We introduce a new circular statistic, the PPC (pairwise phase consistency). We demonstrate that the sample estimate of the PPC is a bias-free and consistent estimator of its corresponding population parameter. We show, both analytically and by means of numerical simulations, that the population statistic of the PPC is equivalent to the population statistic of the squared PLV. The variance and mean squared error of the PPC and PLV are compared. Finally, we demonstrate the practical relevance of the method in actual neuronal data recorded from the orbitofrontal cortex of rats that engage in a two-odour discrimination task. We find a strong increase in rhythmic synchronization of spikes relative to the local field potential (as measured by the PPC) for a wide range of low frequencies (including the thetaband) during the anticipation of sucrose delivery in comparison to the anticipation of quinine delivery. address: M.A.Vinck@uva.nl (M. Vinck). 1 MV conceived the original idea of the pairwise phase consistency and was primarily responsible for theoretical and data analysis.

Research paper thumbnail of Improved (I)CA-noise elimination of electrophysiological data using band-pass filtered components

Frontiers in Systems Neuroscience, 2009

Research paper thumbnail of The role of neuronal synchronization in selective attention

Current Opinion in Neurobiology, 2007

Attention selectively enhances the influence of neuronal responses conveying information about re... more 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.

Research paper thumbnail of Specific Contributions of Ventromedial, Anterior Cingulate, and Lateral Prefrontal Cortex for Attentional Selection and Stimulus Valuation

PLOS Biology, 2011

Attentional control ensures that neuronal processes prioritize the most relevant stimulus in a gi... more Attentional control ensures that neuronal processes prioritize the most relevant stimulus in a given environment. Controlling which stimulus is attended thus originates from neurons encoding the relevance of stimuli, i.e. their expected value, in hand with neurons encoding contextual information about stimulus locations, features, and rules that guide the conditional allocation of attention. Here, we examined how these distinct processes are encoded and integrated in macaque prefrontal cortex (PFC) by mapping their functional topographies at the time of attentional stimulus selection. We find confined clusters of neurons in ventromedial PFC (vmPFC) that predominantly convey stimulus valuation information during attention shifts. These valuation signals were topographically largely separated from neurons predicting the stimulus location to which attention covertly shifted, and which were evident across the complete medial-to-lateral extent of the PFC, encompassing anterior cingulate cortex (ACC), and lateral PFC (LPFC). LPFC responses showed particularly early-onset selectivity and primarily facilitated attention shifts to contralateral targets. Spatial selectivity within ACC was delayed and heterogeneous, with similar proportions of facilitated and suppressed responses during contralateral attention shifts. The integration of spatial and valuation signals about attentional target stimuli was observed in a confined cluster of neurons at the intersection of vmPFC, ACC, and LPFC. These results suggest that valuation processes reflecting stimulus-specific outcome predictions are recruited during covert attentional control. Value predictions and the spatial identification of attentional targets were conveyed by largely separate neuronal populations, but were integrated locally at the intersection of three major prefrontal areas, which may constitute a functional hub within the larger attentional control network.

Research paper thumbnail of Modulation of Neuronal Interactions Through Neuronal Synchronization

Science, 2007

Brain processing depends on the interactions between neuronal groups. Those interactions are gove... more Brain processing depends on the interactions between neuronal groups. Those interactions are governed by the pattern of anatomical connections and by yet unknown mechanisms that modulate the effective strength of a given connection. We found that the mutual influence among neuronal groups depends on the phase relation between rhythmic activities within the groups. Phase relations supporting interactions between the groups preceded those interactions by a few milliseconds, consistent with a mechanistic role. These effects were specific in time, frequency, and space, and we therefore propose that the pattern of synchronization flexibly determines the pattern of neuronal interactions.

Research paper thumbnail of Gamma-band synchronization in visual cortex predicts speed of change detection

Nature, 2006

Our capacity to process and respond behaviourally to multiple incoming stimuli is very limited. T... more Our capacity to process and respond behaviourally to multiple incoming stimuli is very limited. To optimize the use of this limited capacity, attentional mechanisms give priority to behaviourally relevant stimuli at the expense of irrelevant distractors. In visual areas, attended stimuli induce enhanced responses and an improved synchronization of rhythmic neuronal activity in the gamma frequency band (40-70 Hz) 1-11 . Both effects probably improve the neuronal signalling of attended stimuli within and among brain areas 1,12-16 . Attention also results in improved behavioural performance and shortened reaction times. However, it is not known how reaction times are related to either response strength or gamma-band synchronization in visual areas. Here we show that behavioural response times to a stimulus change can be predicted specifically by the degree of gamma-band synchronization among those neurons in monkey visual area V4 that are activated by the behaviourally relevant stimulus. When there are two visual stimuli and monkeys have to detect a change in one stimulus while ignoring the other, their reactions are fastest when the relevant stimulus induces strong gamma-band synchronization before and after the change in stimulus. This enhanced gamma-band synchronization is also followed by shorter neuronal response latencies on the fast trials. Conversely, the monkeys' reactions are slowest when gamma-band synchronization is high in response to the irrelevant distractor. Thus, enhanced neuronal gamma-band synchronization and shortened neuronal response latencies to an attended stimulus seem to have direct effects on visually triggered behaviour, reflecting an early neuronal correlate of efficient visuo-motor integration.

Research paper thumbnail of The effects of visual stimulation and selective visual attention on rhythmic neuronal synchronization in macaque area V4

Journal of Neuroscience, 2008

In addition to the modulation of synchronization during visual stimulation, selective attention s... more 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.

Research paper thumbnail of Gamma-phase shifting in awake monkey visual cortex

Journal of Neuroscience, 2010

Research paper thumbnail of A Microsaccadic Rhythm Modulates Gamma-Band Synchronization and Behavior

Journal of Neuroscience, 2009

Rhythms occur both in neuronal activity and in behavior. Behavioral rhythms abound at frequencies... more 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.

Research paper thumbnail of Neuronal coherence during selective attentional processing and sensory–motor integration

Journal of Physiology-paris, 2006

Groups of neurons synchronize their activities during a variety of conditions, but whether this s... more Groups of neurons synchronize their activities during a variety of conditions, but whether this synchronization is functionally relevant has remained a matter of debate. Here, we survey recent findings showing that synchronization is dynamically modulated during cognitive processes. Based on this evidence, synchronization appears to reflect a general mechanism that renders interactions among selective subsets of neurons effective. We show that neuronal synchronization predicts which sensory input is processed and how efficient it is transmitted to postsynaptic target neurons during sensory-motor integration. Four lines of evidence are presented supporting the hypothesis that rhythmic neuronal synchronization, also called neuronal coherence, underlies effective and selective neuronal communication. (1) Findings from intracellular recordings strongly suggest that postsynaptic neurons are particularly sensitive to synaptic input that is synchronized in the gamma-frequency (30-90 Hz) range. (2) Neurophysiological studies in awake animals revealed enhanced rhythmic synchronization among neurons encoding task-relevant information. (3) The trial-by-trial variation in the precision of neuronal synchronization predicts part of the trial-by-trial variation in the speed of visuo-motor integration. (4) The planning and selection of specific movements can be predicted by the strength of coherent oscillations among local neuronal groups in frontal and parietal cortex. Thus, neuronal coherence appears as a neuronal substrate of an effective neuronal communication structure that dynamically links neurons into functional groups processing task-relevant information and selecting appropriate actions during attention and effective sensory-motor integration.

Research paper thumbnail of Comparison of Orientation Maps Obtained with Different Number of Stimulus Orientations

Neuroimage, 2001

The structure of orientation maps computed from a different number of stimulus orientations was s... more The structure of orientation maps computed from a different number of stimulus orientations was studied in visual cortical area 18 of the cat. Single condition maps (SCMs) were obtained to 16 stimulus orientations, of which angle maps were generated using 4, 8, and 16 SCMs corresponding to multiples of 45, 22.5, and 11.25°, respectively. The overall orientation distribution of the three types of maps was compared on a pixel-by-pixel basis. Twenty percent of the pixels of the 4-orientations maps differed by more than ؎17°f rom those produced by 16 orientations. Maps of 8 orientations differed by 6.4 and 5.8% from those of 4 and 16 orientations, respectively. Structural differences between the maps were mainly found at locations displaying high rate of change in orientation preference, i.e., orientation centers and adjoining short, fracture-like zones. These changes included lateral shifts up to 155 m (average: 38.7 m) in the position of orientation centers and appearance/disappearance of orientation centers when compared between different conditions. In general, these changes were three times more frequent between maps of 4/8 and 4/16 orientations than 8/16 orientations. It is concluded that orientation maps should be calculated from activity maps representing 8 or more stimulus orientations.

Research paper thumbnail of Selective Attention:Gamma-Range Synchronization between Sensoryand Executive Reconciling Coherent Oscillation with Modulationof Irregular Spiking Activity in

Buia CI, Tiesinga PH. Role of interneuron diversity in the cortical microcircuit for attention. f... more Buia CI, Tiesinga PH. Role of interneuron diversity in the cortical microcircuit for attention. fields of neurons in cortical area V4 are large enough to fit multiple stimuli, making V4 the ideal place to study the effects of selective attention at the single-neuron level. Experiments have revealed evidence for stimulus competition and have characterized the effect thereon of spatial and feature-based attention. We developed a biophysical model with spiking neurons and conductance-based synapses. To account for the comprehensive set of experimental results, it was necessary to include in the model, in addition to regular spiking excitatory (E) cells, two types of interneurons: feedforward interneurons (FFI) and top-down interneurons (TDI). Feature-based attention was mediated by a projection of the TDI to the FFI, stimulus competition was mediated by a cross-columnar excitatory connection to the FFI, whereas spatial attention was mediated by an increase in activity of the feedforward inputs from cortical area V2. The model predicts that spatial attention increases the FFI firing rate, whereas feature-based attention decreases the FFI firing rate and increases the TDI firing rate. During strong stimulus competition, the E cells were synchronous in the beta frequency range (15-35 Hz), but with featurebased attention, they became synchronous in the gamma frequency range (35)(36)(37)(38)(39)(40)(41)(42)(43)(44)(45)(46)(47)(48)(49)(50). We propose that the FFI correspond to fast-spiking, parvalbumin-positive basket cells and that the TDI correspond to cells with a double-bouquet morphology that are immunoreactive to calbindin or calretinin. Taken together, the model results provide an experimentally testable hypothesis for the behavior of two interneuron types under attentional modulation.

Research paper thumbnail of Modeling the influence of spatial attention on visual receptive fields

Frontiers in Computational Neuroscience, 1970

Research paper thumbnail of Predicting human perceptual decisions by decoding neuronal information profiles

Biological Cybernetics, 2008

Perception relies on the response of populations of neurons in sensory cortex. How the response p... more Perception relies on the response of populations of neurons in sensory cortex. How the response profile of a neuronal population gives rise to perception and perceptual discrimination has been conceptualized in various ways. Here we suggest that neuronal population responses represent information about our environment explicitly as Fisher information (FI), which is a local measure of the variance estimate of the sensory input. We show how this sensory information can be read out and combined to infer from the available information profile which stimulus value is perceived during a fine discrimination task. In particular, we propose that the perceived stimulus corresponds to the stimulus value that leads to the same information for each of the alternative directions, and compare the model prediction to standard models considered in the literature (population vector, maximum likelihood, maximum-a-posteriori Bayesian inference). The models are applied to human performance in a motion discrimination task that induces perceptual misjudgements of a target direction of motion by task irrelevant motion in the spatial surround of the target stimulus (motion repulsion). By using the neurophysiological insight that surround motion suppresses neuronal responses to the target motion in the center, all models predicted the pattern of perceptual misjudgements. The variation of discrimination thresholds (error on the perceived value) was also explained through the changes of the total FI content with varying surround motion directions. The proposed FI decoding scheme incorporates recent neurophysiological evidence from macaque visual cortex showing that perceptual decisions do not rely on the most active neurons, but rather on the most informative neuronal responses. We statistically compare the prediction capability of the FI decoding approach and the standard decoding models. Notably, all models reproduced the variation of the perceived stimulus values for different surrounds, but with different neuronal tuning characteristics underlying perception. Compared to the FI approach the prediction power of the standard models was based on neurons with far wider tuning width and stronger surround suppression. Our study demonstrates that perceptual misjudgements can be based on neuronal populations encoding explicitly the available sensory information, and provides testable neurophysiological predictions on neuronal tuning characteristics underlying human perceptual decisions.

Research paper thumbnail of Dynamic shifts of visual receptive fields in cortical area MT by spatial attention

Nature Neuroscience, 2006

Voluntary attention is the top-down selection process that focuses cortical processing resources ... more Voluntary attention is the top-down selection process that focuses cortical processing resources on the most relevant sensory information. Spatial attention-that is, selection based on stimulus position-alters neuronal responsiveness throughout primate visual cortex. It has been hypothesized that it also changes receptive field profiles by shifting their centers toward attended locations and by shrinking them around attended stimuli. Here we examined, at high resolution, receptive fields in cortical area MT of rhesus macaque monkeys when their attention was directed to different locations within and outside these receptive fields. We found a shift of receptive fields, even far from the current location of attention, accompanied by a small amount of shrinkage. Thus, already in early extrastriate cortex, receptive fields are not static entities but are highly modifiable, enabling the dynamic allocation of processing resources to attended locations and supporting enhanced perception within the focus of attention by effectively increasing the local cortical magnification.

Research paper thumbnail of Receptive Field Shift and Shrinkage in Macaque Middle Temporal Area through Attentional Gain Modulation

Journal of Neuroscience, 2008

Selective attention is the top-down mechanism to allocate neuronal processing resources to the mo... more Selective attention is the top-down mechanism to allocate neuronal processing resources to the most relevant subset of the information provided by an organism's sensors. Attentional selection of a spatial location modulates the spatial-tuning characteristics (i.e., the receptive fields of neurons in macaque visual cortex). These tuning changes include a shift of receptive field centers toward the focus of attention and a narrowing of the receptive field when the attentional focus is directed into the receptive field. Here, we report that when attention is directed into versus of receptive fields of neurons in the middle temporal visual area (area MT), the magnitude of the shift of the spatial-tuning functions is positively correlated with a narrowing of spatial tuning around the attentional focus. By developing and applying a general attentional gain model, we show that these nonmultiplicative attentional modulations of basic neuronal-tuning characteristics could be a direct consequence of a spatially distributed multiplicative interaction of a bell-shaped attentional spotlight with the spatially fined-grained sensory inputs of MT neurons. Additionally, the model lets us estimate the spatial spread of the attentional top-down signal impinging on visual cortex. Consistent with psychophysical reports, the estimated size of the "spotlight of attention" indicates a coarse spatial resolution of attention. These results illustrate how spatially specific nonmultiplicative attentional changes of neuronal-tuning functions can be the result of multiplicative gain modulation affecting sensory neurons in a widely distributed region in cortical space.

Research paper thumbnail of Feature-based attention influences contextual interactions during motion repulsion

Vision Research, 2006

Visual perception is strongly shaped by the spatial context in which stimuli are presented. Using... more Visual perception is strongly shaped by the spatial context in which stimuli are presented. Using center-surround configurations with oriented stimuli, recent studies suggest that voluntary attention critically determines which stimuli in the surround affect the percept of the central stimulus. However, evidence for attentional influences on center-surround interactions is restricted to the spatial selection of few among several surround stimuli of different orientations. Here, we extend these insights of center-surround interactions to the motion domain and show that the influence of surround information is critically shaped by feature-based attention. We used motion repulsion as an experimental test tool. When a central target motion was surrounded by a ring of motion, subjects misperceived the direction of the foveal target for particular center-surround direction differences (repulsion condition). Adding an appropriate second motion in the surround counterbalanced the effect, eliminating the repulsion. Introducing feature-based attention to one of the two superimposed directions of motion in the surround reinstated the strong contextual effects. The task relevance of the attended surround motion component effectively induced a strong motion repulsion on the foveally presented stimulus. In addition, the task relevance of the foveal stimulus also induced motion repulsion on the attended surround direction of motion. Our results show that feature-based attention to the surround strongly modulates the veridical perception of a foveally presented motion. The observed attentional effects reflect a feature-based mechanism affecting human perception, by modulating spatial interactions among sensory information and enhancing the attended direction of motion.

Research paper thumbnail of Theta-activity in anterior cingulate cortex predicts task rules and their adjustments following errors

Proceedings of The National Academy of Sciences, 2010

Accomplishing even simple tasks depend on neuronal circuits to configure how incoming sensory sti... more Accomplishing even simple tasks depend on neuronal circuits to configure how incoming sensory stimuli map onto responses. Controlling these stimulus-response (SR) mapping rules relies on a cognitive control network comprising the anterior cingulate cortex (ACC). Single neurons within the ACC convey information about currently relevant SR mapping rules and signal unexpected action outcomes, which can be used to optimize behavioral choices. However, its functional significance and the mechanistic means of interaction with other nodes of the cognitive control network remain elusive and poorly understood. Here, we report that core aspects of cognitive control are encoded by rhythmic theta-band activity within neuronal circuits in the ACC. Throughout task performance, theta-activity predicted which of two SR mapping rules will be established before processing visual target information. Task-selective theta-activity emerged particularly early during those trials, which required the adjustment of SR rules following an erroneous rule representation in the preceding trial. These findings demonstrate a functional correlation of cognitive control processes and oscillatory theta-band activity in macaque ACC. Moreover, we report that spike output of a subset of cells in ACC is synchronized to predictive theta-activity, suggesting that the theta-cycle could serve as a temporal reference for coordinating local task selective computations across a larger network of frontal areas and the hippocampus to optimize and adjust the processing routes of sensory and motor circuits to achieve efficient sensory-motor control.

Research paper thumbnail of Precise spike synchronization in the gamma band increases information gain in awake monkey V1

Frontiers in Systems Neuroscience, 2009

... in area V1 of three awake macaque monkeys performing a fixation task. During fixation, neuron... more ... in area V1 of three awake macaque monkeys performing a fixation task. During fixation, neuronal sites were stimulated with moving gratings of eight different orientations. For each orientation, we calculated the neuronal spiking responses as a function of the LFP gamma-band ...

Research paper thumbnail of Rhythmic Neuronal Synchronization Subserves Selective Attentional Processing

Selective attention relies on dynamic restructuring of cortical information flow to prioritize ne... more Selective attention relies on dynamic restructuring of cortical information flow to prioritize neuronal communication between those neuronal groups conveying information about behaviorally relevant information while reducing the influence from groups encoding irrelevant and distracting information. Electrophysiological evidence suggests that such selective neuronal communication is instantiated and sustained through selective neuronal synchronization of rhythmic gamma band activity within and between neuronal groups. Attentionally modulated synchronization patterns evolve rapidly, are evident even before sensory inputs arrive, follow closely subjective readiness to process information in time, can be sustained for prolonged time periods, and convey specific information about perceptually selected sensory features and motor plans. These functional implications of selective synchronization patterns are complemented by recent insights about the mechanistic origins of rhythmic synchronization at micro- and macro- scales of cortical neuronal processing, suggesting that selective attention is subserved by precise neuronal synchronization that is selective in space, time and frequency.

Research paper thumbnail of The pairwise phase consistency: A bias-free measure of rhythmic neuronal synchronization

Neuroimage, 2010

Oscillatory activity is a widespread phenomenon in nervous systems and has been implicated in num... more Oscillatory activity is a widespread phenomenon in nervous systems and has been implicated in numerous functions. Signals that are generated by two separate neuronal sources often demonstrate a consistent phase-relationship in a particular frequency-band, i.e., they demonstrate rhythmic neuronal synchronization. This consistency is conventionally measured by the PLV (phase-locking value) or the spectral coherence measure. Both statistical measures suffer from significant bias, in that their sample estimates overestimate the population statistics for finite sample sizes. This is a significant problem in the neurosciences where statistical comparisons are often made between conditions with a different number of trials or between neurons with a different number of spikes. We introduce a new circular statistic, the PPC (pairwise phase consistency). We demonstrate that the sample estimate of the PPC is a bias-free and consistent estimator of its corresponding population parameter. We show, both analytically and by means of numerical simulations, that the population statistic of the PPC is equivalent to the population statistic of the squared PLV. The variance and mean squared error of the PPC and PLV are compared. Finally, we demonstrate the practical relevance of the method in actual neuronal data recorded from the orbitofrontal cortex of rats that engage in a two-odour discrimination task. We find a strong increase in rhythmic synchronization of spikes relative to the local field potential (as measured by the PPC) for a wide range of low frequencies (including the thetaband) during the anticipation of sucrose delivery in comparison to the anticipation of quinine delivery. address: M.A.Vinck@uva.nl (M. Vinck). 1 MV conceived the original idea of the pairwise phase consistency and was primarily responsible for theoretical and data analysis.

Research paper thumbnail of Improved (I)CA-noise elimination of electrophysiological data using band-pass filtered components

Frontiers in Systems Neuroscience, 2009

Research paper thumbnail of The role of neuronal synchronization in selective attention

Current Opinion in Neurobiology, 2007

Attention selectively enhances the influence of neuronal responses conveying information about re... more 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.

Research paper thumbnail of Specific Contributions of Ventromedial, Anterior Cingulate, and Lateral Prefrontal Cortex for Attentional Selection and Stimulus Valuation

PLOS Biology, 2011

Attentional control ensures that neuronal processes prioritize the most relevant stimulus in a gi... more Attentional control ensures that neuronal processes prioritize the most relevant stimulus in a given environment. Controlling which stimulus is attended thus originates from neurons encoding the relevance of stimuli, i.e. their expected value, in hand with neurons encoding contextual information about stimulus locations, features, and rules that guide the conditional allocation of attention. Here, we examined how these distinct processes are encoded and integrated in macaque prefrontal cortex (PFC) by mapping their functional topographies at the time of attentional stimulus selection. We find confined clusters of neurons in ventromedial PFC (vmPFC) that predominantly convey stimulus valuation information during attention shifts. These valuation signals were topographically largely separated from neurons predicting the stimulus location to which attention covertly shifted, and which were evident across the complete medial-to-lateral extent of the PFC, encompassing anterior cingulate cortex (ACC), and lateral PFC (LPFC). LPFC responses showed particularly early-onset selectivity and primarily facilitated attention shifts to contralateral targets. Spatial selectivity within ACC was delayed and heterogeneous, with similar proportions of facilitated and suppressed responses during contralateral attention shifts. The integration of spatial and valuation signals about attentional target stimuli was observed in a confined cluster of neurons at the intersection of vmPFC, ACC, and LPFC. These results suggest that valuation processes reflecting stimulus-specific outcome predictions are recruited during covert attentional control. Value predictions and the spatial identification of attentional targets were conveyed by largely separate neuronal populations, but were integrated locally at the intersection of three major prefrontal areas, which may constitute a functional hub within the larger attentional control network.

Research paper thumbnail of Modulation of Neuronal Interactions Through Neuronal Synchronization

Science, 2007

Brain processing depends on the interactions between neuronal groups. Those interactions are gove... more Brain processing depends on the interactions between neuronal groups. Those interactions are governed by the pattern of anatomical connections and by yet unknown mechanisms that modulate the effective strength of a given connection. We found that the mutual influence among neuronal groups depends on the phase relation between rhythmic activities within the groups. Phase relations supporting interactions between the groups preceded those interactions by a few milliseconds, consistent with a mechanistic role. These effects were specific in time, frequency, and space, and we therefore propose that the pattern of synchronization flexibly determines the pattern of neuronal interactions.

Research paper thumbnail of Gamma-band synchronization in visual cortex predicts speed of change detection

Nature, 2006

Our capacity to process and respond behaviourally to multiple incoming stimuli is very limited. T... more Our capacity to process and respond behaviourally to multiple incoming stimuli is very limited. To optimize the use of this limited capacity, attentional mechanisms give priority to behaviourally relevant stimuli at the expense of irrelevant distractors. In visual areas, attended stimuli induce enhanced responses and an improved synchronization of rhythmic neuronal activity in the gamma frequency band (40-70 Hz) 1-11 . Both effects probably improve the neuronal signalling of attended stimuli within and among brain areas 1,12-16 . Attention also results in improved behavioural performance and shortened reaction times. However, it is not known how reaction times are related to either response strength or gamma-band synchronization in visual areas. Here we show that behavioural response times to a stimulus change can be predicted specifically by the degree of gamma-band synchronization among those neurons in monkey visual area V4 that are activated by the behaviourally relevant stimulus. When there are two visual stimuli and monkeys have to detect a change in one stimulus while ignoring the other, their reactions are fastest when the relevant stimulus induces strong gamma-band synchronization before and after the change in stimulus. This enhanced gamma-band synchronization is also followed by shorter neuronal response latencies on the fast trials. Conversely, the monkeys' reactions are slowest when gamma-band synchronization is high in response to the irrelevant distractor. Thus, enhanced neuronal gamma-band synchronization and shortened neuronal response latencies to an attended stimulus seem to have direct effects on visually triggered behaviour, reflecting an early neuronal correlate of efficient visuo-motor integration.

Research paper thumbnail of The effects of visual stimulation and selective visual attention on rhythmic neuronal synchronization in macaque area V4

Journal of Neuroscience, 2008

In addition to the modulation of synchronization during visual stimulation, selective attention s... more 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.

Research paper thumbnail of Gamma-phase shifting in awake monkey visual cortex

Journal of Neuroscience, 2010

Research paper thumbnail of A Microsaccadic Rhythm Modulates Gamma-Band Synchronization and Behavior

Journal of Neuroscience, 2009

Rhythms occur both in neuronal activity and in behavior. Behavioral rhythms abound at frequencies... more 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.

Research paper thumbnail of Neuronal coherence during selective attentional processing and sensory–motor integration

Journal of Physiology-paris, 2006

Groups of neurons synchronize their activities during a variety of conditions, but whether this s... more Groups of neurons synchronize their activities during a variety of conditions, but whether this synchronization is functionally relevant has remained a matter of debate. Here, we survey recent findings showing that synchronization is dynamically modulated during cognitive processes. Based on this evidence, synchronization appears to reflect a general mechanism that renders interactions among selective subsets of neurons effective. We show that neuronal synchronization predicts which sensory input is processed and how efficient it is transmitted to postsynaptic target neurons during sensory-motor integration. Four lines of evidence are presented supporting the hypothesis that rhythmic neuronal synchronization, also called neuronal coherence, underlies effective and selective neuronal communication. (1) Findings from intracellular recordings strongly suggest that postsynaptic neurons are particularly sensitive to synaptic input that is synchronized in the gamma-frequency (30-90 Hz) range. (2) Neurophysiological studies in awake animals revealed enhanced rhythmic synchronization among neurons encoding task-relevant information. (3) The trial-by-trial variation in the precision of neuronal synchronization predicts part of the trial-by-trial variation in the speed of visuo-motor integration. (4) The planning and selection of specific movements can be predicted by the strength of coherent oscillations among local neuronal groups in frontal and parietal cortex. Thus, neuronal coherence appears as a neuronal substrate of an effective neuronal communication structure that dynamically links neurons into functional groups processing task-relevant information and selecting appropriate actions during attention and effective sensory-motor integration.