Scientific Understanding of Consciousness
Consciousness as an Emergent Property of Thalamocortical Activity

Attention -- Recent Research


Citation: Masuda N, Doiron B (2007) Gamma Oscillations of Spiking Neural Populations Enhance Signal Discrimination. PLoS Comput Biol 3(11): e236. doi:10.1371/journal.pcbi.0030236

Gamma Oscillations of Spiking Neural Populations Enhance Signal Discrimination

Naoki Masuda 1 ,2, Brent Doiron 3

1 Graduate School of Information Science and Technology, the University of Tokyo, Bunkyo, Tokyo, Japan, 2 Amari Research Unit, RIKEN Brain Science Institute, Wako, Saitama, Japan, 3 Center for Neural Science, New York University, New York, New York, United States of America


Selective attention is an important filter for complex environments where distractions compete with signals. Attention increases both the gamma-band power of cortical local field potentials and the spike-field coherence within the receptive field of an attended object. However, the mechanisms by which gamma-band activity enhances, if at all, the encoding of input signals are not well understood. We propose that gamma oscillations induce binomial-like spike-count statistics across noisy neural populations. Using simplified models of spiking neurons, we show how the discrimination of static signals based on the population spike-count response is improved with gamma induced binomial statistics. These results give an important mechanistic link between the neural correlates of attention and the discrimination tasks where attention is known to enhance performance. Further, they show how a rhythmicity of spike responses can enhance coding schemes that are not temporally sensitive.

Author Summary

Rhythmic brain activity is observed in many neural structures and is an inferred critical component of neural processing. In particular, stimulus induced oscillations in the gamma-frequency band (30–80 Hz) are common in several cortical networks. Many experimental and theoretical studies have established the neural mechanisms by which a population of neurons produce and control gamma-band activity. However, the beneficial role, if any, of gamma activity in neural processing is rarely discussed. It is increasingly apparent that gamma oscillatory power increases with subject attention to a sensory scene. Attention is associated with enhanced performance of discrimination tasks, where relevant stimuli compete with distracters. In this study we explore how gamma-band activity serves to enhance the discrimination of stimuli. We use computational models to show that the gamma rhythmicity in a population of spiking neurons drastically reduces the response variability when a preferred stimulus is present. This drop in response variability enhances stimulus discrimination and increases the overall information throughput in sensory cortex. Our results provide a much-needed link between the dynamics of neural populations and the coding tasks they perform, as well as give insight on why—rather than how—attention mediates gamma activity.


Science 23 February 2001: Vol. 291. no. 5508, pp. 1560 - 1563

Modulation of Oscillatory Neuronal Synchronization by Selective Visual Attention

Pascal Fries,1* John H. Reynolds,1, 2 Alan E. Rorie,1 Robert Desimone1

1 Laboratory of Neuropsychology, National Institute of Mental Health, National Institutes of Health, Building 49, Room 1B80, 9000 Rockville Pike, Bethesda, MD 20892-4415, USA.
2 Systems Neurobiology Laboratory, The Salk Institute for Biological Studies, 10010 North Torrey Pines Road, La Jolla, CA 92037-1099, USA.

In crowded visual scenes, attention is needed to select relevant stimuli. To study the underlying mechanisms, we recorded neurons in cortical area V4 while macaque monkeys attended to behaviorally relevant stimuli and ignored distracters. Neurons activated by the attended stimulus showed increased gamma-frequency (35 to 90 hertz) synchronization but reduced low-frequency (<17 hertz) synchronization compared with neurons at nearby V4 sites activated by distracters. Because postsynaptic integration times are short, these localized changes in synchronization may serve to amplify behaviorally relevant signals in the cortex.


Science 15 June 2007: Vol. 316. no. 5831, pp. 1612 - 1615

Neural Mechanisms of Visual Attention: How Top-Down Feedback Highlights Relevant Locations

Yuri B. Saalmann,1 Ivan N. Pigarev,2 Trichur R. Vidyasagar1

1 Department of Optometry and Vision Sciences, The University of Melbourne, Parkville 3010, Australia.
2 Institute for Information Transmission Problems, Russian Academy of Sciences, Bol'shoy Karetniy 19, 127994 Moscow, Russia.

Attention helps us process potentially important objects by selectively increasing the activity of sensory neurons that represent the relevant locations and features of our environment. This selection process requires top-down feedback about what is important in our environment. We investigated how parietal cortical output influences neural activity in early sensory areas. Neural recordings were made simultaneously from the posterior parietal cortex and an earlier area in the visual pathway, the medial temporal area, of macaques performing a visual matching task. When the monkey selectively attended to a location, the timing of activities in the two regions became synchronized, with the parietal cortex leading the medial temporal area. Parietal neurons may thus selectively increase activity in earlier sensory areas to enable focused spatial attention.


Science 29 May 2009: Vol. 324. no. 5931, pp. 1207 - 1210

High-Frequency, Long-Range Coupling Between Prefrontal and Visual Cortex During Attention

Georgia G. Gregoriou,1 Stephen J. Gotts,2 Huihui Zhou,1 Robert Desimone1

1 McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
2 Laboratory of Brain and Cognition, National Institute of Mental Health, National Institutes of Health, Bethesda, MD 20892, USA.

Electrical recordings in humans and monkeys show attentional enhancement of evoked responses and gamma synchrony in ventral stream cortical areas. Does this synchrony result from intrinsic activity in visual cortex or from inputs from other structures? Using paired recordings in the frontal eye field (FEF) and area V4, we found that attention to a stimulus in their joint receptive field leads to enhanced oscillatory coupling between the two areas, particularly at gamma frequencies. This coupling appeared to be initiated by FEF and was time-shifted by about 8 to 13 milliseconds across a range of frequencies. Considering the expected conduction and synaptic delays between the areas, this time-shifted coupling at gamma frequencies may optimize the postsynaptic impact of spikes from one area upon the other, improving cross-area communication with attention.

A typical crowded scene contains many objects that cannot be processed simultaneously, thus requiring attentional mechanisms to select the ones most relevant to behavior. Electrophysiological studies in monkeys have shown that attention leads to enhanced responses of neurons in ventral stream areas that are important for object recognition, at the expense of responses to distracting stimuli. Moreover, attention increases neural synchrony, often in the gamma frequency range. Given that cells have limited integration times, increases in synchrony and firing rates may together have a larger impact on downstream neurons and thus increase the effectiveness of behaviorally relevant stimuli. Areas in the prefrontal cortex (PFC) and parietal cortex may be sources of the top-down attentional feedback to ventral stream areas, which could enhance firing rates with attention.


Nature 421, 370-373 (23 January 2003)

Selective gating of visual signals by microstimulation of frontal cortex

Tirin Moore & Katherine M. Armstrong

Department of Psychology, Princeton University, Princeton, New Jersey 08544, USA

Several decades of psychophysical and neurophysiological studies have established that visual signals are enhanced at the locus of attention. What remains a mystery is the mechanism that initiates biases in the strength of visual representations. Recent evidence argues that, during spatial attention, these biases reflect nascent saccadic eye movement commands. We examined the functional interaction of saccade preparation and visual coding by electrically stimulating sites within the frontal eye fields (FEF) and measuring its effect on the activity of neurons in extrastriate visual cortex. Here we show that visual responses in area V4 could be enhanced after brief stimulation of retinotopically corresponding sites within the FEF using currents below that needed to evoke saccades. The magnitude of the enhancement depended on the effectiveness of receptive field stimuli as well as on the presence of competing stimuli outside the receptive field. Stimulation of non-corresponding FEF representations could suppress V4 responses. The results suggest that the gain of visual signals is modified according to the strength of spatially corresponding eye movement commands.


Nature 454, 1110-1114 (28 August 2008)

Acetylcholine contributes through muscarinic receptors to attentional modulation in V1

J. L. Herrero, M. J. Roberts, L. S. Delicato, M. A. Gieselmann, P. Dayan, A. Thiele

Institute of Neuroscience, Newcastle University, Newcastle upon Tyne NE2 4HH, UK

Gatsby Computational Neuroscience Unit, University College London, 17 Queens Square, London WCIN 3AR, UK

Present addresses: F. C. Donders Centre for Cognitive Neuroimaging, PO Box 9101, 6500 HB Nijmegen, The Netherlands (M.J.R.); Department of Psychology, School of Business, Law & Psychology, University of Sunderland, Sunderland SR6 0DD, UK (L.S.D.).

Attention exerts a strong influence over neuronal processing in cortical areas. It selectively increases firing rates and affects tuning properties, including changing receptive field locations and sizes. Although these effects are well studied, their cellular mechanisms are poorly understood. To study the cellular mechanisms, we combined iontophoretic pharmacological analysis of cholinergic receptors with single cell recordings in V1 while rhesus macaque monkeys (Macaca mulatta) performed a task that demanded top-down spatial attention. Attending to the receptive field of the V1 neuron under study caused an increase in firing rates. Here we show that this attentional modulation was enhanced by low doses of acetylcholine. Furthermore, applying the muscarinic antagonist scopolamine reduced attentional modulation, whereas the nicotinic antagonist mecamylamine had no systematic effect. These results demonstrate that muscarinic cholinergic mechanisms play a central part in mediating the effects of attention in V1.

Modulation of sensory areas is assumed to be driven by the frontal and parietal cortex through direct cortico–cortical feedback connections. However, frontal regions also influence sensory areas indirectly, through connections to cholinergic neurons in the basal forebrain that have ascending projections to sensory areas, and there is ample evidence for the involvement of acetylcholine (ACh) in attentional modulation.

We recorded the strength of attentional modulation in neurons from V1 of three macaque monkeys, while simultaneously performing pharmacological analysis of cholinergic receptor contributions. Subjects performed a task demanding voluntary allocation of attention under control conditions and when ACh, or muscarinic or nicotinic receptor antagonists, were iontophoretically applied in the vicinity of the neurons under study.


Science 1 May 2009: Vol. 324. no. 5927, pp. 643 - 646

Burst Spiking of a Single Cortical Neuron Modifies Global Brain State

Cheng-yu T. Li, Mu-ming Poo, Yang Dan

1 Division of Neurobiology, Department of Molecular and Cell Biology, Helen Wills Institute of Neuroscience, University of California, Berkeley, CA 94720, USA.
2 Howard Hughes Medical Institute, University of California, Berkeley, CA 94720, USA.

Different global patterns of brain activity are associated with distinct arousal and behavioral states of an animal, but how the brain rapidly switches between different states remains unclear. We here report that repetitive high-frequency burst spiking of a single rat cortical neuron could trigger a switch between the cortical states resembling slow-wave and rapid–eye-movement sleep. This is reflected in the switching of the membrane potential of the stimulated neuron from slow UP/DOWN oscillations to a persistent-UP state or vice versa, with concurrent changes in the temporal pattern of cortical local field potential (LFP) recorded several millimeters away. These results point to the power of single cortical neurons in modulating the behavioral state of an animal.


Science 13 February 2009: Vol. 323. no. 5916, pp. 940 - 943

A Neural Mechanism for Microsaccade Generation in the Primate Superior Colliculus

Ziad M. Hafed,1 Laurent Goffart,2 Richard J. Krauzlis1

1 Systems Neurobiology Laboratory, Salk Institute for Biological Studies, 10010 North Torrey Pines Road, La Jolla, CA 92037, USA.
2 Institut de Neurosciences Cognitives de la Méditerranée, Equipe Dynamique de la Perception Visuelle et de l'Action, UMR 6193, CNRS–Aix-Marseille Universités, 13402 Marseille, France.

During fixation, the eyes are not still but often exhibit microsaccadic movements. The function of microsaccades is controversial, largely because the neural mechanisms responsible for their generation are unknown. Here, we show that the superior colliculus (SC), a retinotopically organized structure involved in voluntary-saccade target selection, plays a causal role in microsaccade generation. Neurons in the foveal portion of the SC increase their activity before and during microsaccades with sizes of only a few minutes of arc and exhibit selectivity for the direction and amplitude of these movements. Reversible inactivation of these neurons significantly reduces microsaccade rate without otherwise compromising fixation. These results, coupled with computational modeling of SC activity, demonstrate that microsaccades are controlled by the SC and explain the link between microsaccades and visual attention.

Microsaccades are the very small (typically <12 min arc), involuntary, fast eye movements that occur during fixation. The behavioral properties and functional role of microsaccades have been extensively studied, and sometimes vigorously debated, for many years. However, the neural mechanisms responsible for their generation are unexplored. We show that the superior colliculus (SC), a retinotopically organized structure known to be important for selecting and initiating voluntary eye movements, is also part of the neural mechanism that controls microsaccades.