Stimulus-dependent synchronization of neuronal responses in the visual cortex of the awake macaque monkey
Open accessAbstract
In visual areas of the cerebral cortex, most neurons exhibit preferences for particular features of visual stimuli, but in general, the tuning is broad. Thus, even simple stimuli evoke responses in numerous neurons with differing but overlapping feature preferences, and it is commonly held that a particular feature is encoded in the pattern of graded responses of the activated population rather than in the optimal responses of individual cells. To decipher this population code, responses evoked by a particular stimulus need to be identified and bound together for further joint processing and must not be confounded with responses to other, nearby stimuli. Such selection of related responses could be achieved by synchronizing the respective discharges at a time scale of milliseconds, as this would selectively and jointly enhance their saliency. This hypothesis predicts that a given set of neurons should exhibit synchronized discharges more often when responding to a single stimulus than when activated by different but simultaneously presented stimuli. To test this prediction, recordings were performed with two electrodes from spatially segregated cells in the middle temporal area (MT) of the awake behaving macaque monkey. It was found that cells with overlapping receptive fields, but different preferences for directions of motion, can engage in synchronous activity if they are stimulated with a single moving bar. In contrast, if the same cells are activated with two different bars, each moving in the direction preferred by the cells at the two respective sites, responses show no or much fewer synchronous epochs. Control experiments exclude that this effect is attributable to changes in response amplitude, the mere presence of two stimuli, or the specific orientation of the bars. The critical variable determining the strength of correlation is the extent to which both sites are activated by a common stimulus or by two different stimuli with different directions of motion.
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Neurons processing visual information fire asynchronously when an animal does not attend to a stimulus, but fire synchronously when the animal attends to and is presumed conscious of the stimulus.
“work conducted by Wolf Singer and colleagues demonstrated that neurones processing visual information fired asynchronously when an animal does not attend to the stimulus, but fired synchronously when the animal attends to, and is presumed to be conscious of, the stimulus (Kreiter and Singer, 1996).”
From Consciousness: Matter or EMF? (2023) · cites this paper as Kreiter and Singer, 1996
The Results and Discussion report greater synchrony when recorded neurons responded to one moving bar than when they responded to two different bars. Materials and Methods describes a fixation task, not a comparison of attended and unattended stimuli. The paper does not establish the claimed link between synchrony, attention, and presumed consciousness. (LLM, conf=0.88)
Experimental — accuracy not yet measuredNeurons in the monkey brain fire synchronously when the animal attends to the stimulus.
“Work conducted by Wolf Singer and colleagues in the 1990s demonstrated that neurons in the monkey brain fire synchronously when the animal attends to the stimulus [14], and additional studies confirmed and extended these findings [15].”
From The electromagnetic will (2021) · cites this paper as [14]
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Self-citationNeuronal gamma-band synchronization as a fundamental process in cortical computation
Fries, P. (2009) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.051508.135603 · Cited by 1,713 · see citing works
Spectral fingerprints of large-scale neuronal interactions
Siegel, M., Donner, T. H., & Engel, A. K. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3137 · Cited by 1,295 · see citing works
Temporal binding and the neural correlates of sensory awareness.
Engel, A. K., & Singer, W. (2001) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(00)01568-0 · Cited by 1,372 · see citing works
Self-citationTop-down influences on visual processing
Gilbert, C. D., & Li, W. (2013) · Nature Reviews Neuroscience · doi:10.1038/nrn3476 · Cited by 1,224 · see citing works
Transient induced gamma-band response in EEG as a manifestation of miniature saccades
Yuval-Greenberg, S., Tomer, O., Keren, A. S., Nelken, I., & Deouell, L. Y. (2008) · Neuron · doi:10.1016/j.neuron.2008.03.027 · Cited by 776 · see citing works
Neural synchrony in cortical networks: history, concept and current status
Uhlhaas, P. (2009) · Frontiers in Integrative Neuroscience · doi:10.3389/neuro.07.017.2009 · Cited by 758 · see citing works
Theta and gamma oscillations predict encoding and retrieval of declarative memory
Osipova, D., Takashima, A., Oostenveld, R., Fernández, G., Maris, E., & Jensen, O. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.1948-06.2006 · Cited by 671 · see citing works
Uhlhaas, P. J., Haenschel, C., Nikolic, D., & Singer, W. (2008) · Schizophrenia Bulletin · doi:10.1093/schbul/sbn062 · Cited by 629 · see citing works
Self-citationNeural synchrony and the development of cortical networks
Uhlhaas, P. J., Roux, F., Rodriguez, E., Rotarska-Jagiela, A., & Singer, W. (2010) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2009.12.002 · Cited by 532 · see citing works
Self-citationvon der Malsburg, C. (1999) · Neuron · doi:10.1016/s0896-6273(00)80825-9 · Cited by 501 · see citing works
Convergence of biological and psychological perspectives on cognitive coordination in schizophrenia
Phillips, W. A., & Silverstein, S. M. (2003) · Behavioral and Brain Sciences · doi:10.1017/s0140525x03000025 · Cited by 445 · see citing works
Temporal binding, binocular rivalry, and consciousness
Engel, A. K., Fries, P., König, P., Brecht, M., & Singer, W. (1999) · Consciousness and Cognition · doi:10.1006/ccog.1999.0389 · Cited by 379 · see citing works
Self-citationConsciousness and the Binding Problem
SINGER, W. (2001) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2001.tb05712.x · Cited by 367 · see citing works
Self-citationInteraction between neocortical and hippocampal networks via slow oscillations
Sirota, A., & Buzsáki, G. (2005) · Thalamus and Related Systems · doi:10.1017/s1472928807000258 · Cited by 270 · see citing works
TALLON-BAUDRY, C., KREITER, A., & BERTRAND, O. (1999) · Visual Neuroscience · doi:10.1017/s0952523899163065 · Cited by 281 · see citing works
Self-citationThe neurophysics of consciousness
John, E. R. (2002) · Brain Research Reviews · doi:10.1016/s0165-0173(02)00142-x · Cited by 262 · see citing works
Role of the temporal domain for response selection and perceptual binding
Engel, A. (1997) · Cerebral Cortex · doi:10.1093/cercor/7.6.571 · Cited by 237 · see citing works
A field theory of consciousness.
John, E. R. (2001) · Consciousness and Cognition · doi:10.1006/ccog.2001.0508 · Cited by 214 · see citing works
Top-Down Beta Enhances Bottom-Up Gamma
Richter, C. G., Thompson, W. H., Bosman, C. A., & Fries, P. (2017) · The Journal of Neuroscience · doi:10.1523/jneurosci.3771-16.2017 · Cited by 195 · see citing works
Integrating information in the brain's EM field: the cemi field theory of consciousness
McFadden, J. (2020) · Neuroscience of Consciousness · doi:10.1093/nc/niaa016 · Cited by 148 · see citing works
Spatiotemporal Interactions in Retinal Prosthesis Subjects
Horsager, A., Greenberg, R. J., & Fine, I. (2010) · Investigative Opthalmology & Visual Science · doi:10.1167/iovs.09-3746 · Cited by 95 · see citing works
Cortical layers, rhythms and BOLD signals
Scheeringa, R., & Fries, P. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2017.11.002 · Cited by 88 · see citing works
Ayzenshtat, I., Meirovithz, E., Edelman, H., Werner-Reiss, U., Bienenstock, E., Abeles, M., & Slovin, H. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.5177-09.2010 · Cited by 75 · see citing works
“Although the binding-by-synchrony model posits that the presence of dynamic synchrony or spatiotemporal patterns during visual processing should correlate positively with perceptual grouping (Kreiter and Singer, 1996), other models might actually predict a negative correlation.”
BackgroundMcFadden, J. (2023) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2022.1024934 · Cited by 27 · see citing works
“For example, work conducted by Wolf Singer and colleagues demonstrated that neurones processing visual information fired asynchronously when an animal does not attend to the stimulus, but fired synchronously when the animal attends to, and is presumed to be conscious of, the stimulus (Kreiter and Singer, 1996).”
BackgroundMcFadden, J. (2021) · NeuroSci · doi:10.3390/neurosci2030021 · Cited by 13 · see citing works
- Authors
- Kreiter, A., & Singer, W.
- Affiliations
- Max Planck Institute for Brain Research (DE)
- ORCID
- Singer, W
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 1996-04-01
- Volume
- 16
- Issue
- 7
- Pages
- 2381-2396
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6578521
- OpenAlex
- W2166037666
- Cited by
- 477
- References
- 113
- Citations by year
- 2026: 2 · 2025: 6 · 2024: 8 · 2023: 3 · 2022: 6 · 2021: 7 · 2020: 13 · 2019: 10 · 2018: 8 · 2017: 16 · 2016: 8 · 2015: 16 · 2014: 6 · 2013: 17 · 2012: 18
- FWCI
- 16.77
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Multisensory perception and integration
- Keywords
- neuronal synchronization, population coding, middle temporal area, MT, direction selectivity, receptive fields, stimulus selectivity, visual cortex, macaque
- MeSH terms
- Action Potentials, Animals, Consciousness, Electrophysiology, Eye Movements, Macaca fascicularis, Male, Neurons, Photic Stimulation, Visual Cortex
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