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Cortical microstimulation influences perceptual judgements of motion direction
Abstract
Neurons in the visual cortex respond selectively to perceptually salient features of the visual scene, such as the direction and speed of moving objects, the orientation of local contours, or the colour or relative depth of a visual pattern. It is commonly assumed that the brain constructs its percept of the visual scene from information encoded in the selective responses of such neurons. We have now tested this hypothesis directly by measuring the effect on psychophysical performance of modifying the firing rates of physiologically characterized neurons. We required rhesus monkeys to report the direction of motion in a visual display while we electrically stimulated clusters of directionally selective neurons in the middle temporal visual area (MT, or V5), an extrastriate area that plays a prominent role in the analysis of visual motion information. Microstimulation biased the animals' judgements towards the direction of motion encoded by the stimulated neurons. This result indicates that physiological properties measured at the neuronal level can be causally related to a specific aspect of perceptual performance.
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“A combination of recording, lesion, and stimulation studies has established that neurons in extrastriate cortex (areas MT and MST) carry critical sensory information about motion direction (Newsome and Pare, 1988;Salzman et al., 1990;1992;Britten et al., 1992;Celebrini and Newsome, 1994;1995).”
From Response of Neurons in the Lateral Intraparietal Area during a Combined Visual Discrimination Reaction Time Task (2002) · cites this paper as Salzman et al., 1990
In the citing paper
“Neurons in extrastriate visual cortex (areas MT and MST) furnish the”
From Response of Neurons in the Lateral Intraparietal Area during a Combined Visual Discrimination Reaction Time Task (2002) · cites this paper as Salzman et al., 1990
In the citing paper
“Thus, MT provides at least some of the motion information used to form the direction decision.”
From Neural correlates of perceptual learning in a sensory-motor, but not a sensory, cortical area (2008) · cites this paper as [19]
In the citing paper
“the established role of MT in task performance16–19”
From Neural correlates of perceptual learning in a sensory-motor, but not a sensory, cortical area (2008) · cites this paper as [19]
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Neural events and perceptual awareness
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“Salzman, Britten, and Newsome (1990) showed that when a monkey performs a motion direction discrimination task, its response can be biased by microstimulation of a small region within cortical area MT where cells respond preferentially to a given direction of motion.”
BackgroundTransneuronal circuit tracing with neurotropic viruses
Callaway, E. M. (2008) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2009.03.007 · Cited by 252
“com areas are inferred and tested with lesions or electrical stimulation [2] [3].”
Zaksas, D., & Pasternak, T. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.3420-06.2006 · Cited by 252
“, 1985), and their activity has been linked closely to the perception of motion (Newsome et al., 1989; Salzman et al., 1990; Bisley et al., 2001).”
BackgroundMapping Cortical Activity Elicited with Electrical Microstimulation Using fMRI in the Macaque
Tolias, A. S., Sultan, F. R., Augath, M. A., Oeltermann, A., Tehovnik, E. J., Schiller, P. H., & Logothetis, N. K. (2005) · Neuron · doi:10.1016/j.neuron.2005.11.034 · Cited by 250
“Newsome and colleagues have shown that currents as low as 10 mA delivered in long trains (1 s) to a directionally selective column in MT/V5 biases a monkey’s motion perception (Salzman et al., 1990; Murasugi et al., 1993).”
BackgroundRoyer, S., Zemelman, B. V., Barbic, M., Losonczy, A., Buzsáki, G., & Magee, J. C. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07250.x · Cited by 247
“Microstimulation is an important tool for investigating the contribution of small groups of neurons to the network patterns (Salzman et al., 1990; Seidemann et al., 2002; Butovas & Schwarz, 2003; Cohen & Newsome, 2004; Butovas et al., 2006).”
MethodButovas, S., & Schwarz, C. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00245.2003 · Cited by 246
“Despite this insight, column-specific effects of microstimulation have been reported to exist on the behavioral level in monkey's primary somatosensory cortex (Romo et al. 2000) and visual area MT (Salzman et al. 1990; see for review Nichols and Newsome 2002 ).”
BackgroundMethodMapping human brain networks with cortico-cortical evoked potentials
Keller, C. J., Honey, C. J., Mégevand, P., Entz, L., Ulbert, I., & Mehta, A. D. (2014) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0528 · Cited by 257
“In experimental animals, Newsome and co-workers [39] were among the first to demonstrate how microstimulation of a specific cortical area could influence perceptual judgement.”
BackgroundComputational Maps in the Visual Cortex
Miikkulainen, R., Sirosh, J., Choe, Y., & Bednar, J. A. (2005) · Springer eBooks · doi:10.1007/0-387-28806-6 · Cited by 247
Ethological Action Maps: A Paradigm Shift for the Motor Cortex
Graziano, M. S. A. (2015) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2015.10.008 · Cited by 242
“This approach has a long history of use; for example, to study eye movements [17–20], perceptual decision making in visual and somatosensory cortex [21,22], and the control of motivated states such as hunger and sexual arousal in the hypothalamus [23–25].”
BackgroundYeatman, J. D., Rauschecker, A. M., & Wandell, B. A. (2012) · Brain and Language · doi:10.1016/j.bandl.2012.04.010 · Cited by 239
A model of self-motion estimation within primate extrastriate visual cortex
Perrone, J. A., & Stone, L. S. (1994) · Vision Research · doi:10.1016/0042-6989(94)90060-4 · Cited by 235
Cracking the Neural Code for Sensory Perception by Combining Statistics, Intervention, and Behavior
Panzeri, S., Harvey, C. D., Piasini, E., Latham, P. E., & Fellin, T. (2017) · Neuron · doi:10.1016/j.neuron.2016.12.036 · Cited by 240
“A classic example of this approach can be found in the work of Newsome and colleagues (Salzman et al., 1990) showing that MT microstimulation in a visual motion”
BackgroundResultNavigating the Neural Space in Search of the Neural Code
Jazayeri, M., & Afraz, A. (2017) · Neuron · doi:10.1016/j.neuron.2017.02.019 · Cited by 240
“For example, Salzman and Newsome exploited prior knowledge about the clustered nature of direction-tuning neurons in the MT area (Maunsell and Van Essen, 1983; Mikami et al., 1986) to establish a causal role for area MT in motion perception using electrical microstimulation (Salzman et al., 1990).”
MethodGroh, J. M., Born, R. T., & Newsome, W. T. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-11-04312.1997 · Cited by 228
“Is the readout mechanism task-dependent? Our results confirm that MT supplies motion signals to both the pursuit and saccadic target velocity compensation systems (Newsome et al., 1985; Komatsu and Wurtz, 1988; Schiller and Lee, 1994), and previous work from this laboratory has shown that MT provides motion signals fo…”
BackgroundResultSelf-citationBeckers, G., & Hömberg, V. (1992) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1992.0100 · Cited by 226
In-vivo Optical Imaging of Cortical Architecture and Dynamics
Grinvald, A., Shoham, D., Shmuel, A., Glaser, D. E., Vanzetta, I., Shtoyerman, E., Slovin, H., Wijnbergen, C., Hildesheim, R., & Arieli, A. (1999) · Springer eBooks · doi:10.1007/978-3-642-58552-4_34 · Cited by 222
Cohen, M. R., & Newsome, W. T. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.5179-08.2009 · Cited by 212
“…and Paré, 1988; Schiller, 1993; Schiller and Lee, 1994; Orban et al., 1995; Rudolph and Pasternak, 1999) or activation through microstimulation (Salzman et al., 1990; Salzman and Newsome, 1994; DeAngelis et al., 1998; Bisley et al., 2001; Nichols and Newsome, 2002; Ditterich et al., 2003;…”
Self-citationSpatiotopic temporal integration of visual motion across saccadic eye movements
Melcher, D., & Morrone, M. C. (2003) · Nature Neuroscience · doi:10.1038/nn1098 · Cited by 211
“Motion coherence sensitivity thresholds are correlated with the response of single MT/MST neurons in monkey”
BackgroundCorrelation between Speed Perception and Neural Activity in the Middle Temporal Visual Area
Liu, J., & Newsome, W. T. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.4034-04.2005 · Cited by 205
Self-citationThe Basal Ganglia’s Contributions to Perceptual Decision Making
Ding, L., & Gold, J. I. (2013) · Neuron · doi:10.1016/j.neuron.2013.07.042 · Cited by 208
Effects of cortical microstimulation on confidence in a perceptual decision
Fetsch, C. R., Kiani, R., Newsome, W. T., & Shadlen, M. N. (2014) · Neuron · doi:10.1016/j.neuron.2014.07.011 · Cited by 185
“Previous studies showed that mS of direction-selective neurons in the macaque visual cortex during a direction discrimination task causes monkeys to choose the preferred direction of neurons near the electrode tip more often (Salzman et al., 1990, 1992) and more rapidly (Ditterich et al., 2003).”
BackgroundResultSelf-citationWarden, M. R., Cardin, J. A., & Deisseroth, K. A. (2014) · Annual Review of Biomedical Engineering · doi:10.1146/annurev-bioeng-071813-104733 · Cited by 197
Generating Spike Trains with Specified Correlation Coefficients
Macke, J. H., Berens, P., Ecker, A. S., Tolias, A. S., & Bethge, M. (2008) · Neural Computation · doi:10.1162/neco.2008.02-08-713 · Cited by 190
“These techniques allow the direct manipulation of neural population activity in various brain areas (e.g., Salzman, Britten, & Newsome, 1990).”
Metadata
- Authors
- Salzman, C. D., Britten, K. H., & Newsome, W. T.
- Affiliations
- Stanford Medicine (US)
- Venue
- Nature
- Published
- 1990-07-12
- Volume
- 346
- Issue
- 6280
- Pages
- 174-177
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2037781104
- Cited by
- 881
- References
- 17
- Citations by year
- 2026: 20 · 2025: 21 · 2024: 25 · 2023: 24 · 2022: 27 · 2021: 24 · 2020: 46 · 2019: 33 · 2018: 29 · 2017: 26 · 2016: 25 · 2015: 37 · 2014: 31 · 2013: 31 · 2012: 23
- FWCI
- 19.44
- Type
- journal article
- Language
- en
- Update notices
- erratum (1990-08-09)
- Open access
- closed
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Multisensory perception and integration
- Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
- Keywords
- motion direction perception, directionally selective neurons, middle temporal area, V5, visual motion processing, neuronal firing rate, perceptual judgment, rhesus monkeys, visual cortex
- MeSH terms
- Animals, Electric Stimulation, Eye Movements, Macaca mulatta, Motion Perception, Visual Cortex, Visual Pathways, Visual Perception
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