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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Neurons in extrastriate cortex (areas MT and MST) carry critical sensory information about motion direction.
“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
Neurons in extrastriate visual cortex (areas MT and MST) furnish information about the direction of motion that is critical to performance on this task.
“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
MT provides at least some of the motion information used to form the direction decision.
“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]
MT has an established role in task performance.
“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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“In a series of experiments Newsome and his colleagues (Newsome et al., 1989; Salzman et al., 1990) were able to demonstrate that area MT forms a topographic map of the visual world in which the strength of motion in the visual world is encoded by the rate at which each neuron in the map fires…”
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Demb, J. B., Boynton, G. M., & Heeger, D. J. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-17-06939.1998 · Cited by 284 · see citing works
“…between neural activity in MT1 and the perception of motion (Siegel and Andersen, 1986; Newsome and Pare, 1988; Logothetis and Schall, 1989; Newsome et al., 1989; Salzman et al., 1990, 1992; Britten et al., 1992; Celebrini and Newsome, 1994, 1995; Pasternak and Merigan, 1994; Orban et al., 1995).”
BackgroundA theory of visual stability across saccadic eye movements
Bridgeman, B., van der Heijden, A. H. C., & Velichkovsky, B. M. (1994) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00034361 · Cited by 286 · see citing works
Romo, R., Hernández, A., Zainos, A., Brody, C. D., & Lemus, L. (2000) · Neuron · doi:10.1016/s0896-6273(00)81156-3 · Cited by 270 · see citing works
“…consecutively to the glabrous (hairless) skin, separated by an inter-which occurred simultaneously with the current injection stimulus delay period of 1.5–3.5 s, and the animal was rewarded for (Salzman et al., 1990, 1992; Britten and Wezel, 1998; correct discriminations with a drop of liquid.”
BackgroundInfluentialNeuroscience: Breaking Down Scientific Barriers to the Study of Brain and Mind
Kandel, E. R., & Squire, L. R. (2000) · Science · doi:10.1126/science.290.5494.1113 · Cited by 270 · see citing works
Selective corticostriatal plasticity during acquisition of an auditory discrimination task
Xiong, Q., Znamenskiy, P., & Zador, A. M. (2015) · Nature · doi:10.1038/nature14225 · Cited by 250 · see citing works
Touch and Go: Decision-Making Mechanisms in Somatosensation
Romo, R., & Salinas, E. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.107 · Cited by 259 · see citing works
“Intracortical microstimulation can produce results that are much closer to such proof (Salzman et al 1990, 1992; Britten & van Wezel 1998; Romo et al 1998, 2000).”
BackgroundNeural coding during active somatosensation revealed using illusory touch
O'Connor, D. H., Hires, S. A., Guo, Z. V., Li, N., Yu, J., Sun, Q.-Q., Huber, D., & Svoboda, K. (2013) · Nature Neuroscience · doi:10.1038/nn.3419 · Cited by 252 · see citing works
Neural events and perceptual awareness
Kanwisher, N. (2001) · Cognition · doi:10.1016/s0010-0277(00)00125-6 · Cited by 253 · see citing works
“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 · see citing works
“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 247 · see citing works
“, 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 · see citing works
“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 · see citing works
“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 · see citing works
“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 244 · see citing works
“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 · see citing works
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 · see citing works
“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 · see citing works
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 · see citing works
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 227 · see citing works
“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 227 · see citing works
“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 · see citing works
“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 · see citing works
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 · see citing works
Cohen, M. R., & Newsome, W. T. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.5179-08.2009 · Cited by 214 · see citing works
“…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 · see citing works
“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 199 · see citing works
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 201 · see citing works
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 · see citing works
“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 188 · see citing works
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 185 · see citing works
“These techniques allow the direct manipulation of neural population activity in various brain areas (e.g., Salzman, Britten, & Newsome, 1990).”
- 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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