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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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“The random-dot motion task is useful for studying this process because (1) its solution requires integration of evidence across space and time and (2) a neural representation of the momentary evidence has been established in areas MT and MST (Salzman et al., 1990; Celebrini and Newsome, 1994; Ditterich et al., 2003).”
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“For example, global motion signals such as found in random-dot motion (RDM) stimuli are processed in higherorder visual cortices such as the middle temporal (MT) and the medial superior temporal (MST) areas (Newsome et al., 1989; Salzman et al., 1990; Britten et al., 1992; Celebrini and Newsome, 1994), and a lesion of…”
BackgroundPeeling the Onion of Brain Representations
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“Stimulation of these key regions can bias decisions depending on the area influenced (Salzman et al., 1990; Cohen and Newsome, 2004).”
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“Libet (1982) has also used brain stimulation to good effect, and more recently Newsome and colleagues (e.g. Salzman et al 1990) have used brain stimulation to draw some conclusions about neural correlates of motion perception in monkeys.”
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“…of a relatively small amount of neurons by electrical stimulation can bias the decisions of monkeys performing a visual direction discrimination task in favor of the preferred direction of the stimulated population (Salzman et al., 1990, 1992; Salzman & Newsome, 1994; Celebrini & Newsome, 1995).”
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“…as evoked neurotransmitter release (Katz 1969), the topographic organization of somatosensory and motor cortices (Penfield & Rasmussen 1950), decision making (Salzman et al. 1990, Salzman & Newsome 1994), and the specification of simple actions by cortical pyramidal cells (Brecht et al. 2004).”
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“…local circuit, thus resulting in a shift of the psychometric function toward the preferred heading of MU activity recorded at the stimulation site (Salzman et al., 1990, 1992; Murasugi et al., 1993; Celebrini and Newsome, 1995; Nichols and Newsome, 2002; Cohen and Newsome, 2004; Afraz et al.,…”
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“…the direction of random moving dots while a current was injected in area MT and MST. Consistently with previous findings (Ditterich et al., 2003; Salzman et al., 1990; Salzman et al., 1992), the authors found that the monkey was more likely to choose the preferred direction of stimulated…”
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“In principle, trial-bytrial shifts in MT responsiveness of particular subsets of MT neurons could affect choices in a manner analogous to the effects of electrical microstimulation, which biases choices in the preferred direction of the stimulated neurons (Salzman et al. 1990, 1992).”
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“…some studies combining readout with manipu- lation have made significant progress in this direction (Ceballo et al., 2019a; Ceballo et al., 2019b; Salzman et al., 1990; Znamenskiy and Zador, 2013), they have lacked spatial resolution and target- ing flexibility either on the level of readout…”
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“…or electrical microstimulation to perturb focal regions of the sensory representation and test for effects on behavior (Afraz et al., 2006; Celebrini and Newsome, 1995; Newsome and Pare, 1988; Nichols and Newsome, 2002; Romo et al., 1998; Salzman et al., 1990, 1992; Uka and DeAngelis, 2006).”
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“However, at this stage, there is no certainty that the electrical stimulation applied by Salzman et al. (1990) actually excited a particular group of neurons with measurable CPs.”
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“Electrical microstimulation has been used widely in nonhuman primates (NHPs) as a tool to probe perception (Salzman et al., 1990; Murphey and Maunsell, 2007), decision making (Cohen and Newsome, 2004; Moore and Fallah, 2004), motor control (Graziano et al., 2002), and network connectivity (Ekstrom…”
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“). Our results are therefore consistent with the hypothesis that area 1 comprises a population of neurons whose responses underlie our ability to perceive the direction of tactile motion. However, the neuronal and behavioral data were obtained from different species; this hypothesis could be tested in future experimen…”
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“Single-unit studies by Newsome and colleagues show a robust link between activity in macaque MT and motion perception (Newsome and Pare, 1988; Newsome et al., 1989; Salzman et al., 1990; Britten et al., 1996), even when the monkey is viewing an ambiguous stimulus (Britten et al.”
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“We therefore recorded from single neurons in the MT area, a cortical area known to be causally involved in sensory decisions about motion direction (26, 27).”
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“In those experiments, monkeys were trained to distinguish the mean direction of motion of a partially coherent random dot display [63–65].”
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“These values are three to five orders of magnitude below current levels typically used with extracellular stimulation (for review, see Ranck, 1975) (Gerken, 1984; Salzman et al., 1990; Cruikshank et al., 1992; Maldonado and Gerstein, 1992; Recanzone et al., 1992; Kitzes and Doherty, 1994), suggesting minimal effective…”
Millisecond-scale differences in neural activity in auditory cortex can drive decisions
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Making choices: the neurophysiology of visual-saccadic decision making
Glimcher, P. W. (2001) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01932-9 · Cited by 101
Interfacing the Somatosensory System to Restore Touch and Proprioception: Essential Considerations
Weber, D. J., Friesen, R., & Miller, L. E. (2012) · Journal of Motor Behavior · doi:10.1080/00222895.2012.735283 · Cited by 98
Velocity computation in the primate visual system
Bradley, D. C., & Goyal, M. S. (2008) · Nature reviews. Neuroscience · doi:10.1038/nrn2472 · Cited by 98
Hübener, M., & Bonhoeffer, T. (2010) · Neuron · doi:10.1016/j.neuron.2010.06.033 · Cited by 103
A system for neural recording and closed-loop intracortical microstimulation in awake rodents.
Venkatraman, S., Elkabany, K., Long, J. D., Yao, Y., & Carmena, J. M. (2009) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2008.2005944 · Cited by 96
The Speed and Accuracy of a Simple Perceptual Decision: A Mathematical Primer
Shadlen, M. N., Hanks, T. D., Churchland, A. K., Kiani, R., & Yang, T. (2006) · The MIT Press eBooks · doi:10.7551/mitpress/9780262042383.003.0010 · Cited by 95
“Indeed microstimulation of a cluster of rightward-preferring MT neurons causes the monkey to decide that motion is rightward more often [28] and to do so more quickly than when there is no stimulation [11].”
BackgroundNeural mechanisms of saccade target selection: gated accumulator model of the visual-motor cascade
Schall, J. D., Purcell, B. A., Heitz, R. P., Logan, G. D., & Palmeri, T. J. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07715.x · Cited by 94
“…Shadlen, 2002; Churchland et al., 2008), the effects of middle temporal area and LIP microstimulation on performance (Ditterich et al., 2003; Hanks et al., 2006; Salzman et al., 1990; Salzman et al., 1992), and the effects of motion pulse stimuli on behavior and LIP activity (Huk & Shadlen, 2005).”
BackgroundTargeted Cortical Manipulation of Auditory Perception
Ceballo, S., Piwkowska, Z., Bourg, J., Daret, A., & Bathellier, B. (2019) · Neuron · doi:10.1016/j.neuron.2019.09.043 · Cited by 100
Partial tuning of motor cortex neurons to final posture in a free-moving paradigm
Aflalo, T., & Graziano, M. S. A. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0511139103 · Cited by 95
Visual resolution with retinal implants estimated from recordings in cat visual cortex
Eckhorn, R., Wilms, M., Schanze, T., Eger, M., Hesse, L., Eysel, U. T., Kisvárday, Z. F., Zrenner, E., Gekeler, F., Schwahn, H., et al. (2006) · Vision Research · doi:10.1016/j.visres.2006.01.034 · Cited by 94
Global motion perception: No interaction between the first- and second-order motion pathways
Edwards, M., & Badcock, D. R. (1995) · Vision Research · doi:10.1016/0042-6989(95)00003-i · Cited by 93
Churchland, M. M., & Lisberger, S. G. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-23-09387.2001 · Cited by 92
“Recording and microstimulation studies also link MT with direction discrimination in monkeys (Newsome et al., 1989; Salzman et al., 1990; Britten et al., 1992, 1996; Shadlen et al., 1996).”
BackgroundA versatile all-channel stimulator for electrode arrays, with real-time control
Wagenaar, D. A., & Potter, S. M. (2004) · Journal of Neural Engineering · doi:10.1088/1741-2560/1/1/006 · Cited by 92
Rapid Integration of Artificial Sensory Feedback during Operant Conditioning of Motor Cortex Neurons
Prsa, M., Galiñanes, G. L., & Huber, D. (2017) · Neuron · doi:10.1016/j.neuron.2017.01.023 · Cited by 97
“Stimulation of sensory cortex can create behaviorally distinguishable percepts (Romo et al., 1998, 2000; Tabot et al., 2013); bias (Salzman et al., 1990), mimic (O’Connor et al., 2013; Sachidhanandam et al., 2013; Tabot et al., 2013), or even augment (Thomson et al., 2013) natural perception; and…”
Human smooth pursuit direction discrimination
Watamaniuk, S. N. J., & Heinen, S. J. (1999) · Vision Research · doi:10.1016/s0042-6989(98)00128-x · Cited by 92
Spiking Irregularity and Frequency Modulate the Behavioral Report of Single-Neuron Stimulation
Doron, G., von Heimendahl, M., Schlattmann, P., Houweling, A. R., & Brecht, M. (2014) · Neuron · doi:10.1016/j.neuron.2013.11.032 · Cited by 90
“Intracortical microstimulation was, until recently, the only method that enabled activation of localized populations of neurons and directly influencing sensory perception (Afraz et al., 2006; Romo et al., 1998; Salzman et al., 1990).”
Principles for models of neural information processing
Kay, K., & Weiner, K. S. (2017) · NeuroImage · doi:10.1016/j.neuroimage.2017.08.016 · Cited by 90
“…made in specific brain areas (Gallant et al., 2000), surgical removal of entire brain areas (Weiner et al., 2016b), the effects of enhancement (Salzman et al., 1990) or disruption (Pascual-Leone and Walsh, 2001) of neural activity, or the effects of psychoactive drugs (Rokem and Silver,…”
BackgroundAll-optical interrogation of neural circuits in behaving mice
Russell, L. E., Dalgleish, H. W. P., Nutbrown, R., Gauld, O. M., Herrmann, D., Fişek, M., Packer, A. M., & Häusser, M. (2022) · Nature Protocols · doi:10.1038/s41596-022-00691-w · Cited by 99
Visual Guidance of Smooth Pursuit Eye Movements
Lisberger, S. G. (2015) · Annual Review of Vision Science · doi:10.1146/annurev-vision-082114-035349 · Cited by 91
“In an experiment inspired by the demonstration that microstimulation in MT could alter a monkey’s reports of what he saw for a given visual stimulus (Salzman et al. 1990), we showed that stimulation in the FEFSEM could alter how the motor system responded to a given sensory stimulus (Tanaka &…”
Beutter, B. R., & Stone, L. S. (1998) · Vision Research · doi:10.1016/s0042-6989(97)00276-9 · Cited by 88
Handbook of Reward and Decision Making
Dreher, J., & Tremblay, L. (2009) · Elsevier eBooks · doi:10.1016/b978-0-12-374620-7.x0001-5 · Cited by 88
Comparison of Form and Motion Coherence Processing in Autistic Spectrum Disorders and Dyslexia
Tsermentseli, S. K., O'Brien, J. M. D., & Spencer, J. V. (2007) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-007-0500-3 · Cited by 91
“Removal or excision of V5 significantly reduces task performance on motion direction discrimination (Newsome and Pare 1988), and stimulation of V5 changes macaque’s choices in such tasks ( Salzman et al. 1990 ).”
BackgroundNeural Mechanisms of Tactile Motion Integration in Somatosensory Cortex
Pei, Y., Hsiao, S. S., Craig, J. C., & Bensmaı̈a, S. J. (2011) · Neuron · doi:10.1016/j.neuron.2010.12.033 · Cited by 83
Perceptual “Read-Out” of Conjoined Direction and Disparity Maps in Extrastriate Area MT
DeAngelis, G. C., & Newsome, W. T. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0020077 · Cited by 82
“and Disparity Maps in Extrastriate Area MT”
BackgroundSelf-citationPhosphene induction and the generation of saccadic eye movements by striate cortex
Tehovnik, E. J., Slocum, W. M., Carvey, C. E., & Schiller, P. H. (2005) · Journal of Neurophysiology · doi:10.1152/jn.00736.2004 · Cited by 87
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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