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Evaluating the Operations Underlying Multisensory Integration in the Cat Superior Colliculus
Open accessAbstract
It is well established that superior colliculus (SC) multisensory neurons integrate cues from different senses; however, the mechanisms responsible for producing multisensory responses are poorly understood. Previous studies have shown that spatially congruent cues from different modalities (e.g., auditory and visual) yield enhanced responses and that the greatest relative enhancements occur for combinations of the least effective modality-specific stimuli. Although these phenomena are well documented, little is known about the mechanisms that underlie them, because no study has systematically examined the operation that multisensory neurons perform on their modality-specific inputs. The goal of this study was to evaluate the computations that multisensory neurons perform in combining the influences of stimuli from two modalities. The extracellular activities of single neurons in the SC of the cat were recorded in response to visual, auditory, and bimodal visual-auditory stimulation. Each neuron was tested across a range of stimulus intensities and multisensory responses evaluated against the null hypothesis of simple summation of unisensory influences. We found that the multisensory response could be superadditive, additive, or subadditive but that the computation was strongly dictated by the efficacies of the modality-specific stimulus components. Superadditivity was most common within a restricted range of near-threshold stimulus efficacies, whereas for the majority of stimuli, response magnitudes were consistent with the linear summation of modality-specific influences. In addition to providing a constraint for developing models of multisensory integration, the relationship between response mode and stimulus efficacy emphasizes the importance of considering stimulus parameters when inducing or interpreting multisensory phenomena.
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“Moreover, deviations from optimal integration have been observed in tasks with time constraints or novel stimuli (Arnold et al. 2019; Stanford et al. 2005), suggesting that the Bayesian fit may reflect task-specific tuning rather than a general cognitive strategy.”
From The myth of the Bayesian brain (2025) · cites this paper as Stanford et al. 2005
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Cites
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Interactions Among Converging Sensory Inputs in the Superior Colliculus
Meredith, M. A., & Stein, B. E. (1983) · Science · doi:10.1126/science.6867718 · Cited by 850
Self-citationSparks, D. L. (1986) · Physiological Reviews · doi:10.1152/physrev.1986.66.1.118 · Cited by 824
Determinants of multisensory integration in superior colliculus neurons. I. Temporal factors
Meredith, M. A., Nemitz, J. W., & Stein, B. (1987) · Journal of Neuroscience · doi:10.1523/jneurosci.07-10-03215.1987 · Cited by 763
Self-citationStein, B. E., Meredith, M. A., Huneycutt, W. S., & McDade, L. (1989) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.1989.1.1.12 · Cited by 416
Self-citationKing, A. J., & Palmer, A. R. (1985) · Experimental Brain Research · doi:10.1007/bf00236934 · Cited by 355
Wallace, M. T., Meredith, M. A., & Stein, B. E. (1993) · Journal of Neurophysiology · doi:10.1152/jn.1993.69.6.1797 · Cited by 261
Self-citationNeurons and behavior: the same rules of multisensory integration apply
Stein, B. E., Huneycutt, W. S., & Meredith, M. A. (1988) · Brain Research · doi:10.1016/0006-8993(88)91276-0 · Cited by 251
Self-citationTwo Cortical Areas Mediate Multisensory Integration in Superior Colliculus Neurons
Jiang, W., Wallace, M. T., Jiang, H., Vaughan, J. W., & Stein, B. E. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.85.2.506 · Cited by 205
Self-citationThe role of anterior ectosylvian cortex in cross-modality orientation and approach behavior
Wilkinson, L. K., Meredith, M. A., & Stein, B. E. (1996) · Experimental Brain Research · doi:10.1007/bf00227172 · Cited by 163
Self-citationCross-modal synthesis in the midbrain depends on input from cortex
Wallace, M. T., & Stein, B. E. (1994) · Journal of Neurophysiology · doi:10.1152/jn.1994.71.1.429 · Cited by 163
Self-citationMechanisms of Within- and Cross-Modality Suppression in the Superior Colliculus
Kadunce, D. C., Vaughan, J. W., Wallace, M. T., Benedek, G., & Stein, B. E. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.78.6.2834 · Cited by 149
Self-citationMeredith, M. A., & Clemo, H. R. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902890412 · Cited by 143
Two Corticotectal Areas Facilitate Multisensory Orientation Behavior
Jiang, W., Jiang, H., & Stein, B. E. (2002) · Journal of Cognitive Neuroscience · doi:10.1162/089892902760807230 · Cited by 142
Self-citationBimodal Interactions in the Superior Colliculus of the Behaving Cat
Populin, L. C., & Yin, T. C. T. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-07-02826.2002 · Cited by 105
Corticotectal and corticothalamic efferent projections of SIV somatosensory cortex in cat
Stein, B. E., Spencer, R. F., & Edwards, S. B. (1983) · Journal of Neurophysiology · doi:10.1152/jn.1983.50.4.896 · Cited by 98
Self-citationBook Review: Cortex Governs Multisensory Integration in the Midbrain
Stein, B. E., Wallace, M. W., Stanford, T. R., & Jiang, W. (2002) · The Neuroscientist · doi:10.1177/107385840200800406 · Cited by 74
Self-citationChapter 1 Neural mechanisms of visual orienting responses
Sprague, J. M. (1996) · Progress in brain research · doi:10.1016/s0079-6123(08)63317-8 · Cited by 56
Multisensory Integration in Single Neurons of the Midbrain
Stein, B. E., Jiang, W., & Stanford, T. R. (2004) · The MIT Press eBooks · doi:10.7551/mitpress/3422.003.0020 · Cited by 35
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Research works printed but not linked: 2
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- 2000, Soc Neurosci Abstr, 26, 455
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Multisensory integration: current issues from the perspective of the single neuron
Stein, B. E., & Stanford, T. R. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2331 · Cited by 1,598
Self-citationBayesian inference with probabilistic population codes
Ma, W. J., Beck, J. M., Latham, P. E., & Pouget, A. (2006) · Nature Neuroscience · doi:10.1038/nn1790 · Cited by 1,457
Neural correlates of multisensory cue integration in macaque MSTd
Gu, Y., Angelaki, D. E., & DeAngelis, G. C. (2008) · Nature Neuroscience · doi:10.1038/nn.2191 · Cited by 554
Visual Modulation of Neurons in Auditory Cortex
Kayser, C., Petkov, C. I., & Logothetis, N. K. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhm187 · Cited by 528
Development of multisensory integration from the perspective of the individual neuron
Stein, B. E., Stanford, T. R., & Rowland, B. A. (2014) · Nature reviews. Neuroscience · doi:10.1038/nrn3742 · Cited by 430
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Metadata
- Authors
- Stanford, T. R., Quessy, S., & Stein, B. E.
- Affiliations
- Wake Forest University Health Sciences (US)
- University of Rochester Medicine (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2005-07-13
- Volume
- 25
- Issue
- 28
- Pages
- 6499-6508
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC1237124
- OpenAlex
- W2038735682
- Cited by
- 314
- References
- 19
- Citations by year
- 2026: 6 · 2025: 19 · 2024: 22 · 2023: 12 · 2022: 7 · 2021: 12 · 2020: 13 · 2019: 15 · 2018: 11 · 2017: 14 · 2016: 14 · 2015: 15 · 2014: 14 · 2013: 12 · 2012: 12
- FWCI
- 23.32
- 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)
- Funders
- National Institutes of Health (NS36916)
- National Institute of Neurological Disorders and Stroke (NS 36916, NS22543, R01NS036916, R01NS022543)
- Topics
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Multisensory perception and integration
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- multisensory integration, superior colliculus, cats, superadditivity, linear summation, single-unit recording, multisensory neurons, audiovisual integration
- MeSH terms
- Acoustic Stimulation, Action Potentials, Animals, Auditory Perception, Brain Mapping, Cats, Models, Neurological, Neurons, Photic Stimulation, Reaction Time, Sensation, Superior Colliculi, Visual Perception
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