Literature DB >> 30183470

Superior colliculus signals decisions rather than confidence: analysis of single neurons.

Piercesare Grimaldi1,2,3,4,5, Seong Hah Cho6,5,7, Hakwan Lau4,8,7, Michele A Basso1,2,9,3,4,5.   

Abstract

Recent findings indicate that monkeys can report their confidence in perceptual decisions and that this information is encoded in neurons involved in making decisions, including the lateral intraparietal area (LIP) and the supplementary eye field (SEF). A key issue to consider when studying confidence is that decision accuracy often correlates with confidence reports; when we are performing well, we generally feel more confident. Expanding on work performed in humans, we designed a novel task for monkeys that dissociates perceptual information leading to decisions from perceptual information leading to confidence reports. Using this task, we recently showed that decoded ensemble activity recorded from the superior colliculus (SC) reflected decisions rather than confidence reports. However, our previous population level analysis collapsed over multiple SC neuronal types and therefore left open the possibility that first, individual discharge rates might encode information related to decision confidence, and second, different neuronal cell types within the SC might signal decision confidence independently of decision accuracy. We found that when decision accuracy and decision confidence covaried, modulation occurred primarily in neurons with prelude activity (buildup neurons). However, isolating decision confidence from decision accuracy uncovered that only a few, primarily buildup neurons showed signals correlating uniquely with decision confidence and the effect sizes were very small. Based on this work and our previous work using decoding methods, we conclude that neuronal signals for decision confidence, independent of decision accuracy, are unlikely to exist at the level of single or populations of neurons in the SC. Our results together with other recent work call into question normative models of confidence based on the optimal readout of decision signals. NEW & NOTEWORTHY Models of decision confidence suggest that our sense of confidence is an optimal readout of perceptual decision signals. Here, we report that a subcortical area, the superior colliculus (SC), contains neurons with activity that signal decisions and confidence in a task in which decision accuracy and confidence covary, similar to area lateral intraparietal area in cortex. The signals from SC occur primarily in the neurons with prelude activity (buildup neurons). However, in a task that dissociates decision accuracy from decision confidence, we find that only a few individual neurons express unique signals of confidence. These results call into question normative models of confidence based on optimal readout of perceptual decision signals.

Entities:  

Keywords:  confidence; electrophysiology; metacognition; superior colliculus

Mesh:

Year:  2018        PMID: 30183470      PMCID: PMC6295535          DOI: 10.1152/jn.00152.2018

Source DB:  PubMed          Journal:  J Neurophysiol        ISSN: 0022-3077            Impact factor:   2.714


  35 in total

1.  Separate signals for target selection and movement specification in the superior colliculus.

Authors:  G D Horwitz; W T Newsome
Journal:  Science       Date:  1999-05-14       Impact factor: 47.728

2.  A role for neural integrators in perceptual decision making.

Authors:  Mark E Mazurek; Jamie D Roitman; Jochen Ditterich; Michael N Shadlen
Journal:  Cereb Cortex       Date:  2003-11       Impact factor: 5.357

3.  Saccade target selection in the superior colliculus: a signal detection theory approach.

Authors:  Byounghoon Kim; Michele A Basso
Journal:  J Neurosci       Date:  2008-03-19       Impact factor: 6.167

4.  Confidence and certainty: distinct probabilistic quantities for different goals.

Authors:  Alexandre Pouget; Jan Drugowitsch; Adam Kepecs
Journal:  Nat Neurosci       Date:  2016-03       Impact factor: 24.884

5.  Does perceptual confidence facilitate cognitive control?

Authors:  Ai Koizumi; Brian Maniscalco; Hakwan Lau
Journal:  Atten Percept Psychophys       Date:  2015-05       Impact factor: 2.199

6.  Superior colliculus neuronal ensemble activity signals optimal rather than subjective confidence.

Authors:  Brian Odegaard; Piercesare Grimaldi; Seong Hah Cho; Megan A K Peters; Hakwan Lau; Michele A Basso
Journal:  Proc Natl Acad Sci U S A       Date:  2018-01-30       Impact factor: 11.205

7.  Neural basis of a perceptual decision in the parietal cortex (area LIP) of the rhesus monkey.

Authors:  M N Shadlen; W T Newsome
Journal:  J Neurophysiol       Date:  2001-10       Impact factor: 2.714

8.  Neuronal correlates of metacognition in primate frontal cortex.

Authors:  Paul G Middlebrooks; Marc A Sommer
Journal:  Neuron       Date:  2012-08-09       Impact factor: 17.173

9.  Representation of confidence associated with a decision by neurons in the parietal cortex.

Authors:  Roozbeh Kiani; Michael N Shadlen
Journal:  Science       Date:  2009-05-08       Impact factor: 47.728

10.  Multivoxel neurofeedback selectively modulates confidence without changing perceptual performance.

Authors:  Aurelio Cortese; Kaoru Amano; Ai Koizumi; Mitsuo Kawato; Hakwan Lau
Journal:  Nat Commun       Date:  2016-12-15       Impact factor: 14.919

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  8 in total

Review 1.  Using rAAV2-retro in rhesus macaques: Promise and caveats for circuit manipulation.

Authors:  Adriana K Cushnie; Hala G El-Nahal; Martin O Bohlen; Paul J May; Michele A Basso; Piercesare Grimaldi; Maya Zhe Wang; Marron Fernandez de Velasco Ezequiel; Marc A Sommer; Sarah R Heilbronner
Journal:  J Neurosci Methods       Date:  2020-07-12       Impact factor: 2.390

2.  Variable Statistical Structure of Neuronal Spike Trains in Monkey Superior Colliculus.

Authors:  Seong-Hah Cho; Trinity Crapse; Piercesare Grimaldi; Hakwan Lau; Michele A Basso
Journal:  J Neurosci       Date:  2021-02-23       Impact factor: 6.167

3.  Behavior- and Modality-General Representation of Confidence in Orbitofrontal Cortex.

Authors:  Paul Masset; Torben Ott; Armin Lak; Junya Hirokawa; Adam Kepecs
Journal:  Cell       Date:  2020-06-05       Impact factor: 41.582

4.  Adeno-Associated Virus Capsid-Promoter Interactions in the Brain Translate from Rat to the Nonhuman Primate.

Authors:  Martin O Bohlen; Thomas J McCown; Sara K Powell; Hala G El-Nahal; Tierney Daw; Michele A Basso; Marc A Sommer; R Jude Samulski
Journal:  Hum Gene Ther       Date:  2020-10-22       Impact factor: 5.695

5.  Alcohol use severity and the neural correlates of the effects of sleep disturbance on sustained visual attention.

Authors:  Guangfei Li; Yu Chen; Xiaoying Tang; Chiang-Shan R Li
Journal:  J Psychiatr Res       Date:  2021-08-16       Impact factor: 5.250

6.  Sensory and decisional components of endogenous attention are dissociable.

Authors:  Sanjna Banerjee; Shrey Grover; Suhas Ganesh; Devarajan Sridharan
Journal:  J Neurophysiol       Date:  2019-07-03       Impact factor: 2.714

7.  Subcortical connectivity correlates selectively with attention's effects on spatial choice bias.

Authors:  Varsha Sreenivasan; Devarajan Sridharan
Journal:  Proc Natl Acad Sci U S A       Date:  2019-09-06       Impact factor: 11.205

8.  Contributions of anterior cingulate cortex and basolateral amygdala to decision confidence and learning under uncertainty.

Authors:  A Stolyarova; M Rakhshan; E E Hart; T J O'Dell; M A K Peters; H Lau; A Soltani; A Izquierdo
Journal:  Nat Commun       Date:  2019-10-17       Impact factor: 14.919

  8 in total

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