How hallucinations may arise from brain mechanisms of learning, attention, and volition
- PMID: 10932478
- DOI: 10.1017/s135561770065508x
How hallucinations may arise from brain mechanisms of learning, attention, and volition
Abstract
This article suggests how brain mechanisms of learning, attention, and volition may give rise to hallucinations during schizophrenia and other mental disorders. The article suggests that normal learning and memory are stabilized through the use of learned top-down expectations. These expectations learn prototypes that are capable of focusing attention upon the combinations of features that comprise conscious perceptual experiences. When top-down expectations are active in a priming situation, they can modulate or sensitize their target cells to respond more effectively to matched bottom-up information. They cannot, however, fully activate these target cells. These matching properties are shown to be essential towards stabilizing the memory of learned representations. The modulatory property of top-down expectations is achieved through a balance between top-down excitation and inhibition. The learned prototype is the excitatory on-center in this top-down network. Phasic volitional signals can shift the balance between excitation and inhibition to favor net excitatory activation. Such a volitionally mediated shift enables top-down expectations, in the absence of supportive bottom-up inputs, to cause conscious experiences of imagery and inner speech and thereby to enable fantasy and planning activities to occur. If these volitional signals become tonically hyperactive during a mental disorder, the top-down expectations can give rise to conscious experiences in the absence of bottom-up inputs and volition. These events are compared with data about hallucinations. The article predicts where these top-down expectations and volitional signals may act in the laminar circuits of visual cortex and, by extension, in other sensory and cognitive neocortical areas, and how the level of abstractness of learned prototypes may covary with the abstractness of hallucinatory content. A similar breakdown of volition may lead to delusions of control in the motor system.
Similar articles
-
The link between brain learning, attention, and consciousness.Conscious Cogn. 1999 Mar;8(1):1-44. doi: 10.1006/ccog.1998.0372. Conscious Cogn. 1999. PMID: 10072692 Review.
-
Towards a functional neuroanatomy of conscious perception and its modulation by volition: implications of human auditory neuroimaging studies.Philos Trans R Soc Lond B Biol Sci. 1998 Nov 29;353(1377):1883-8. doi: 10.1098/rstb.1998.0340. Philos Trans R Soc Lond B Biol Sci. 1998. PMID: 9854260 Free PMC article. Review.
-
From brain synapses to systems for learning and memory: Object recognition, spatial navigation, timed conditioning, and movement control.Brain Res. 2015 Sep 24;1621:270-93. doi: 10.1016/j.brainres.2014.11.018. Epub 2014 Nov 20. Brain Res. 2015. PMID: 25446436 Review.
-
"Hearing voices": auditory hallucinations as failure of top-down control of bottom-up perceptual processes.Scand J Psychol. 2009 Dec;50(6):553-60. doi: 10.1111/j.1467-9450.2009.00775.x. Scand J Psychol. 2009. PMID: 19930254 Review.
-
Visual Priming and Visual Hallucinations in Parkinson's Disease. Evidence for Normal Top-Down Processes.J Geriatr Psychiatry Neurol. 2016 Jan;29(1):25-30. doi: 10.1177/0891988715598237. Epub 2015 Jul 30. J Geriatr Psychiatry Neurol. 2016. PMID: 26232406
Cited by 33 articles
-
Hallucinations as intensified forms of mind-wandering.Philos Trans R Soc Lond B Biol Sci. 2021 Feb;376(1817):20190700. doi: 10.1098/rstb.2019.0700. Epub 2020 Dec 14. Philos Trans R Soc Lond B Biol Sci. 2021. PMID: 33308066
-
Flowers in the Attic: Lateralization of the detection of meaning in visual noise.J Vis. 2020 Oct 1;20(10):11. doi: 10.1167/jov.20.10.11. J Vis. 2020. PMID: 33027510 Free PMC article.
-
Abnormal dynamic resting-state brain network organization in auditory verbal hallucination.Brain Struct Funct. 2020 Nov;225(8):2315-2330. doi: 10.1007/s00429-020-02119-1. Epub 2020 Aug 19. Brain Struct Funct. 2020. PMID: 32813156 Free PMC article.
-
A Hallucinogenic Serotonin-2A Receptor Agonist Reduces Visual Response Gain and Alters Temporal Dynamics in Mouse V1.Cell Rep. 2019 Mar 26;26(13):3475-3483.e4. doi: 10.1016/j.celrep.2019.02.104. Cell Rep. 2019. PMID: 30917304 Free PMC article.
-
Auditory hallucinations, top-down processing and language perception: a general population study.Psychol Med. 2019 Dec;49(16):2772-2780. doi: 10.1017/S003329171800380X. Epub 2019 Jan 4. Psychol Med. 2019. PMID: 30606279 Free PMC article.