1932

Abstract

Visual processing is dynamically controlled by multiple neuromodulatory molecules that modify the responsiveness of neurons and the strength of the connections between them. In particular, modulatory control of processing in the lateral geniculate nucleus of the thalamus, V1, and V2 will alter the outcome of all subsequent processing of visual information, including the extent to and manner in which individual inputs contribute to perception and decision making and are stored in memory. This review addresses five small-molecule neuromodulators—acetylcholine, dopamine, serotonin, noradrenaline, and histamine—considering the structural basis for their action, and the effects of their release, in the early visual pathway of the macaque monkey. Traditionally, neuromodulators are studied in isolation and in discrete circuits; this review makes a case for considering the joint action of modulatory molecules and differences in modulatory effects across brain areas as a better means of understanding the diverse roles that these molecules serve.

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2021-09-15
2024-04-19
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Literature Cited

  1. Arnsten AF, Wang M, Paspalas CD. 2015. Dopamine's actions in primate prefrontal cortex: challenges for treating cognitive disorders. Pharmacol. Rev. 67:681–96
    [Google Scholar]
  2. Aston-Jones G, Cohen JD 2005. Adaptive gain and the role of the locus coeruleus-norepinephrine system in optimal performance. J. Comp. Neurol. 493:99–110
    [Google Scholar]
  3. Avendano C, Umbriaco D, Dykes RW, Descarries L. 1996. Acetylcholine innervation of sensory and motor neocortical areas in adult cat: a choline acetyltransferase immunohistochemical study. J. Chem. Neuroanat. 11:113–30
    [Google Scholar]
  4. Avery MC, Krichmar JL. 2017. Neuromodulatory systems and their interactions: a review of models, theories, and experiments. Front. Neural Circuits 11:108
    [Google Scholar]
  5. Azimi Z, Barzan R, Spoida K, Surdin T, Wollenweber P et al. 2020. Separable gain control of ongoing and evoked activity in the visual cortex by serotonergic input. eLife 9:e53552
    [Google Scholar]
  6. Balaram P, Young NA, Kaas JH. 2014. Histological features of layers and sublayers in cortical visual areas V1 and V2 of chimpanzees, macaque monkeys, and humans. Eye Brain 2014:5–18
    [Google Scholar]
  7. Bentley P, Driver J, Dolan RJ. 2011. Cholinergic modulation of cognition: insights from human pharmacological functional neuroimaging. Prog. Neurobiol. 94:360–88
    [Google Scholar]
  8. Berger B, Gaspar P, Verney C 1991. Dopaminergic innervation of the cerebral cortex: unexpected differences between rodents and primates. Trends Neurosci 14:21–27
    [Google Scholar]
  9. Berger B, Trottier S, Verney C, Gaspar P, Alvarez C 1988. Regional and laminar distribution of the dopamine and serotonin innervation in the macaque cerebral cortex: a radioautographic study. J. Comp. Neurol. 273:99–119
    [Google Scholar]
  10. Berke JD. 2018. What does dopamine mean?. Nat. Neurosci. 21:787–93
    [Google Scholar]
  11. Berridge CW, Arnsten AF. 2013. Psychostimulants and motivated behavior: arousal and cognition. Neurosci. Biobehav. Rev. 37:1976–84
    [Google Scholar]
  12. Berridge CW, Waterhouse BD. 2003. The locus coeruleus-noradrenergic system: modulation of behavioral state and state-dependent cognitive processes. Brain Res. Brain Res. Rev. 42:33–84
    [Google Scholar]
  13. Bowden DM, German DC, Poynter WD. 1978. An autoradiographic, semistereotaxic mapping of major projections from locus coeruleus and adjacent nuclei in Macaca mulatta. Brain Res 145:257–76
    [Google Scholar]
  14. Brzosko Z, Mierau SB, Paulsen O. 2019. Neuromodulation of spike-timing-dependent plasticity: past, present, and future. Neuron 103:563–81
    [Google Scholar]
  15. Byth W, McMahon D, King DJ. 2000. Cholinergic agents and the McCollough effect. Perception 29:461–80
    [Google Scholar]
  16. Callaway EM. 1998. Local circuits in primary visual cortex of the macaque monkey. Annu. Rev. Neurosci. 21:47–74
    [Google Scholar]
  17. Caton R. 1887. Researches on electrical phenomena of cerebral grey matter. Trans. Int. Med. Congr. 3:246–49
    [Google Scholar]
  18. Coppola JJ, Disney AA. 2018. Is there a canonical cortical circuit for the cholinergic system? Anatomical differences across common model systems. Front. Neural Circuits 12:8
    [Google Scholar]
  19. Coppola JJ, Ward NJ, Jadi MP, Disney AA. 2016. Modulatory compartments in cortex and local regulation of cholinergic tone. J. Physiol. Paris 110:3–9
    [Google Scholar]
  20. Dascal N. 2001. Ion-channel regulation by G proteins. Trends Endocrinol. Metab. 12:391–98
    [Google Scholar]
  21. Dayan P, Huys Q 2015. Serotonin's many meanings elude simple theories. eLife 4:e07390
    [Google Scholar]
  22. de Lima AD, Bloom FE, Morrison JH. 1988. Synaptic organization of serotonin-immunoreactive fibers in primary visual cortex of the macaque monkey. J. Comp. Neurol. 274:280–94
    [Google Scholar]
  23. Delmas P, Coste B, Gamper N, Shapiro MS. 2005. Phosphoinositide lipid second messengers: new paradigms for calcium channel modulation. Neuron 47:179–82
    [Google Scholar]
  24. Disney AA, Aoki C, Hawken MJ. 2007. Gain modulation by nicotine in macaque v1. Neuron 56:701–13
    [Google Scholar]
  25. Disney AA, Aoki C, Hawken MJ. 2012. Cholinergic suppression of visual responses in primate V1 is mediated by GABAergic inhibition. J. Neurophysiol. 108:1907–23
    [Google Scholar]
  26. Disney AA, Higley MJ. 2020. Diverse spatiotemporal scales of cholinergic signaling in the neocortex. J. Neurosci. 40:720–25
    [Google Scholar]
  27. Disney AA, Reynolds JH. 2014. Expression of m1-type muscarinic acetylcholine receptors by parvalbumin-immunoreactive neurons in the primary visual cortex: a comparative study of rat, guinea pig, ferret, macaque, and human. J. Comp. Neurol. 522:986–1003
    [Google Scholar]
  28. Disney AA, Robert JS 2019. Translational implications of the anatomical nonequivalence of functionally equivalent cholinergic circuit motifs. PNAS 116:26181–86
    [Google Scholar]
  29. Disney AA, Schultz SR. 2004. Hallucinations and acetylcholine: signal or noise?. Behav. Brain Sci. 27:790–91
    [Google Scholar]
  30. Foote SL, Morrison JH. 1987. Extrathalamic modulation of cortical function. Annu. Rev. Neurosci. 10:67–95
    [Google Scholar]
  31. Froemke RC. 2015. Plasticity of cortical excitatory-inhibitory balance. Annu. Rev. Neurosci. 38:195–219
    [Google Scholar]
  32. Garcia-Cabezas MA, Rico B, Sanchez-Gonzalez MA, Cavada C. 2007. Distribution of the dopamine innervation in the macaque and human thalamus. NeuroImage 34:965–84
    [Google Scholar]
  33. Giustino TF, Maren S 2018. Noradrenergic modulation of fear conditioning and extinction. Front. Behav. Neurosci. 12:43
    [Google Scholar]
  34. Gu Q. 2002. Neuromodulatory transmitter systems in the cortex and their role in cortical plasticity. Neuroscience 111:815–35
    [Google Scholar]
  35. Harris KD, Thiele A. 2011. Cortical state and attention. Nat. Rev. Neurosci. 12:509–23
    [Google Scholar]
  36. Hurley LM, Devilbiss DM, Waterhouse BD. 2004. A matter of focus: monoaminergic modulation of stimulus coding in mammalian sensory networks. Curr. Opin. Neurobiol. 14:488–95
    [Google Scholar]
  37. Jacob SN, Nienborg H. 2018. Monoaminergic neuromodulation of sensory processing. Front. Neural Circuits 12:51
    [Google Scholar]
  38. Kaczmarek LK, Levitan IB 1987. What is neuromodulation?. Neuromodulation: The Biochemical Control of Neuronal Excitability LK Kaczmarek, IB Levitan 3–17 Oxford, UK: Oxford Univ. Press
    [Google Scholar]
  39. Katz PS 1999. What are we talking about? Modes of neuronal communication. Beyond Neurotransmission: Neuromodulation and its Importance for Information Processing PS Katz 2–28 Oxford, UK: Oxford Univ. Press
    [Google Scholar]
  40. Katz PS, Lillvis JL. 2014. Reconciling the deep homology of neuromodulation with the evolution of behavior. Curr. Opin. Neurobiol. 29:39–47
    [Google Scholar]
  41. Kievit J, Kuypers HG. 1975. Basal forebrain and hypothalamic connection to frontal and parietal cortex in the rhesus monkey. Science 187:660–62
    [Google Scholar]
  42. Kosofsky BE, Molliver ME, Morrison JH, Foote SL. 1984. The serotonin and norepinephrine innervation of primary visual cortex in the cynomolgus monkey (Macaca fascicularis). J. Comp. Neurol. 230:168–78
    [Google Scholar]
  43. Krueger J, Disney AA. 2019. Structure and function of dual-source cholinergic modulation in early vision. J. Comp. Neurol. 527:738–50
    [Google Scholar]
  44. Lee SH, Dan Y 2012. Neuromodulation of brain states. Neuron 76:209–22
    [Google Scholar]
  45. Manning KA, Wilson JR, Uhlrich DJ. 1996. Histamine-immunoreactive neurons and their innervation of visual regions in the cortex, tectum, and thalamus in the primate Macaca mulatta. J. Comp. Neurol. 373:271–82
    [Google Scholar]
  46. Marder E. 2012. Neuromodulation of neuronal circuits: back to the future. Neuron 76:1–11
    [Google Scholar]
  47. McCormick DA. 1992. Neurotransmitter actions in the thalamus and cerebral cortex and their role in neuromodulation of thalamocortical activity. Prog. Neurobiol. 39:337–88
    [Google Scholar]
  48. McCormick DA, Williamson A. 1991. Modulation of neuronal firing mode in cat and guinea pig LGNd by histamine: possible cellular mechanisms of histaminergic control of arousal. J. Neurosci. 11:3188–99
    [Google Scholar]
  49. McLean J, Waterhouse BD. 1994. Noradrenergic modulation of cat area 17 neuronal responses to moving visual stimuli. Brain Res 667:83–97
    [Google Scholar]
  50. Mesulam MM, Van Hoesen GW. 1976. Acetylcholinesterase-rich projections from the basal forebrain of the rhesus monkey to neocortex. Brain Res 109:152–57
    [Google Scholar]
  51. Morrison JH, Foote SL. 1986. Noradrenergic and serotoninergic innervation of cortical, thalamic, and tectal visual structures in Old and New World monkeys. J. Comp. Neurol. 243:117–38
    [Google Scholar]
  52. Mrzljak L, Goldman-Rakic PS. 1993. Low-affinity nerve growth factor receptor (p75NGFR)- and choline acetyltransferase (ChAT)-immunoreactive axons in the cerebral cortex and hippocampus of adult macaque monkeys and humans. Cereb. Cortex 3:133–47
    [Google Scholar]
  53. Mrzljak L, Levey AI, Rakic P 1996. Selective expression of m2 muscarinic receptor in the parvocellular channel of the primate visual cortex. PNAS 93:7337–40
    [Google Scholar]
  54. Murphy PC, Sillito AM. 1991. Cholinergic enhancement of direction selectivity in the visual cortex of the cat. Neuroscience 40:13–20
    [Google Scholar]
  55. Nassi JJ, Callaway EM. 2009. Parallel processing strategies of the primate visual system. Nat. Rev. Neurosci. 10:360–72
    [Google Scholar]
  56. O'Donnell J, Zeppenfeld D, McConnell E, Pena S, Nedergaard M. 2012. Norepinephrine: a neuromodulator that boosts the function of multiple cell types to optimize CNS performance. Neurochem. Res. 37:2496–512
    [Google Scholar]
  57. Passani MB, Panula P, Lin JS. 2014. Histamine in the brain. Front. Syst. Neurosci. 8:64
    [Google Scholar]
  58. Patton MH, Blundon JA, Zakharenko SS. 2019. Rejuvenation of plasticity in the brain: opening the critical period. Curr. Opin. Neurobiol. 54:83–89
    [Google Scholar]
  59. Picciotto MR. 2003. Nicotine as a modulator of behavior: beyond the inverted U. Trends Pharmacol. Sci. 24:493–99
    [Google Scholar]
  60. Picciotto MR, Higley MJ, Mineur YS. 2012. Acetylcholine as a neuromodulator: cholinergic signaling shapes nervous system function and behavior. Neuron 76:116–29
    [Google Scholar]
  61. Rakic P, Goldman-Rakic PS, Gallager D 1988. Quantitative autoradiography of major neurotransmitter receptors in the monkey striate and extrastriate cortex. J. Neurosci. 8:3670–90
    [Google Scholar]
  62. Roberts MJ, Zinke W, Guo K, Robertson R, McDonald JS, Thiele A. 2005. Acetylcholine dynamically controls spatial integration in marmoset primary visual cortex. J. Neurophysiol. 93:2062–72
    [Google Scholar]
  63. Roelfsema PR, Holtmaat A. 2018. Control of synaptic plasticity in deep cortical networks. Nat. Rev. Neurosci. 19:166–80
    [Google Scholar]
  64. Sanchez-Gonzalez MA, Garcia-Cabezas MA, Rico B, Cavada C 2005. The primate thalamus is a key target for brain dopamine. J. Neurosci. 25:6076–83
    [Google Scholar]
  65. Sara SJ, Bouret S. 2012. Orienting and reorienting: the locus coeruleus mediates cognition through arousal. Neuron 76:130–41
    [Google Scholar]
  66. Saras A, Gisselmann G, Vogt-Eisele AK, Erlkamp KS, Kletke O et al. 2008. Histamine action on vertebrate GABAA receptors: direct channel gating and potentiation of GABA responses. J. Biol. Chem. 283:10470–75
    [Google Scholar]
  67. Sarter M, Lustig C. 2020. Forebrain cholinergic signaling: wired and phasic, not tonic, and causing behavior. J. Neurosci. 40:712–19
    [Google Scholar]
  68. Sarter M, Parikh V, Howe WM. 2009. nAChR agonist-induced cognition enhancement: integration of cognitive and neuronal mechanisms. Biochem. Pharmacol. 78:658–67
    [Google Scholar]
  69. Schofield SPM, Dixson AF. 1982. Comparative anatomy of brain monoaminergic neurons in New World and Old World monkeys. Am. J. Primatol. 2:3–19
    [Google Scholar]
  70. Schultz W. 2007. Multiple dopamine functions at different time courses. Annu. Rev. Neurosci. 30:259–88
    [Google Scholar]
  71. Seillier L, Lorenz C, Kawaguchi K, Ott T, Nieder A et al. 2017. Serotonin decreases the gain of visual responses in awake macaque V1. J. Neurosci. 37:11390–405
    [Google Scholar]
  72. Sharma G, Grybko M, Vijayaraghavan S. 2008. Action potential-independent and nicotinic receptor-mediated concerted release of multiple quanta at hippocampal CA3-mossy fiber synapses. J. Neurosci. 28:2563–75
    [Google Scholar]
  73. Sherman SM. 2001. Tonic and burst firing: dual modes of thalamocortical relay. Trends Neurosci 24:122–26
    [Google Scholar]
  74. Sincich LC, Horton JC. 2005. The circuitry of V1 and V2: integration of color, form, and motion. Annu. Rev. Neurosci. 28:303–26
    [Google Scholar]
  75. Soma S, Shimegi S, Osaki H, Sato H. 2012. Cholinergic modulation of response gain in the primary visual cortex of the macaque. J. Neurophysiol. 107:283–91
    [Google Scholar]
  76. Sugihara H, Chen N, Sur M. 2016. Cell-specific modulation of plasticity and cortical state by cholinergic inputs to the visual cortex. J. Physiol. Paris 110:37–43
    [Google Scholar]
  77. Sykova E, Nicholson C. 2008. Diffusion in brain extracellular space. Physiol. Rev. 88:1277–340
    [Google Scholar]
  78. Tamvacakis AN, Senatore A, Katz PS. 2018. Single neuron serotonin receptor subtype gene expression correlates with behaviour within and across three molluscan species. Proc. Biol. Sci. 285:20180791
    [Google Scholar]
  79. Thiele A, Herrero JL, Distler C, Hoffmann KP. 2012. Contribution of cholinergic and GABAergic mechanisms to direction tuning, discriminability, response reliability, and neuronal rate correlations in macaque middle temporal area. J. Neurosci. 32:16602–15
    [Google Scholar]
  80. Threlfell S, Lalic T, Platt NJ, Jennings KA, Deisseroth K, Cragg SJ. 2012. Striatal dopamine release is triggered by synchronized activity in cholinergic interneurons. Neuron 75:58–64
    [Google Scholar]
  81. Usrey WM, Alitto HJ. 2015. Visual functions of the thalamus. Annu. Rev. Vis. Sci. 1:351–71
    [Google Scholar]
  82. Vizi ES. 1979. Presynaptic modulation of neurochemical transmission. Prog. Neurobiol. 12:181–290
    [Google Scholar]
  83. Vizi ES, Fekete A, Karoly R, Mike A 2010. Non-synaptic receptors and transporters involved in brain functions and targets of drug treatment. Br. J. Pharmacol. 160:785–809
    [Google Scholar]
  84. Watakabe A, Komatsu Y, Sadakane O, Shimegi S, Takahata T et al. 2009. Enriched expression of serotonin 1B and 2A receptor genes in macaque visual cortex and their bidirectional modulatory effects on neuronal responses. Cereb. Cortex 19:1915–28
    [Google Scholar]
  85. Wilson JR, Manning KA, Forestner DM, Counts SE, Uhlrich DJ. 1999. Comparison of cholinergic and histaminergic axons in the lateral geniculate complex of the macaque monkey. Anat. Rec. 255:295–305
    [Google Scholar]
  86. Wilson MA, Molliver ME. 1991a. The organization of serotonergic projections to cerebral cortex in primates: regional distribution of axon terminals. Neuroscience 44:537–53
    [Google Scholar]
  87. Wilson MA, Molliver ME. 1991b. The organization of serotonergic projections to cerebral cortex in primates: retrograde transport studies. Neuroscience 44:555–70
    [Google Scholar]
  88. Yoshikawa T, Naganuma F, Iida T, Nakamura T, Harada R et al. 2013. Molecular mechanism of histamine clearance by primary human astrocytes. Glia 61:905–16
    [Google Scholar]
  89. Yousif N, Fu RZ, Abou-El-Ela Bourquin B, Bhrugubanda V, Schultz SR, Seemungal BM. 2016. Dopamine activation preserves visual motion perception despite noise interference of human V5/MT. J. Neurosci. 36:9303–12
    [Google Scholar]
  90. Zinke W, Roberts MJ, Guo K, McDonald JS, Robertson R, Thiele A. 2006. Cholinergic modulation of response properties and orientation tuning of neurons in primary visual cortex of anaesthetized marmoset monkeys. Eur. J. Neurosci. 24:314–28
    [Google Scholar]
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