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

Journal of Comparative Neurology

Volumn 522, Issue 5, 2014, Pages 986-1003

  Disney, Anita A ^a   Reynolds, John H ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

Anatomy; Calcium binding proteins; Immunofluorescence; Neuromodulation; Parvalbumin; Quantitative; Striate cortex

Indexed keywords

ANATOMY; CALCIUM-BINDING PROTEINS; IMMUNOFLUORESCENCE; NEUROMODULATION; PARVALBUMIN; QUANTITATIVE; STRIATE CORTEX;

ADULT; ANIMALS; CELL COUNT; FEMALE; FERRETS; GENE EXPRESSION REGULATION; GUINEA PIGS; HUMANS; MACACA MULATTA; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MIDDLE AGED; NEURONS; PARVALBUMINS; RECEPTOR, MUSCARINIC M1; SPECIES SPECIFICITY; TRANSDUCTION, GENETIC; VISUAL CORTEX;

EID: 84893748602     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23456     Document Type: Article

References (50)

1. Alitto HJ, Dan Y. 2012. Cell-type-specific modulation of neocortical activity by basal forebrain input. Front Systems Neurosci 6:79.
2. Aoki C, Kabak S. 1992. Cholinergic terminals in the cat visual cortex: ultrastructural basis for interaction with glutamate-immunoreactive neurons and other cells. Vis Neurosci 8:177-191.
3. Arnold HM, Burk JA, Hodgson EM, Sarter M, Bruno JP. 2002. Differential cortical acetylcholine release in rats performing a sustained attention task versus behavioral control tasks that do not explicitly tax attention. Neuroscience 114:451-460.
4. Beaulieu C, Somogyi P. 1991. Enrichment of cholinergic synaptic terminals on GABAergic neurons and coexistence of immunoreactive GABA and choline acetyltransferase in the same synaptic terminals in the striate cortex of the cat. J Comp Neurol 304:666-680.
5. Beaulieu C, Kisvarday Z, Somogyi P, Cynader M, Cowey A. 1992. Quantitative distribution of GABA-immunopositive and -immunonegative neurons and synapses in the monkey striate cortex (area 17). Cereb Cortex 2:295-309.
6. Brodmann K. 1909. Localisation in the cerebral cortex. Garey LJ, translator. London: Smith-Gordon.
7. Brown DA, Adams PR. 1980. Muscarinic suppression of a novel voltage-sensitive K+ current in a vertebrate neurone. Nature 283:673-676.
8. Burette A, Zabel U, Weinberg RJ, Schmidt HH, Valtschanoff JG. 2002. Synaptic localization of nitric oxide synthase and soluble guanylyl cyclase in the hippocampus. J Neurosci 22:8961-8970.
9. Celio MR, Baier W, Scharer L, de Viragh PA, Gerday C. 1988. Monoclonal antibodies directed against the calcium binding protein parvalbumin. Cell Calcium 9:81-86.
10. Choudhury BP. 1978. Retinotopic organization of the guinea pig's visual cortex. Brain Res 144:19-29.
11. Collins CE, Airey DC, Young NA, Leitch DB, Kaas JH. 2010. Neuron densities vary across and within cortical areas in primates. Proc Natl Acad Sci U S A 107:15927-15932.
12. Conde F, Lund JS, Jacobowitz DM, Baimbridge KG, Lewis DA. 1994. Local circuit neurons immunoreactive for calretinin, calbindin D-28k or parvalbumin in monkey prefrontal cortex: distribution and morphology. J Comp Neurol 341:95-116.
13. Deco G, Thiele A. 2011. Cholinergic control of cortical network interactions enables feedback-mediated attentional modulation. Eur J Neurosci 34:146-157.
14. DeFelipe J, Gonzalez-Albo MC, Del Rio MR, Elston GN. 1999. Distribution and patterns of connectivity of interneurons containing calbindin, calretinin, and parvalbumin in visual areas of the occipital and temporal lobes of the macaque monkey. J Comp Neurol 412:515-526.
15. Disney AA, Aoki C. 2008. Muscarinic acetylcholine receptors in macaque V1 are most frequently expressed by parvalbumin-immunoreactive neurons. J Comp Neurol 507:1748-1762.
16. Disney AA, Domakonda K, Aoki C. 2006. Differential expression of muscarinic acetylcholine receptors across excitatory and inhibitory cells in visual cortical areas V1 and V2 of the macaque monkey. J Comp Neurol 499:49-63.
17. Disney AA, Aoki C, Hawken MJ. 2007. Gain modulation by nicotine in macaque v1. Neuron 56:701-713.
18. Disney AA, Aoki C, Hawken MJ. 2012. Cholinergic suppression of visual responses in primate V1 is mediated by GABAergic inhibition. J Neurophysiol 108:1907-1923.
19. Elston GN, Rosa MG. 1997. The occipitoparietal pathway of the macaque monkey: comparison of pyramidal cell morphology in layer III of functionally related cortical visual areas. Cereb Cortex 7:432-452.
20. Gallyas F. 1970. Silver staining of micro- and oligodendroglia by means of physical development. Acta Neuropathol 16:35-38.
21. Gil Z, Connors BW, Amitai Y. 1997. Differential regulation of neocortical synapses by neuromodulators and activity. Neuron 19:679-686.
22. Gonchar Y, Burkhalter A. 1997. Three distinct families of GABAergic neurons in rat visual cortex. Cerebral Cortex 7:347-358.
23. Guillery RW. 2002. On counting and counting errors. J Comp Neurol 447:1-7.
24. Gulledge AT, Park SB, Kawaguchi Y, Stuart GJ. 2007. Heterogeneity of phasic cholinergic signalling in neocortical neurons. J Neurophysiol 97:2215-2229.
25. Hasselmo ME, Bower JM. 1992. Cholinergic suppression specific to intrinsic not afferent fiber synapses in rat piriform (olfactory) cortex. J Neurophysiol 67:1222-1229.
26. Hasselmo ME, McGaughy J. 2004. High acetylcholine levels set circuit dynamics for attention and encoding and low acetylcholine levels set dynamics for consolidation. Prog Brain Res 145:207-231.
27. Herrero JL, Roberts MJ, Delicato LS, Gieselmann MA, Dayan P, Thiele A. 2008. Acetylcholine contributes through muscarinic receptors to attentional modulation in V1. Nature 454:1110-1114.
28. Himmelheber AM, Sarter M, Bruno JP. 2000. Increases in cortical acetylcholine release during sustained attention performance in rats. Brain Res Cogn Brain Res 9:313-325.
29. Hsieh CY, Cruikshank SJ, Metherate R. 2000. Differential modulation of auditory thalamocortical and intracortical synaptic transmission by cholinergic agonist. Brain Res 880:51-64.
30. Katzner S, Busse L, Carandini M. 2011. GABAA inhibition controls response gain in visual cortex. J Neurosci 31:5931-5941.
31. Kawaguchi Y. 1997. Selective cholinergic modulation of cortical GABAergic cell subtypes. J Neurophysiol 78:1743-1747.
32. Kawaguchi Y, Kubota Y. 1993. Correlation of physiological subgroupings of nonpyramidal cells with parvalbumin- and calbindinD28k-immunoreactive neurons in layer V of rat frontal cortex. J Neurophysiol 70:387-396.
33. Kimura F. 2000. Cholinergic modulation of cortical function: a hypothetical role in shifting the dynamics in cortical network. Neurosci Res 38:19-26.
34. Kruglikov I, Rudy B. 2008. Perisomatic GABA release and thalamocortical integration onto neocortical excitatory cells are regulated by neuromodulators. Neuron 58:911-924.
35. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C. 2004. Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5:793-807.
36. McConnell SK, LeVay S. 1986. Anatomical organization of the visual system of the mink, Mustela vison. J Comp Neurol 250:109-132.
37. McCormick DA, Prince DA. 1986. Mechanisms of action of acetylcholine in the guinea-pig cerebral cortex in vitro. J Physiol 375:169-194.
38. McGaughy J, Sarter M. 1998. Sustained attention performance in rats with intracortical infusions of 192 IgG-saporin-induced cortical cholinergic deafferentation: effects of physostigmine and FG 7142. Behav Neurosci 112:1519-1525.
39. Muir JL, Everitt BJ, Robbins TW. 1994. AMPA-induced excitotoxic lesions of the basal forebrain: a significant role for the cortical cholinergic system in attentional function. J Neurosci 14:2313-2326.
40. Paxinos G, Franklin KBJ. 2003. The mouse brain in stereotaxic coordinates, 2nd ed. Academic Press.
41. Paxinos G, Watson C. 2007. The Rat Brain in Stereotaxic Coordinates, Sixth Edition: San Diego, CA: Academic Press.
42. Paxinos G, Huang XF, Toga AW. 2000. The rhesus monkey brain in stereotaxic coordinates: Academic Press.
43. Sarter M, Hasselmo ME, Bruno JP, Givens B. 2005. Unraveling the attentional functions of cortical cholinergic inputs: interactions between signal-driven and cognitive modulation of signal detection. Brain Res Brain Res Rev 48:98-111.
44. Schwaller B, Dick J, Dhoot G, Carroll S, Vrbova G, Nicotera P, Pette D, Wyss A, Bluethmann H, Hunziker W, Celio MR. 1999. Prolonged contraction-relaxation cycle of fast-twitch muscles in parvalbumin knockout mice. Am J Physiol 276:C395-403.
45. Turrini P, Casu MA, Wong TP, De Koninck Y, Ribeiro-da-Silva A, Cuello AC. 2001. Cholinergic nerve terminals establish classical synapses in the rat cerebral cortex: synaptic pattern and age-related atrophy. Neuroscience 105:277-285.
46. Umbriaco D, Watkins KC, Descarries L, Cozzari C, Hartman BK. 1994. Ultrastructural and morphometric features of the acetylcholine innervation in adult rat parietal cortex: an electron microscopic study in serial sections. J Comp Neurol 348:351-373.
47. Van Brederode JF, Mulligan KA, Hendrickson AE. 1990. Calcium-binding proteins as markers for subpopulations of GABAergic neurons in monkey striate cortex. J Comp Neurol 298:1-22.
48. White LE, Bosking WH, Williams SM, Fitzpatrick D. 1999. Maps of central visual space in ferret V1 and V2 lack matching inputs from the two eyes. J Neurosci 19:7089-7099.
49. Wong-Riley M, Anderson B, Liebl W, Huang Z. 1998. Neurochemical organization of the macaque striate cortex: correlation of cytochrome oxidase with Na+K+ATPase, NADPH-diaphorase, nitric oxide synthase, and N-methyl-D-aspartate receptor subunit 1. Neuroscience 83:1025-1045.
50. Xiang Z, Huguenard JR, Prince DA. 1998. Cholinergic switching within neocortical inhibitory networks. Science 281:985-988.