Chemogenetic Inactivation of Dorsal Anterior Cingulate Cortex Neurons Disrupts Attentional Behavior in Mouse

Neuropsychopharmacology

Volumn 41, Issue 4, 2016, Pages 1014-1023

  Koike, Hiroyuki ^a   Demars, Michael P ^a   Short, Jennifer A ^a   Nabel, Elisa M ^a   Akbarian, Schahram ^a   Baxter, Mark G ^a   Morishita, Hirofumi ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY LABELING; ARTICLE; ATTENTION; ATTENTION DEFICIT DISORDER; CHEMOGENETIC INACTIVATION; CONTROLLED STUDY; DORSAL ANTERIOR CINGULATE CORTEX; GENE INACTIVATION; IMMUNOHISTOCHEMISTRY; LATENT PERIOD; LOCOMOTION; MALE; MOTIVATION; MOTOR PERFORMANCE; MOUSE; NONHUMAN; ONCOGENE C FOS; PREFRONTAL CORTEX; PRIORITY JOURNAL; STIMULUS; ANALOGS AND DERIVATIVES; ANIMAL; C57BL MOUSE; CINGULATE GYRUS; DRUG EFFECTS; GENE VECTOR; GENETICS; METABOLISM; NERVE CELL; PHYSIOLOGY; REACTION TIME;

4 AMINOBUTYRIC ACID RECEPTOR BLOCKING AGENT; CLOZAPINE; CLOZAPINE N-OXIDE; MUSCARINIC M4 RECEPTOR; PENTETRAZOLE;

ANIMALS; ATTENTION; CLOZAPINE; GABA ANTAGONISTS; GENETIC VECTORS; GYRUS CINGULI; MALE; MICE; MICE, INBRED C57BL; NEURONS; PENTYLENETETRAZOLE; REACTION TIME; RECEPTOR, MUSCARINIC M4;

EID: 84957437039     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2015.229     Document Type: Article

References (64)

1. Alexander GM, Rogan SC, Abbas AI, Armbruster BN, Pei Y, Allen JA et al (2009). Remote control of neuronal activity in transgenic mice expressing evolved G protein-coupled receptors. Neuron 63: 27-39.
2. Alexander MP, Stuss DT, Shallice T, Picton TW, Gillingham S (2005). Impaired concentration due to frontal lobe damage from two distinct lesion sites. Neurology 65: 572-579.
3. Andre V, Pineau N, Motte JE, Marescaux C, Nehlig A (1998). Mapping of neuronal networks underlying generalized seizures induced by increasing doses of pentylenetetrazol in the immature and adult rat: A c-Fos immunohistochemical study. Eur J Neurosci 10: 2094-2106.
4. Arnold HM, Bruno JP, Sarter M (2003). Assessment of sustained and divided attention in rats. Curr Protoc Neurosci Chapter 8: Unit 8.5E.
5. Aschauer DF, Kreuz S, Rumpel S (2013). Analysis of transduction efficiency, tropism and axonal transport of AAV serotypes 1, 2, 5, 6, 8 and 9 in the mouse brain. PLoS One 8: e76310.
6. Bari A, Dalley JW, Robbins TW (2008). The application of the 5-choice serial reaction time task for the assessment of visual attentional processes and impulse control in rats. Nat Protoc 3: 759-767.
7. Barnett JH, Robbins TW, Leeson VC, Sahakian BJ, Joyce EM, Blackwell AD (2010). Assessing cognitive function in clinical trials of schizophrenia. Neurosci Biobehav Rev 34: 1161-1177.
8. Boender AJ, de Jong JW, Boekhoudt L, Luijendijk MC, van der Plasse G, Adan RA (2014). Combined use of the canine adenovirus-2 and DREADD-Technology to activate specific neural pathways in vivo. PLoS One 9: e95392.
9. Booth JR, Burman DD, Meyer JR, Lei Z, Trommer BL, Davenport ND et al (2003). Neural development of selective attention and response inhibition. Neuroimage 20: 737-751.
10. Brown RG, Scott LC, Bench CJ, Dolan RJ (1994). Cognitive function in depression: its relationship to the presence and severity of intellectual decline. Psychol Med 24: 829-847.
11. Bush G, Frazier JA, Rauch SL, Seidman LJ, Whalen PJ, Jenike MA et al (1999). Anterior cingulate cortex dysfunction in attentiondeficit/hyperactivity disorder revealed by fMRI and the Counting Stroop. Biol Psychiatry 45: 1542-1552.
12. Bussey TJ, Holmes A, Lyon L, Mar AC, McAllister KA, Nithianantharajah J et al (2012). New translational assays for preclinical modelling of cognition in schizophrenia: The touchscreen testing method for mice and rats. Neuropharmacology 62: 1191-1203.
13. Carli M, Baviera M, Invernizzi RW, Balducci C (2006). Dissociable contribution of 5-HT1A and 5-HT2A receptors in the medial prefrontal cortex to different aspects of executive control such as impulsivity and compulsive perseveration in rats. Neuropsychopharmacology 31: 757-767.
14. Carter ME, Soden ME, Zweifel LS, Palmiter RD (2013). Genetic identification of a neural circuit that suppresses appetite. Nature 503: 111-114.
15. Chen WJ, Faraone SV (2000). Sustained attention deficits as markers of genetic susceptibility to schizophrenia. Am J Med Genet 97: 52-57.
16. Chudasama Y, Passetti F, Rhodes SE, Lopian D, Desai A, Robbins TW (2003). Dissociable aspects of performance on the 5-choice serial reaction time task following lesions of the dorsal anterior cingulate, infralimbic and orbitofrontal cortex in the rat: differential effects on selectivity, impulsivity and compulsivity. Behav Brain Res 146: 105-119.
17. Cohen RA, Kaplan RF, Moser DJ, Jenkins MA, Wilkinson H (1999). Impairments of attention after cingulotomy. Neurology 53: 819-824.
18. Corbetta M, Miezin FM, Dobmeyer S, Shulman GL, Petersen SE (1991). Selective and divided attention during visual discriminations of shape, color, and speed: functional anatomy by positron emission tomography. J Neurosci 11: 2383-2402.
19. Cornblatt BA, Malhotra AK (2001). Impaired attention as an endophenotype for molecular genetic studies of schizophrenia. Am J Med Genet 105: 11-15.
20. Cuthbert BN (2015). Research Domain Criteria: Toward future psychiatric nosologies. Dialog Clin Neurosci 17: 89-97.
21. Demars MP, Morishita H (2014). Cortical parvalbumin and somatostatin GABA neurons express distinct endogenous modulators of nicotinic acetylcholine receptors. Mol Brain 7: 75.
22. Fair DA, Dosenbach NU, Church JA, Cohen AL, Brahmbhatt S, Miezin FM et al (2007). Development of distinct control networks through segregation and integration. Proc Natl Acad Sci USA 104: 13507-13512.
23. Farrell MS, Roth BL (2013). Pharmacosynthetics: reimagining the pharmacogenetic approach. Brain Res 1511: 6-20.
24. Ferguson SM, Eskenazi D, Ishikawa M, Wanat MJ, Phillips PE, Dong Y et al (2011). Transient neuronal inhibition reveals opposing roles of indirect and direct pathways in sensitization. Nat Neurosci 14: 22-24.
25. Goodkind M, Eickhoff SB, Oathes DJ, Jiang Y, Chang A, Jones-Hagata LB et al (2015). Identification of a common neurobiological substrate for mental illness. JAMA Psychiatry 72: 305-315.
26. Homayoun H, Moghaddam B (2007). NMDA receptor hypofunction produces opposite effects on prefrontal cortex interneurons and pyramidal neurons. J Neurosci 27: 11496-11500.
27. Huang-Pollock CL, Karalunas SL, Tam H, Moore AN (2012). Evaluating vigilance deficits in ADHD: A meta-Analysis of CPT performance. J Abnorm Psychol 121: 360-371.
28. Insel T, Cuthbert B, Garvey M, Heinssen R, Pine DS, Quinn K et al (2010). Research domain criteria (RDoC): Toward a new classification framework for research on mental disorders. Am J Psychiatry 167: 748-751.
29. Johnston K, Levin HM, Koval MJ, Everling S (2007). Top-down control-signal dynamics in anterior cingulate and prefrontal cortex neurons following task switching. Neuron 53: 453-462.
30. Koch M, Varela L, Kim JG, Kim JD, Hernandez-Nuno F, Simonds SE et al (2015). Hypothalamic POMC neurons promote cannabinoid-induced feeding. Nature 519: 45-50.
31. Krashes MJ, Koda S, Ye C, Rogan SC, Adams AC, Cusher DS et al (2011). Rapid, reversible activation of AgRP neurons drives feeding behavior in mice. J Clin Invest 121: 1424-1428.
32. Lazo OM, Mauna JC, Pissani CA, Inestrosa NC, Bronfman FC (2010). Axotomy-induced neurotrophic withdrawal causes the loss of phenotypic differentiation and downregulation of NGF signalling, but not death of septal cholinergic neurons. Mol Neurodegener 5: 5.
33. Li B, Wang L, Sun Z, Zhou Y, Shao D, Zhao J et al (2014). The anticonvulsant effects of SR 57227 on pentylenetetrazole-induced seizure in mice. PLoS One 9: e93158.
34. Lustig C, Kozak R, Sarter M, Young JW, Robbins TW (2013). CNTRICS final animal model task selection: control of attention. Neurosci Biobehav Rev 37: 2099-2110.
35. Mahler SV, Vazey EM, Beckley JT, Keistler CR, McGlinchey EM, Kaufling J et al (2014). Designer receptors show role for ventral pallidum input to ventral tegmental area in cocaine seeking. Nat Neurosci 17: 577-585.
36. Mar AC, Horner AE, Nilsson SR, Alsio J, Kent BA, Kim CH et al (2013). The touchscreen operant platform for assessing executive function in rats and mice. Nat Protoc 8: 1985-2005.
37. Moore H, Geyer MA, Carter CS, Barch DM (2013). Harnessing cognitive neuroscience to develop new treatments for improving cognition in schizophrenia: CNTRICS selected cognitive paradigms for animal models. Neurosci Biobehav Rev 37: 2087-2091.
38. Ochsner KN, Kosslyn SM, Cosgrove GR, Cassem EH, Price BH, Nierenberg AA et al (2001). Deficits in visual cognition and attention following bilateral anterior cingulotomy. Neuropsychologia 39: 219-230.
39. Parnaudeau S, O'Neill PK, Bolkan SS, Ward RD, Abbas AI, Roth BL et al (2013). Inhibition of mediodorsal thalamus disrupts thalamofrontal connectivity and cognition. Neuron 77: 1151-1162.
40. Parnaudeau S, Taylor K, Bolkan SS, Ward RD, Balsam PD, Kellendonk C (2015). Mediodorsal thalamus hypofunction impairs flexible goal-directed behavior. Biol Psychiatry 77: 445-453.
41. Passetti F, Chudasama Y, Robbins TW (2002). The frontal cortex of the rat and visual attentional performance: dissociable functions of distinct medial prefrontal subregions. Cereb Cortex 12: 1254-1268.
42. Pehrson AL, Bondi CO, Totah NK, Moghaddam B (2013). The influence of NMDA and GABA(A) receptors and glutamic acid decarboxylase (GAD) activity on attention. Psychopharmacology 225: 31-39.
43. Penzo MA, Robert V, Tucciarone J, De Bundel D, Wang M, Van Aelst L et al (2015). The paraventricular thalamus controls a central amygdala fear circuit. Nature 519: 455-459.
44. Perova Z, Delevich K, Li B (2015). Depression of excitatory synapses onto parvalbumin interneurons in the medial prefrontal cortex in susceptibility to stress. J Neurosci 35: 3201-3206.
45. Ray RS, Corcoran AE, Brust RD, Kim JC, Richerson GB, Nattie E et al (2011). Impaired respiratory and body temperature control upon acute serotonergic neuron inhibition. Science 333: 637-642.
46. Richards BA, Xia F, Santoro A, Husse J, Woodin MA, Josselyn SA et al (2014). Patterns across multiple memories are identified over time. Nat Neurosci 17: 981-986.
47. Robbins TW (2002). The 5-choice serial reaction time task: behavioural pharmacology and functional neurochemistry. Psychopharmacology 163: 362-380.
48. Romberg C, Mattson MP, Mughal MR, Bussey TJ, Saksida LM (2011). Impaired attention in the 3xTgAD mouse model of Alzheimer's disease: rescue by donepezil (Aricept). J Neurosci 31: 3500-3507.
49. Sasaki K, Suzuki M, Mieda M, Tsujino N, Roth B, Sakurai T (2011). Pharmacogenetic modulation of orexin neurons alters sleep/wakefulness states in mice. PLoS One 6: e20360.
50. Silverman JL, Gastrell PT, Karras MN, Solomon M, Crawley JN (2013). Cognitive abilities on transitive inference using a novel touchscreen technology for mice. Cereb Cortex 25: 1133-1142.
51. Totah NK, Jackson ME, Moghaddam B (2013). Preparatory attention relies on dynamic interactions between prelimbic cortex and anterior cingulate cortex. Cereb Cortex 23: 729-738.
52. Totah NK, Kim YB, Homayoun H, Moghaddam B (2009). Anterior cingulate neurons represent errors and preparatory attention within the same behavioral sequence. J Neurosci 29: 6418-6426.
53. Urban DJ, Roth BL (2015). DREADDs (designer receptors exclusively activated by designer drugs): chemogenetic tools with therapeutic utility. Annu Rev Pharmacol Toxicol 55: 399-417.
54. Uylings HB, Groenewegen HJ, Kolb B (2003). Do rats have a prefrontal cortex? Behav Brain Res 146: 3-17.
55. Vogt BA, Paxinos G (2014). Cytoarchitecture of mouse and rat cingulate cortex with human homologies. Brain Struct Funct 219: 185-192.
56. Weissman DH, Gopalakrishnan A, Hazlett CJ, Woldorff MG (2005). Dorsal anterior cingulate cortex resolves conflict from distracting stimuli by boosting attention toward relevant events. Cereb Cortex 15: 229-237.
57. Young JW, Amitai N, Geyer MA (2012). Behavioral animal models to assess pro-cognitive treatments for schizophrenia. Handb Exp Pharmacol 39-79.
58. Young JW, Geyer MA (2015). Developing treatments for cognitive deficits in schizophrenia: The challenge of translation. J Psychopharmacol 29: 178-196.
59. Young JW, Geyer MA, Rissling AJ, Sharp RF, Eyler LT, Asgaard GL et al (2013a). Reverse translation of the rodent 5C-CPT reveals that the impaired attention of people with schizophrenia is similar to scopolamine-induced deficits in mice. Transl Psychiatry 3: e324.
60. Young JW, Jentsch JD, Bussey TJ, Wallace TL, Hutcheson DM (2013b). Consideration of species differences in developing novel molecules as cognition enhancers. Neurosci Biobehav Rev 37: 2181-2193.
61. Young JW, Light GA, Marston HM, Sharp R, Geyer MA (2009). The 5-choice continuous performance test: evidence for a translational test of vigilance for mice. PLoS One 4: e4227.
62. Zhang S, Xu M, Kamigaki T, Hoang Do JP, Chang WC, Jenvay S et al (2014). Selective attention. Long-range and local circuits for top-down modulation of visual cortex processing. Science 345: 660-665.
63. Zhu H, Roth BL (2014). DREADD: A chemogenetic GPCR signaling platform. Int J Neuropsychopharmacol 18 Please provide the page range in reference Zhu and Roth, 2014.
64. Zingg B, Hintiryan H, Gou L, Song MY, Bay M, Bienkowski MS et al (2014). Neural networks of the mouse neocortex. Cell 156: 1096-1111.