Distinct local circuit properties of the superficial and intermediate layers of the rodent superior colliculus

European Journal of Neuroscience

Volumn 40, Issue 2, 2014, Pages 2329-2343

  Phongphanphanee, Penphimon ^a,f   Marino, Robert A ^b   Kaneda, Katsuyuki ^a,c,g   Yanagawa, Yuchio ^d,e   Munoz, Douglas P ^b   Isa, Tadashi ^a,c,e  

^a NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

^b QUEEN S UNIVERSITY   (Canada)

^c GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^d GUNMA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^e JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^f Pharmaceutical Division Novartis (Thailand) Limited   (Thailand)

^g HOKKAIDO UNIVERSITY   (Japan)

Author keywords

Inhibition; Lateral interactions; Mouse; Patch clamp; Saliency

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; 6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; GLUTAMIC ACID;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; CONTROLLED STUDY; DECISION MAKING; EXCITATORY POSTSYNAPTIC POTENTIAL; FUNCTIONAL ELECTRICAL STIMULATION; INHIBITORY POSTSYNAPTIC POTENTIAL; INTERMEDIATE LAYER SUPERIOR COLLICULUS; NERVE CELL EXCITABILITY; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE CELL STIMULATION; NONHUMAN; PRIORITY JOURNAL; SACCADIC EYE MOVEMENT; SENSORIMOTOR FUNCTION; SENSORIMOTOR INTEGRATION; STIMULUS RESPONSE; SUPERFICIAL LAYER SUPERIOR COLLICULUS; SUPERIOR COLLICULUS; SYNAPTIC TRANSMISSION; VISUAL NERVOUS SYSTEM; WHOLE CELL PATCH CLAMP; ANIMAL; ANTIBODY SPECIFICITY; MOUSE; PHYSIOLOGY;

ANIMALS; EXCITATORY POSTSYNAPTIC POTENTIALS; INHIBITORY POSTSYNAPTIC POTENTIALS; MICE; NERVE NET; ORGAN SPECIFICITY; SUPERIOR COLLICULI;

EID: 84904696692     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12579     Document Type: Article

References (54)

1. Appell, P.P. & Behan, M. (1990) Sources of subcortical GABAergic projections to the superior colliculus in the cat. J. Comp. Neurol., 302, 143-158.
2. Arai, K., Das, S., Keller, E. & Aiyochi, E. (1999) A distributed model of the saccade system: simulations of temporally perturbed saccades using position and velocity feedback. Neural Networks, 12, 1359-1375.
3. Badler, J.B. & Keller, E.L. (2009) Decoding of a motor command vector from distributed activity in superior colliculus. Biol. Cybern., 86, 179-189.
4. Behan, M. (1985) An EM-autoradiographic and EM-HRP study of the commissural projection of the superior colliculus in the cat. J. Comp. Neurol., 234, 105-116.
5. Boehnke, S.E. & Munoz, D.P. (2008) On the importance of the transient visual response in the superior colliculus. Curr. Opin. Neurobiol., 18, 544-551.
6. Buswell, G. (1935) How People Look at Pictures. University of Chicago Press, Oxford, UK.
7. Dalva, M.B. & Katz, L.C. (1994) Rearrangements of synaptic connections in visual cortex revealed by laser photostimulation. Science, 265, 255-258.
8. Dorris, M.C., Olivier, E. & Munoz, D.P. (2007) Competitive integration of visual and preparatory signals in the superior colliculus during saccadic programming. J. Neurosci., 27, 5053-5062.
9. Edelman, J.A. & Keller, E.L. (1998) Dependence on target configuration of express saccade-related activity in the primate superior colliculus. J. Neurophysiol., 80, 1407-1426.
10. Edwards, S.B. (1980) The deep cell layers of the superior colliculus; their reticular characteristics and structural organization. In Hobson, J.A. & Brazier, MA.B. (Eds), The Reticular Formation Revisited. Raven Press, New York, pp. 193-209.
11. Endo, T., Yanagawa, Y., Obata, K. & Isa, T. (2003) Characteristics of GABAergic neurons in the superficial superior colliculus in mice. Neurosci. Lett., 346, 81-84.
12. Ficalora, A.S. & Mize, R.R. (1989) The neurons of the substantia nigra and zona incerta which project to the cat superior colliculus are GABA immunoreactive: a double-label study using GABA immunocytochemistry and lectin retrograde transport. Neuroscience, 29, 567-581.
13. Gandhi, N.J. & Katnani, H.A. (2011) Motor functions of the superior colliculus. Annu. Rev. Neurosci., 34, 205-231.
14. Godement, P., Salaun, J. & Imbert, M. (1984) Prenatal and postnatal development of retinogeniculate and retinocollicular projections in the mouse. J. Comp. Neurol., 230, 552-575.
15. Helms, M.C., Özen, G. & Hall, W.C. (2004) Organization of the intermediate gray layer of the superior colliculus. I. Intrinsic vertical connections. J. Neurophysiol., 91, 1706-1715.
16. Hikosaka, O. & Wurtz, R.H. (1983) Visual and oculomotor functions of monkey substantia nigra pars reticulata. IV. Relation of substantia nigra to superior colliculus. J. Neurophysiol., 49, 1285-1301.
17. Horwitz, G.D. & Newsome, W.T. (2001) Target selection for saccadic eye movements: prelude activity in the superior colliculus during a direction-discrimination task. J. Neurophysiol., 86, 2543-2558.
18. Isa, T. & Hall, W.C. (2009) Exploring the superior colliculus in vitro. J. Neurophysiol., 102, 2581-2593.
19. Isa, T. & Saito, Y. (2001) The direct visuo-motor pathway in mammalian superior colliculus; novel perspective on the interlaminar connection. Neurosci. Res., 41, 107-113.
20. Isa, T., Endo, T. & Saito, Y. (1998) The visuo-motor pathway in the local circuit of the rat superior colliculus. J. Neurosci., 18, 8496-8504.
21. Itti, L. & Koch, C. (2001) Computational modelling of visual attention. Nat. Rev. Neurosci., 2, 194-203.
22. Kaneda, K., Isa, K., Yanagawa, Y. & Isa, T. (2008) Nigral inhibition of GABAergic neurons in mouse superior colliculus. J. Neurosci., 28, 11071-11078.
23. + conductance: a study using glutamate decarboxylase 67-green fluorescent protein knock-in mice. Neuroscience, 157, 781-797.
24. Krauzlis, R.J., Lovejoy, L.P. & Zénon, A. (2013) Superior colliculus and visual spatial attention. Annu. Rev. Neurosci., 36, 165-182.
25. Langer, T.P. & Lund, R.D. (1974) The upper layers of the superior colliculus of the rat: a Golgi study. J. Comp. Neurol., 158, 418-435.
26. Lee, P. & Hall, W.C. (2006) An in vitro study of horizontal connections in the intermediate layer of the superior colliculus. J. Neurosci., 26, 4763-4768.
27. Lee, C., Rohrer, W.H. & Sparks, D.L. (1988) Population coding of saccadic eye movements by neurons in the superior colliculus. Nature, 332, 357-360.
28. Lee, P.H., Helms, M.C., Augustine, G.J. & Hall, W.C. (1997) Role of intrinsic synaptic circuitry in collicular sensorimotor integration. Proc. Natl. Acad. Sci. USA, 94, 13299-13304.
29. Lee, P.H., Sooksawate, T., Yanagawa, Y., Isa, K., Isa, T. & Hall, W.C. (2007) Identity of a pathway for saccadic suppression. Proc. Natl. Acad. Sci. USA, 104, 6824-6827.
30. Marino, R.A., Trappenberg, T.P., Dorris, M.C. & Munoz, D.P. (2012) Spatial interactions in the superior colliculus predict saccade behavior in a neural field model. J. Cognitive Neurosci., 24, 315-336.
31. May, P.J. & Hall, W.C. (1984) Relationships between the nigrotectal pathway and the cells of origin of the predorsal bundle. J. Comp. Neurol., 226, 357-376.
32. Meredith, M.A. & Ramoa, A.S. (1998) Intrinsic circuitry of the superior colliculus: pharmacophysiological identification of horizontally oriented inhibitory interneurons. J. Neurophysiol., 79, 1597-1602.
33. Mize, R.R. (1992) The organization of GABAergic neurons in the mammalian superior colliculus. Prog. Brain Res., 90, 219-248.
34. Mize, R.R., Whitworth, R.H., Nunes-Cardozo, B. & van der Want, J. (1994) Ultrastructural organization of GABA in the rabbit superior colliculus revealed by quantitative postembedding immunocytochemistry. J. Comp. Neurol., 341, 273-287.
35. Munoz, D.P. & Istvan, P.J. (1998) Lateral inhibitory interactions in the intermediate layers of the monkey superior colliculus. J. Neurophysiol., 79, 1193-1209.
36. Mysore, S.P. & Knudsen, E.I. (2011) The role of a midbrain network in competitive stimulus selection. Curr. Opin. Neurobiol., 21, 653-660.
37. Olivier, E., Corvisier, J., Pauluis, Q. & Hardy, O. (2000) Evidence for glutaminergic tectotectal neurons in the cat superior colliculus: a comparison with GABAergic tectotectal neurons. Eur. J. Neurosci., 12, 2354-2366.
38. Phongphanphanee, P., Kaneda, K. & Isa, T. (2008) Spatiotemporal profiles of field potentials in mouse superior colliculus analyzed by multichannel recording. J. Neurosci., 28, 9309-9318.
39. Ratcliff, R., Cherian, A. & Segraves, M. (2003) A comparison of macaque behavior and superior colliculus neuronal activity to predictions from models of two-choice decisions. J. Neurophysiol., 90, 1392-1407.
40. Robinson, D.A. (1972) Eye movements evoked by collicular stimulation in the alert monkey. Vision Res., 12, 1795-1808.
41. Saito, Y. & Isa, T. (2003) Local excitatory network and NMDA receptor activation generate a synchronous and non-linear bursting command from the superior colliculus. J. Neurosci., 23, 5854-5864.
42. Schiller, P.H. & Stryker, M. (1972) Single-unit recording and stimulation in superior colliculus of the alert rhesus monkey. J. Neurophysiol., 35, 915-924.
43. Sooksawate, T., Saito, Y. & Isa, T. (2005) Electrophysiological and morphological properties of identified crossed tecto-reticular neurons in the rat superior colliculus. Neurosci. Res., 52, 174-184.
44. Sooksawate, T., Isa, K., Behan, M., Yanagawa, Y. & Isa, T. (2011) Organization of GABAergic inhibition in the motor output layer of the superior colliculus. Eur. J. Neurosci., 33, 421-432.
45. Sparks, D.L. (1986) Translation of sensory signals into commands for control of saccadic eye movements: role of primate superior colliculus. Physiol. Rev., 66, 118-171.
46. Sparks, D.L. (2002) The brainstem control of saccadic eye movements. Nat. Rev. Neurosci., 3, 952-964.
47. Takahashi, M., Sugiuchi, Y. & Shinoda, Y. (2007) Commissural mirror-symmetric excitation and reciprocal inhibition between the two superior colliculi and their roles in vertical and horizontal eye movements. J. Neurophysiol., 98, 2664-2682.
48. Tamamaki, N., Uhlrich, D.J. & Sherman, S.M. (1995) Morphology of physiologically identified retinal X and Y axons in the cat's thalamus and midbrain as revealed by intraaxonal injection of biocytin. J. Comp. Neurol., 354, 583-607.
49. Tamamaki, N., Yanagawa, Y., Tomioka, R., Miyazaki, J., Obata, K. & Kaneko, T. (2003) Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J. Comp. Neurol., 467, 60-79.
50. Trappenberg, T.P., Dorris, M.C., Munoz, D.P. & Klein, R.M. (2001) A model of saccade initiation based on the competitive integration of exogenous and endogenous signals in the superior colliculus. J. Cognitive Neurosci., 13, 256-271.
51. Vokoun, C.R., Jackson, M.B. & Basso, M.A. (2010) Intralaminar and interlaminar activity within the rodent superior colliculus visualized with voltage imaging. J. Neurosci., 30, 10667-10682.
52. Vokoun, C.R., Jackson, M.B. & Basso, M.A. (2011) Circuit dynamics of the superior colliculus revealed by in vitro voltage imaging. Ann. NY Acad. Sci., 1233, 41-47.
53. White, B.J. & Munoz, D.P. (2011) Separate visual signals for saccade initiation during target selection in the primate superior colliculus. J. Neurosci., 31, 1570-1578.
54. Yarbus, I.A. (1967) Eye Movements and Vision. Plenum Press, New York.