Back
 JBM  Vol.5 No.8 , August 2017
Development of Functional Interlaminar Pathways in the Mouse Superior Colliculus Revealed by Optical Imaging with Axonal Labeling
Abstract: The superior colliculus (SC) is a laminated midbrain structure responsible for visual orientation behaviors. In the mature SC, neurons in the stratum griseum superficiale (SGS) receive visual inputs that contribute to exciting premotor neurons in the stratum griseum intermediale (SGI) through a dorsoventral pathway. SGI activation generates feedback signals to the SGS through a ventrodorsal pathway. However, the developmental changes in signal transmission within the SC around the time of eye opening are not yet well understood. We compared the functional connections between the SGS and SGI before and after eye opening by imaging the neuronal population responses using a voltage-sensitive absorption dye in mouse SC slices. Electrophoresis of a fluorescent dye from the stimulating electrodes was used to fill the cells in the stimulated site. We here show that the dorsoventral transmission is present both before and after eye opening. This is in contrast to our previous finding that the ventrodorsal transmission develops after eye opening. Functions of intrinsic inhibitory systems mediated by gamma-aminobutyric acid were also investigated with the antagonist. The processes stained by electrophoresis from stimulating electrodes before eye opening were confined within the respective stimulated layers. Whereas, after eye opening, the processes were widely extended especially dorsoventrally and ventrodorsally invading the SGI and SGS, respectively. These corresponded well to the early component of voltage responses that is known to reflect the activation of presynaptic elements, presumably the axonal arborizations and varicosities. Thus, the optically-revealed functional connections between the SGS and SGI were correlated to the morphology.
Cite this paper: Morita, N. , Ito, T. , Hasegawa, R. and Murase, K. (2017) Development of Functional Interlaminar Pathways in the Mouse Superior Colliculus Revealed by Optical Imaging with Axonal Labeling. Journal of Biosciences and Medicines, 5, 11-35. doi: 10.4236/jbm.2017.58002.
References

[1]   Cynader, M. and Berman, N. (1972) Receptive-Field Organization of Monkey Superior Colliculus. Journal of Neurophysiology, 35, 187-201.

[2]   May, P.J. (2006) The Mammalian Superior Colliculus: Laminar Structure and Connections. Progress in Brain Research, 151, 321-378.
https://doi.org/10.1016/S0079-6123(05)51011-2

[3]   Schiller, P.H. and Stryker, M. (1972) Single-Unit Recording and Stimulation in Superior Colliculus of the Alert Rhesus Monkey. Journal of Neurophysiology, 35, 915-924.

[4]   Doubell, T.P., Skaliora, I., Baron, J. and King, A.J. (2003) Functional Connectivity between the Superficial and Deeper Layers of the Superior Colliculus: An Anatomical Substrate for Sensorimotor Integration. Journal of Neurophysiology, 23, 6596-6607.

[5]   Hasegawa, R.P., Hasegawa, Y.T. and Segraves, M.A. (2009) Neural Mind Reading of Multi-Dimensional Decisions by Monkey Mid-Brain Activity. Neural Networks, 22, 1247-1256.
https://doi.org/10.1016/j.neunet.2009.07.028

[6]   Helms, M.C., Ozen, G. and Hall, W.C. (2004) Organization of the Intermediate Gray Layer of the Superior Colliculus. I. Intrinsic Vertical Connections. Journal of Neurophysiology, 91, 1706-1715.
https://doi.org/10.1152/jn.00705.2003

[7]   Ratcliff, R., Hasegawa, Y.T., Hasegawa, R.P., Smith, P.L. and Segraves, M.A. (2007) Dual Diffusion Model for Single-Cell Recording Data from the Superior Colliculus in a Brightness-Discrimination Task. Journal of Neurophysiology, 97, 1756-1774.
https://doi.org/10.1152/jn.00393.2006

[8]   Sparks, D.L. (1986) Translation of Sensory Signals into Commands for Control of Saccadic Eye Movements: Role of Primate Superior Colliculus. Physiological Reviews, 66, 118-171.

[9]   Tehovnik, E.J. (1989) Head and Body Movements Evoked Electrically from the Caudal Superior Colliculus of Rats: Pulse Frequency Effects. Behavioural Brain Research, 34, 71-78.
https://doi.org/10.1016/S0166-4328(89)80091-9

[10]   Fischer, B. and Boch, R. (1983) Saccadic Eye Movements after Extremely Short Reaction Times in the Monkey. Brain Research, 260, 21-26.
https://doi.org/10.1016/0006-8993(83)90760-6

[11]   Higashi, S., Crair, M.C., Kurotani, T., Inokawa, H. and Toyama, K. (1999) Altered Spatial Patterns of Functional Thalamocortical Connections in the Barrel Cortex after Neonatal Infraorbital Nerve Cut Revealed by Optical Recording. Neuroscience, 91, 439-452.
https://doi.org/10.1016/S0306-4522(98)00666-6

[12]   Isa, T., Endo, T. and Saito, Y. (1998) The Visuo-Motor Pathway in the Local Circuit of the Rat Superior Colliculus. Journal of Neurophysiology, 18, 8496-8504.

[13]   Ghitani, N., Bayguinov, P.O., Vokoun, C.R., McMahon, S., Jackson, M.B. and Basso, M.A. (2014) Excitatory Synaptic Feedback from the Motor Layer to the Sensory Layers of the Superior Colliculus. Journal of Neurophysiology, 34, 6822-6833.
https://doi.org/10.1523/JNEUROSCI.3137-13.2014

[14]   Lee, P.H., Sooksawate, T., Yanagawa, Y., Isa, K., Isa, T. and Hall, W.C. (2007) Identity of a Pathway for Saccadic Suppression. Proceedings of the National Academy of Sciences of the United States of America, 104, 6824-6827.
https://doi.org/10.1073/pnas.0701934104

[15]   Cork, R.J., Calhoun, T., Perrone, M. and Mize, R.R. (2000) Postnatal Development of Nitric Oxide Synthase Expression in the Mouse Superior Colliculus. The Journal of Comparative Neurology, 427, 581-592.
https://doi.org/10.1002/1096-9861(20001127)427:4<581::AID-CNE6>3.0.CO;2-M

[16]   King, A.J., Schnupp, J.W. and Thompson, I.D. (1998) Signals from the Superficial Layers of the Superior Colliculus Enable the Development of the Auditory Space Map in the Deeper Layers. The Journal of Neuroscience, 18, 9394-9408.

[17]   Mohler, C.W. and Wurtz, R.H. (1976) Organization of Monkey Superior Colliculus: Intermediate Layer Cells Discharging before Eye Movements. Journal of Neurophysiology, 39, 722-744.

[18]   Morita, N., Hasegawa, R.P., Murase, K. and Ikeda, H. (2014) Development of a Neural Circuit in the Superior Colliculus: Analysis of the Propagation of Neuronal Excitation from Intermediate to Superficial Layers. Neuroreport, 25, 242-247.
https://doi.org/10.1097/WNR.0000000000000081

[19]   Rochefort, N.L., Narushima, M., Grienberger, C., Marandi, N., Hill, D.N. and Konnerth, A. (2011) Development of Direction Selectivity in Mouse Cortical Neurons. Neuron, 71, 425-432.
https://doi.org/10.1016/j.neuron.2011.06.013

[20]   Vokoun, C.R., Jackson, M.B. and Basso, M.A. (2010) Intralaminar and Interlaminar Activity within the Rodent Superior Colliculus Visualized with Voltage Imaging. The Journal of Neuroscience, 30, 10667-10682.
https://doi.org/10.1523/JNEUROSCI.1387-10.2010

[21]   Ben-Ari, Y. (2002) Excitatory Actions of Gaba during Development: The Nature of the Nurture. Nature Reviews Neuroscience, 3, 728-739.
https://doi.org/10.1038/nrn920

[22]   Choen, L.B. and Lesher, S. (1986) Optical Monitoring of Membrane Potential: Methods of Multisite Optical Measurement. In: De Weer, P. and Saltzberg, B.M., Eds., Optical Methods in Cell Physiology, Wiley, New York, 71-99.

[23]   Grinvald, A., Frosting, R.D., Lieke, E. and Hildesheim, R. (1988) Optical Imaging of Neuronal Activity. Physiological Reviews, 68, 1285-1366.

[24]   Ikeda, H., Ryu, P.D., Park, J.B., Tanifuji, M., Asai, T. and Murase, K. (1998) Optical Responses Evoked by Single-Pulse Stimulation to the Dorsal Root in the Rat Spinal Dorsal Horn in Slice. Brain Research, 812, 81-90.
https://doi.org/10.1016/S0006-8993(98)00928-7

[25]   Kiritoshi, T., Ikeda, H. and Murase, K. (2010) Long-Term Potentiation of Neuronal Excitation in the Central Nucleus of the Rat Amygdala Revealed by Imaging with a Voltage-Sensitive Dye. Brain Research, 1349, 32-40.
https://doi.org/10.1016/j.brainres.2010.06.039

[26]   Salzberg, B.M. (1983) Optical Recording of Electrical Activity in Neurons Using Molecular Probes. In: Barker, J. and Mckelvey, J., Eds., Current Methods in Cellular Neurobiology, Wiley, New York, 139-187.

[27]   Pettit, D.L., Helms, M.C., Lee, P., Augustine, G.J. and Hall, W.C. (1999) Local Excitatory Circuits in the Intermediate Gray Layer of the Superior Colliculus. The Journal of Neuroscience, 81, 1424-1427.

[28]   Paxinos, G. and Franklin, K.B.J. (2001) The Mouse Brain in Stereotaxic Coordinates. 2nd Edition, Academic Press, San Diego.

[29]   Ikeda, H. and Murase, K. (2004) Glial Nitric Oxide-Mediated Long-Term Presynaptic Facilitation Revealed by Optical Imaging in Rat Spinal Dorsal Horn. The Journal of Neuroscience, 24, 9888-9896.
https://doi.org/10.1523/JNEUROSCI.2608-04.2004

[30]   Kita, H., Yamada, H., Tanifuji, M. and Murase, K. (1995) Optical Responses Recorded after Local Stimulation in Rat Neostriatal Slice Preparations: Effets of GABA Antagonists, Glutamate Antagonists, and Dopamine Agonists. Experimental Brain Research, 106, 187-195.
https://doi.org/10.1007/BF00241114

[31]   Kusudo, K., Asai, T., Ikeda, H., Takenoshita, M. and Murase, K. (2003) Inhibitory Effect of Caffeine on C-Fibre-Evoked Excitation in the Rat Spinal Dorsal Horn Recorded under Ca2+-Free Condition: An Interaction with Halothane. Neuroscience Letters, 336, 17-20.
https://doi.org/10.1016/S0304-3940(02)01198-9

[32]   Chang, S.L., LoTurco, J.J. and Nisenbaum, L.K. (2000) In Vitro Biocytin Injection into Perinatal Mouse Brain: A Method for Tract Tracing in Developing Tissue. Journal of Neuroscience Methods, 97, 1-6.
https://doi.org/10.1016/S0165-0270(99)00190-9

[33]   Hama, H., Hioki, H., Namiki, K., Hoshida, T., Kurokawa, H., Ishidate, F., Kaneko, T., Akagi, T., Saito, T., Saido, T. and Miyawaki, A. (2015) ScaleS: An Optical Clearing Palette for Biological Imaging. Nature Neuroscience, 18, 1518-1529.
https://doi.org/10.1038/nn.4107

[34]   Mize, R.R. and Butler, G.D. (1997) The Distribution of the GABA (A) Beta2, Beta3 Subunit Receptor in the Cat Superior Colliculus Using Antibody Immunocytochemistry. Neuroscience, 79, 1121-1135.
https://doi.org/10.1016/S0306-4522(96)00667-7

[35]   Sugitani, M., Sugai, T., Tanifuji, M., Murase, K. and Onoda, N. (1994) Optical Imaging of the in vitro Guinea Pig Piriform Cortex Activity Using a Voltage-Sensitive Dye. Neuroscience Letters, 165, 215-218.
https://doi.org/10.1016/0304-3940(94)90748-X

[36]   Tanifuji, M., Sugiyama, T. and Murase, K. (1994) Horizontal Propagation of Excitation in Rat Visual Cortical Slices Revealed by Optical Imaging. Science, 266, 1057- 1059.
https://doi.org/10.1126/science.7973662

[37]   Ichikawa, M., Iijima, T. and Matsumoto, G. (1993) Real-Time Optical Recording of Neuronal Activity in the Brain. In: Ono, T., Squire, L.R., Raichle, M.E., Perrett, D.I. and Fukuda, M., Eds., Brain Mechanisms of Perception and Memory, Oxford U.P., New York, 638-648.

[38]   Pinault, D. (1996) A Novel Single-Cell Staining Procedure Performed in vivo under Electrophysiological Control: Morpho-Functional Features of Juxtacellularly Labeled Thalamic Cells and Other Central Neurons with Biocytin or Neurobiotin. Journal of Neuroscience Methods, 65, 113-136.
https://doi.org/10.1016/0165-0270(95)00144-1

[39]   Warton, S.S. and Jones, D.G. (1985) Postnatal Development of the Superficial Layers in the Rat Superior Colliculus: A Study with Golgi-Cox and Kluver-Barrera Techniques. Experimental Brain Research, 58, 490-502.
https://doi.org/10.1007/BF00235865

[40]   Behan, M. and Appell, P.P. (1992) Intrinsic Circuitry in the Cat Superior Colliculus: Projections from the Superficial Layers. The Journal of Comparative Neurology, 315, 230-243.
https://doi.org/10.1002/cne.903150209

[41]   Lee, P. and Hall, W.C. (1995) Interlaminar Connections of the Superior Colliculus in the Tree Shrew. II: Projections from the Superficial Gray to the Optic Layer. Visual Neuroscience, 12, 573-588.
https://doi.org/10.1017/S0952523800008464

[42]   Lee, P.H., Helms, M.C., Augustine, G.J. and Hall, W.C. (1997) Role of Intrinsic Synaptic Circuitry in Collicular Sensorimotor Integration. Proceedings of the National Academy of Sciences of the United States of America, 94, 13299-13304.
https://doi.org/10.1073/pnas.94.24.13299

[43]   Lee, P.H., Schmidt, M. and Hall, W.C. (2001) Excitatory and Inhibitory Circuitry in the Superficial Gray Layer of the Superior Colliculus. The Journal of Neuroscience, 21, 8145-8153.

[44]   Mooney, R.D., Nikoletseas, M.M., Hess, P.R., Allen, Z., Lewin, A.C. and Rhoades, R.W. (1988) The Projection from the Superficial to the Deep Layers of the Superior Colliculus: An Intracellular Horseradish Peroxidase Injection Study in the Hamster. The Journal of Neuroscience, 8, 1384-1399.

[45]   Endo, T., Yanagawa, Y., Obata, K. and Isa, T. (2003) Characteristics of GABAergic Neurons in the Superficial Superior Colliculus in Mice. Neuroscience Letters, 346, 81-84.
https://doi.org/10.1016/S0304-3940(03)00570-6

[46]   Furman, M., Xu, H.P. and Crair, M.C. (2013) Competition Driven by Retinal Waves Promotes Morphological and Functional Synaptic Development of Neurons in the Superior Colliculus. Journal of Neurophysiology, 110, 1441-1454.
https://doi.org/10.1152/jn.01066.2012

[47]   Mize, R.R. (1992) The Organization of GABAergic Neurons in the Mammalian Superior Colliculus. Progress in Brain Research, 90, 219-248.
https://doi.org/10.1016/S0079-6123(08)63616-X

[48]   Okada, Y. (1992) The Distribution and Function of Gamma-Aminobutyric Acid (GABA) in the Superior Colliculus. Progress in Brain Research, 90, 249-262.
https://doi.org/10.1016/S0079-6123(08)63617-1

[49]   Tsunekawa, N., Yanagawa, Y. and Obata, K. (2005) Development of GABAergic Neurons from the Ventricular Zone in the Superior Colliculus of the Mouse. Journal of Neuroscience Research, 51, 243-251.
https://doi.org/10.1016/j.neures.2004.11.011

 
 
Top