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Response properties of visual neurons in the turtle nucleus isthmi

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Abstract

The optic tectum holds a central position in the tectofugal pathway of non-mammalian species and is reciprocally connected with the nucleus isthmi. Here, we recorded from individual nucleus isthmi pars parvocellularis (Ipc) neurons in the turtle eye-attached whole-brain preparation in response to a range of computer-generated visual stimuli. Ipc neurons responded to a variety of moving or flashing stimuli as long as those stimuli were small. When mapped with a moving spot, the excitatory receptive field was of circular Gaussian shape with an average half-width of less than 3°. We found no evidence for directional sensitivity. For moving spots of varying sizes, the measured Ipc response-size profile was reproduced by the linear Difference-of-Gaussian model, which is consistent with the superposition of a narrow excitatory center and an inhibitory surround. Intracellular Ipc recordings revealed a strong inhibitory connection from the nucleus isthmi pars magnocellularis (Imc), which has the anatomical feature to provide a broad inhibitory projection. The recorded Ipc response properties, together with the modulatory role of the Ipc in tectal visual processing, suggest that the columns of Ipc axon terminals in turtle optic tectum bias tectal visual responses to small dark changing features in visual scenes.

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Abbreviations

ACh:

Acetylcholine

GABA:

Gamma-aminobutyric acid

Imc:

Isthmi pars magnocellularis

Ipc:

Isthmi pars parvocellularis

PBN:

Parabigeminal nucleus

RGC:

Retinal ganglion cell

SFGS:

Stratum fibrosum et griseum superficiale

SGC:

Stratum griseum centrale

SGP:

Stratum griseum periventriculare

References

  • Alitto HJ, Usrey WM (2003) Corticothalamic feedback and sensory processing. Curr Opin Neurobiol 13:440–445

    Article  CAS  PubMed  Google Scholar 

  • Ariel M, Kogo N (2001) Direction tuning of inhibitory inputs to the turtle accessory optic system. J Neurophysiol 86:2919–2930

    CAS  PubMed  Google Scholar 

  • Belekova M, Kenigfest N, Rio JP, Reperant J, Ward R, Vesselkin N, Karamian O (2003) Tectothalamic visual projections in turtles: their cells of origin revealed by tracing methods. J Comp Neurology 457:37–56

    Article  Google Scholar 

  • Bowling DB (1980) Light responses of ganglion cells in the retina of the turtle. J Physiol 299:173–196

    CAS  PubMed  Google Scholar 

  • Brown KT (1969) A linear area centralis extending across the turtle retina and stabilized to the horizon by non-visual cues. Vis Res 9:1053–1062

    Article  CAS  PubMed  Google Scholar 

  • Caudill MS, Eggebrecht AT, Gruberg ER, Wessel R (2010) Electrophysiological properties of isthmic neurons in frogs revealed by in vitro and in vivo studies. J Comp Physiol A 196:249–262

    Article  Google Scholar 

  • Cui H, Malpeli JG (2003) Activity in the parabigeminal nucleus during eye movements directed at moving and stationary targets. J Neurophysiol 89:3128–3142

    Article  PubMed  Google Scholar 

  • DeAngelis GC, Freeman RD, Ohzawa I (1994) Length and width tuning of neurons in the cat’s primary visual cortex. J Neurophysiol 71:347–374

    CAS  PubMed  Google Scholar 

  • Desan PH, Gruberg ER, Eckenstein F (1984) A cholinergic projection from the nucleus isthmi to the optic tectum in turtle and frog. Proc Soc Neurosci 10:575 (abstract)

    Google Scholar 

  • Druckmann S, Berger TK, Hill S, Schürmann F, Markram H, Segev I (2008) Evaluating automated parameter constraining procedures of neuron models by experimental and surrogate data. Biol Cybern 99:371–379

    Article  PubMed  Google Scholar 

  • Dudkin EA, Gruberg ER (2003) Nucleus isthmi enhances calcium influx into optic nerve fiber terminals in Rana pipiens. Brain Res 969:44–52

    Article  CAS  PubMed  Google Scholar 

  • Dudkin EA, Sheffield JB, Gruberg ER (2007) Combining visual information from the two eyes: the relationship between isthmotectal cells that project to ipsilateral and to contralateral optic tectum using fluorescent retrograde labels in the frog, Rana pipiens. J Comp Neurol 502:38–54

    Article  PubMed  Google Scholar 

  • Gallagher SP, Northmore DP (2006) Responses of the teleostean nucleus isthmi to looming objects and other moving stimuli. Vis Neurosci 23:209–219

    Article  PubMed  Google Scholar 

  • Goddard CA, Knudsen EI, Huguenard JR (2007) Intrinsic excitability of cholinergic neurons in the rat parabigeminal nucleus. J Neurophysiol 98:3486–3493

    Article  PubMed  Google Scholar 

  • Granda AM, Fulbrook JE (1989) Classification of turtle retinal ganglion cells. J Neurophysiol 62:723–737

    CAS  PubMed  Google Scholar 

  • Graybiel AM (1978) A satellite system of the superior colliculus: the parabigeminal nucleus and its projection to the superficial collicular layers. Brain Res 145:365–374

    Article  CAS  PubMed  Google Scholar 

  • Gruberg ER, Udin SB (1978) Topographic projections between the nucleus isthmi and the tectum of the frog, Rana pipiens. J Comp Neurol 179:487–500

    Article  CAS  PubMed  Google Scholar 

  • Gruberg ER, Dudkin EA, Wang Y, Marin G, Salas C, Sentis E, Letelier JC, Mpodozis J, Malpeli J, Cui H, Ma R, Northmore D, Udin S (2006) Influencing and interpreting visual input: the role of a visual feedback system. J Neurosci 26:10368–10371

    Article  CAS  PubMed  Google Scholar 

  • Hall WC, Fitzpatrcik D, Klatt LL, Raczkowski D (1989) Cholinergic innervation of the superior colliculus in the cat. J Comp Neurol 287:495–514

    Article  CAS  PubMed  Google Scholar 

  • Kriegstein AR (1987) Synaptic responses of cortical pyramidal neurons to light stimulation in the isolated turtle visual system. J Neurosci 7:2488–2492

    CAS  PubMed  Google Scholar 

  • Kunzle H, Schnyder H (1984) The isthmus-tegmentum complex in the turtle and rat: a comparative analysis of its interconnections with the optic tectum. Exp Brain Res 56:509–522

    Article  CAS  PubMed  Google Scholar 

  • Li DP, Xiao Q, Wang SR (2007) Feedforward construction of the receptive field and orientation selectivity of visual neurons in the pigeon. Cereb Cortex 17:885–893

    Article  CAS  PubMed  Google Scholar 

  • Lucas-Meunier E, Fossier P, Baux G, Amar M (2003) Cholinergic modulation of the cortical neuronal network. Eur J Physiol 446:17–29

    CAS  Google Scholar 

  • Lucas-Meunier E, Monier C, Amar M, Baux G, Fregnac Y, Fossier P (2009) Involvement of nicotinic and muscarinic receptors in the endogenous cholinergic modulation of the balance between excitation and inhibition in the young rat visual cortex. Cereb Cortex 19:2411–2427

    Article  PubMed  Google Scholar 

  • Maczko KA, Knudsen PF, Knudsen EI (2006) Auditory and visual space maps in the cholinergic nucleus isthmi pars parvocellularis of the barn owl. J Neurosci 26:12799–12806

    Article  CAS  PubMed  Google Scholar 

  • Marín G, Mpodozis J, Sentis E, Ossandón T, Letelier JC (2005) Oscillatory bursts in the optic tectum of birds represent re-entrant signals from the nucleus isthmi pars parvocellularis. J Neurosci 25:7081–7089

    Article  PubMed  Google Scholar 

  • Marín G, Salas C, Sentis E, Rojas X, Letelier JC, Mpodozis JA (2007) Cholinergic gating mechanism controlled by competitive interactions in the optic tectum of the pigeon. J Neurosci 27:8112–8121

    Article  PubMed  Google Scholar 

  • McCormick DA (1993) Actions of acetylcholine in the cerebral cortex and thalamus and implications for functions. Prog Brain Res 98:303–308

    Article  CAS  PubMed  Google Scholar 

  • Medina L, Reiner A (1994) Distribution of choline acetyltransferase immunoreactivity in the pigeon brain. J Comp Neurol 342:497–537

    Article  CAS  PubMed  Google Scholar 

  • Metherate R (2004) Nicotinic acetylcholine receptors in sensory cortex. Learn Mem 11:50–59

    Article  PubMed  Google Scholar 

  • Mysore SP, Asadollahi A, Knudsen EI (2010) Global inhibition and stimulus competition in the owl optic tectum. J Neurosci 30:1727–1738

    Article  CAS  PubMed  Google Scholar 

  • Northmore DP (1991) Visual responses of nucleus isthmi in a teleost fish (Lepomis macrochirus). Vision Res 31:525–535

    Article  CAS  PubMed  Google Scholar 

  • Northmore DP, Gallagher SP (2003) Functional relationship between nucleus isthmi and tectum in teleosts: synchrony but no topography. Vis Neurosci 20:335–348

    Article  PubMed  Google Scholar 

  • Northmore DP, Granda AM (1991) Ocular dimensions and schematic eyes of freshwater and sea turtles. Vis Neurosci 7:627–635

    Article  CAS  PubMed  Google Scholar 

  • Peirce JW (2008) Generating stimuli for neuroscience using PsychoPy. Front Neuroinformatics 2:10

    PubMed  Google Scholar 

  • Powers AS, Reiner A (1993) The distribution of cholinergic neurons in the central nervous system of turtles. Brain Behav Evol 41:326–345

    Article  CAS  PubMed  Google Scholar 

  • Quiroga RQ, Nadasdy Z, Ben-Shaul Y (2004) Unsupervised spike detection and sorting with wavelets and superparamagnetic clustering. Neural Comput 16:1661–1687

    Article  PubMed  Google Scholar 

  • Reiner A (1994) Laminar distribution of the cells of origin of ascending and descending tectofugal pathways in turtles: implications for the evolution of tectal lamination. Brain Beh Evol 43:254–292

    Article  CAS  Google Scholar 

  • Rodieck RW (1965) Quantitative analysis of cat retinal ganglion cell response to visual stimuli. Vision Res 5:583–601

    Article  CAS  PubMed  Google Scholar 

  • Rosenberg AF, Ariel M (1990) Visual-response properties of neurons in turtle basal optic nucleus in vitro. J Neurophysiol 63:1033–1045

    CAS  PubMed  Google Scholar 

  • Rosenberg AF, Ariel M (1991) Electrophysiological evidence for a direct projection of direction-sensitive retinal ganglion cells to the turtle’s accessory optic system. J Neurophysiol 65:1022–1033

    CAS  PubMed  Google Scholar 

  • Sato H, Katsuyama N, Tamura H, Hata Y, Tsumoto T (1995) Mechanisms underlying direction selectivity of neurons in the primary visual cortex of the macaque. J Neurophysiol 74:1382–1394

    CAS  PubMed  Google Scholar 

  • Sceniak MP, Ringach DL, Hawken MJ, Shapley R (1999) Contrast’s effect on spatial summation by macaque V1 neurons. Nat Neurosci 2:733–739

    Article  CAS  PubMed  Google Scholar 

  • Schechter Pb, Ulinski PS (1979) Interactions between tectal radial cells in the red-eared turtle, Pseudemys scripta Elegans: an analysis of tectal modules. J Morph 162:17–36

    Article  CAS  PubMed  Google Scholar 

  • Sereno MI, Ulinski PS (1987) Caudal topographic nucleus isthmi and the rostral nontopographic nucleus isthmi in the turtle, Pseudemys scripta. J Comp Neurol 261:319–346

    Article  CAS  PubMed  Google Scholar 

  • Sherk H (1978) Visual response properties and visual field topography in the cat’s parabigeminal nucleus. Brain Res 145:375–379

    Article  CAS  PubMed  Google Scholar 

  • Sherk H (1979a) A comparison of visual-response properties in cat’s parabigeminal nucleus and superior colliculus. J Neurophysiol 42:1640–1655

    CAS  PubMed  Google Scholar 

  • Sherk H (1979b) Connections and visual field mapping in cat’s tectoparabigeminal circuit. J Neurophysiol 42:1656–1668

    CAS  PubMed  Google Scholar 

  • Sillito AM, Jones HE (2002) Corticothalamic interactions in the transfer of visual information. Philos Trans R Soc Lond B Biol Sci 357:1739–1752

    Article  PubMed  Google Scholar 

  • Sorenson EM, Parkinson D, Dahl JL, Chiappinelli VA (1989) Immunohistochemical localization of choline acetyltransferase in the chicken mesencephalon. J Comp Neurol 281:641–657

    Article  CAS  PubMed  Google Scholar 

  • Wang SR (2003) The nucleus isthmi and dual modulation of the receptive field of tectal neurons in non-mammals. Brain Res Rev 41:13–25

    Article  CAS  PubMed  Google Scholar 

  • Wang YC, Frost BJ (1991) Visual response characteristics of neurons in the nucleus isthmi magnocellularis and nucleus isthmi parvocellularis of pigeons. Exp Brain Res 87:624–633

    Article  CAS  PubMed  Google Scholar 

  • Wang SR, Yan K, Wang YT, Jiang SY, Wang XS (1983) Neuroanatomy and electrophysiology of the lacertilian nucleus isthmi. Brain Res 275:355–360

    Article  CAS  PubMed  Google Scholar 

  • Wang SR, Wang YC, Frost BJ (1995) Magnocellular and parvocellular divisions of pigeon nucleus isthmi differentially modulate visual responses in the tectum. Exp Brain Res 104:376–384

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Xiao J, Wang SR (2000) Excitatory and inhibitory receptive fields of tectal cells are differentially modified by magnocellular and parvocellular divisions of the pigeon nucleus isthmi. J Comp Physiol A 186:505–511

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Major DE, Karten HJ (2004) Morphology and connections of nucleus isthmi pars magnocellularis in chicks (Gallus gallus). J Comp Neurol 469:275–297

    Article  PubMed  Google Scholar 

  • Wang Y, Luksch H, Brecha NC, Karten HJ (2006) Columnar projections from the cholinergic nucleus isthmi to the optic tectum in chicks (Gallus gallus): a possible substrate for synchronizing tectal channels. J Comp Neurol 494:7–35

    Article  PubMed  Google Scholar 

  • Wiggers W, Roth G (1991) Anatomy, neurophysiology and functional aspects of the nucleus isthmi in salamanders of the family Plethodontidae. J Comp Physiol A 169:165–176

    Article  Google Scholar 

  • Winkowski DE, Gruberg ER (2002) The representation of the ipsilateral eye in nucleus isthmi of the leopard frog, Rana pipiens. Vis Neurosci 19:669–679

    Article  PubMed  Google Scholar 

  • Yan K, Wang SR (1986) Visual responses of neurons in the avian nucleus isthmi. Neurosci Lett 64:340–344

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was supported by National Eye Institute Grant R01 EY-18818 to R. Wessel. We thank Matthew Caudill for critical reading of early versions of the manuscript. All surgical procedures used in this study were approved by the Washington University Institutional Animal Care and Use Committee and conform to the guidelines of the National Institutes of Health on the Care and Use of Laboratory Animals.

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Correspondence to Debajit Saha.

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Saha, D., Morton, D., Ariel, M. et al. Response properties of visual neurons in the turtle nucleus isthmi. J Comp Physiol A 197, 153–165 (2011). https://doi.org/10.1007/s00359-010-0596-3

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  • DOI: https://doi.org/10.1007/s00359-010-0596-3

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