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.
Similar content being viewed by others
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
Ariel M, Kogo N (2001) Direction tuning of inhibitory inputs to the turtle accessory optic system. J Neurophysiol 86:2919–2930
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
Bowling DB (1980) Light responses of ganglion cells in the retina of the turtle. J Physiol 299:173–196
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
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
Cui H, Malpeli JG (2003) Activity in the parabigeminal nucleus during eye movements directed at moving and stationary targets. J Neurophysiol 89:3128–3142
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
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)
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
Dudkin EA, Gruberg ER (2003) Nucleus isthmi enhances calcium influx into optic nerve fiber terminals in Rana pipiens. Brain Res 969:44–52
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
Gallagher SP, Northmore DP (2006) Responses of the teleostean nucleus isthmi to looming objects and other moving stimuli. Vis Neurosci 23:209–219
Goddard CA, Knudsen EI, Huguenard JR (2007) Intrinsic excitability of cholinergic neurons in the rat parabigeminal nucleus. J Neurophysiol 98:3486–3493
Granda AM, Fulbrook JE (1989) Classification of turtle retinal ganglion cells. J Neurophysiol 62:723–737
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
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
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
Hall WC, Fitzpatrcik D, Klatt LL, Raczkowski D (1989) Cholinergic innervation of the superior colliculus in the cat. J Comp Neurol 287:495–514
Kriegstein AR (1987) Synaptic responses of cortical pyramidal neurons to light stimulation in the isolated turtle visual system. J Neurosci 7:2488–2492
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
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
Lucas-Meunier E, Fossier P, Baux G, Amar M (2003) Cholinergic modulation of the cortical neuronal network. Eur J Physiol 446:17–29
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
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
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
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
McCormick DA (1993) Actions of acetylcholine in the cerebral cortex and thalamus and implications for functions. Prog Brain Res 98:303–308
Medina L, Reiner A (1994) Distribution of choline acetyltransferase immunoreactivity in the pigeon brain. J Comp Neurol 342:497–537
Metherate R (2004) Nicotinic acetylcholine receptors in sensory cortex. Learn Mem 11:50–59
Mysore SP, Asadollahi A, Knudsen EI (2010) Global inhibition and stimulus competition in the owl optic tectum. J Neurosci 30:1727–1738
Northmore DP (1991) Visual responses of nucleus isthmi in a teleost fish (Lepomis macrochirus). Vision Res 31:525–535
Northmore DP, Gallagher SP (2003) Functional relationship between nucleus isthmi and tectum in teleosts: synchrony but no topography. Vis Neurosci 20:335–348
Northmore DP, Granda AM (1991) Ocular dimensions and schematic eyes of freshwater and sea turtles. Vis Neurosci 7:627–635
Peirce JW (2008) Generating stimuli for neuroscience using PsychoPy. Front Neuroinformatics 2:10
Powers AS, Reiner A (1993) The distribution of cholinergic neurons in the central nervous system of turtles. Brain Behav Evol 41:326–345
Quiroga RQ, Nadasdy Z, Ben-Shaul Y (2004) Unsupervised spike detection and sorting with wavelets and superparamagnetic clustering. Neural Comput 16:1661–1687
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
Rodieck RW (1965) Quantitative analysis of cat retinal ganglion cell response to visual stimuli. Vision Res 5:583–601
Rosenberg AF, Ariel M (1990) Visual-response properties of neurons in turtle basal optic nucleus in vitro. J Neurophysiol 63:1033–1045
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
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
Sceniak MP, Ringach DL, Hawken MJ, Shapley R (1999) Contrast’s effect on spatial summation by macaque V1 neurons. Nat Neurosci 2:733–739
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
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
Sherk H (1978) Visual response properties and visual field topography in the cat’s parabigeminal nucleus. Brain Res 145:375–379
Sherk H (1979a) A comparison of visual-response properties in cat’s parabigeminal nucleus and superior colliculus. J Neurophysiol 42:1640–1655
Sherk H (1979b) Connections and visual field mapping in cat’s tectoparabigeminal circuit. J Neurophysiol 42:1656–1668
Sillito AM, Jones HE (2002) Corticothalamic interactions in the transfer of visual information. Philos Trans R Soc Lond B Biol Sci 357:1739–1752
Sorenson EM, Parkinson D, Dahl JL, Chiappinelli VA (1989) Immunohistochemical localization of choline acetyltransferase in the chicken mesencephalon. J Comp Neurol 281:641–657
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
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
Wang SR, Yan K, Wang YT, Jiang SY, Wang XS (1983) Neuroanatomy and electrophysiology of the lacertilian nucleus isthmi. Brain Res 275:355–360
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
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
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
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
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
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
Yan K, Wang SR (1986) Visual responses of neurons in the avian nucleus isthmi. Neurosci Lett 64:340–344
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.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00359-010-0596-3