Abstract
The archerfish, which is unique in its ability to hunt insects above the water level by shooting a jet of water at its prey, operates in a complex visual environment. The fish needs to quickly select one object from among many others. In animals other than the archerfish, long-range inhibition is considered to drive selection. As a result of long-range inhibition, a potential target outside a neuron’s receptive field suppresses the activity elicited by another potential target within the receptive field. We tested whether a similar mechanism operates in the archerfish by recording the activity of neurons in the optic tectum while presenting a target stimulus inside the receptive field and a competing stimulus outside the receptive field. We held the features of the target constant while varying the size, speed, and distance of the competing stimulus. We found cells that exhibit long-range inhibition; i.e., inhibition that extends to a significant part of the entire visual field of the animal. The competing stimulus depressed the firing rate. In some neurons, this effect was dependent on the features of the competing stimulus. These findings suggest that long-range inhibition may play a crucial role in the target selection process in the archerfish.
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References
Allman J, Miezin F, McGuinness E (1985) Direction-and velocity-specific responses from beyond the classical receptive field in the middle temporal visual area (MT). Perception 14:105–126. https://doi.org/10.1068/p140105
Bass A (1977) Effects of lesions of the optic tectum on the ability of turtles to locate food stimuli. Brain Behav Evol 14:251–260. https://doi.org/10.1159/000125665
Ben-Simon A, Ben-Shahar O, Vasserman G (2012) Visual acuity in the archerfish: behavior, anatomy, and neurophysiology. J Vision 12:18. https://doi.org/10.1167/12.12.18
Ben-Tov M, Kopilevich I, Donchin O et al (2013) Visual receptive field properties of cells in the optic tectum of the archer fish. J Neurophysiol 110:748–759. https://doi.org/10.1152/jn.00094.2013
Ben-Tov M, Donchin O, Ben-Shahar O, Segev R (2015) Pop-out in visual search of moving targets in the archer fish. Nat Commun. https://doi.org/10.1038/ncomms7476
Bodznick D (1990) Elasmobranch vision: multimodal integration in the brain. J Exp Zool 256:108–116. https://doi.org/10.1002/jez.1402560515
Carello C, Krauzlis R (2004) Manipulating Intent: evidence for a causal role of the superior colliculus in target selection. Neuron 43:575–583. https://doi.org/10.1016/j.neuron.2004.07.026
Chelazzi L, Miller E, Duncan J, Desimone R (1993) A neural basis for visual search in inferior temporal cortex. Nature 363:345–347. https://doi.org/10.1038/363345a0
Denwood MJ (2016) runjags: an R package providing interface utilities, model templates, parallel computing methods and additional distributions for MCMC models in JAGS. J Stat Softw. https://doi.org/10.18637/jss.v071.i09
Desimone R, Duncan J (1995) Neural mechanisms of selective visual attention. Annu Rev Neurosci 18:193–222. https://doi.org/10.1146/annurev.ne.18.030195.001205
Dudkin EA, Peiffer T, Burkitt B et al (2011) Leopard frog priorities in choosing between prey at different locations. Behav Proc 86:138–142. https://doi.org/10.1016/j.beproc.2010.11.002
Dunn T, Gebhardt C, Naumann E et al (2016) Neural Circuits underlying visually evoked escapes in larval zebrafish. Neuron 89:613–628. https://doi.org/10.1016/j.neuron.2015.12.021
Ekström P (1987) Distribution of choline acetyltransferase-immunoreactive neurons in the brain of a cyprinid teleost (Phoxinus phoxinusL.). J Comp Neurol 256:494–515. https://doi.org/10.1002/cne.902560403
Fecteau J, Munoz D (2006) Salience, relevance, and firing: a priority map for target selection. Trends Cogn Sci 10:382–390. https://doi.org/10.1016/j.tics.2006.06.011
Fleishman L (1986) Motion detection in the presence and absence of background motion in an Anolis lizard. J Comp Physiol A 159:711–720. https://doi.org/10.1007/bf00612043
Gabay S, Leibovich T, Ben-Simon A et al (2013) Inhibition of return in the archer fish. Nat Commun 4:1657. https://doi.org/10.1038/ncomms2644
Herrero L, Rodríguez F, Salas C, Torres B (1998) Tail and eye movements evoked by electrical microstimulation of the optic tectum in goldfish. Exp Brain Res 120:291–305. https://doi.org/10.1007/s002210050403
Houghton G, Tipper S (1996) Inhibitory mechanisms of neural and cognitive control: applications to selective attention and sequential action. Brain Cogn 30:20–43. https://doi.org/10.1006/brcg.1996.0003
Ingle D (1973) Selective choice between double prey objects by frogs. Brain Behav Evol 7:127–144. https://doi.org/10.1159/000124406
Kardamakis A, Saitoh K, Grillner S (2015) Tectal microcircuit generating visual selection commands on gaze-controlling neurons. Proc Natl Acad Sci 112:E1956–E1965. https://doi.org/10.1073/pnas.1504866112
Karoubi N, Segev R, Wullimann MF (2016) The brain of the archerfish toxotes chatareus: a nissl-based neuroanatomical atlas and catecholaminergic/cholinergic systems. Front Neuroanat. https://doi.org/10.3389/fnana.2016.0010
Kastner S (1998) Mechanisms of directed attention in the human extrastriate cortex as revealed by functional MRI. Science 282:108–111. https://doi.org/10.1126/science.282.5386.108
Knierim JJ, Essen DCV (1992) Neuronal responses to static texture patterns in area V1 of the alert macaque monkey. J Neurophysiol 67:961–980. https://doi.org/10.1152/jn.1992.67.4.961
Kostyk S, Grobstein P (1982) Visual orienting deficits in frogs with various unilateral lesions. Behav Brain Res 6:379–388. https://doi.org/10.1016/0166-4328(82)90019-5
Krauzlis R, Dill N (2002) Neural correlates of target choice for pursuit and saccades in the primate superior colliculus. Neuron 35:355–363. https://doi.org/10.1016/s0896-6273(02)00756-0
Krauzlis R, Bogadhi A, Herman J, Bollimunta A (2018) Selective attention without a neocortex. Cortex. https://doi.org/10.1016/j.cortex.2017.08.026
Kruschke J (2014) Doing Bayesian data analysis: a tutorial with R, JAGS, and Stan. Academic Press, Cambridge
Lewicki M (1998) A review of methods for spike sorting: the detection and classification of neural action potentials. Netw Comput Neural Syst. https://doi.org/10.1088/0954-898x/9/4/001
Lüling KH (1958) Morphologisch-Anatomische und Histologische untersuchungen am auge des Schützenfisches Toxotes Jaculatrix (Pallas 1766) (Toxotidae) nebst Bemerkungen zum Spuckgehaben. H. Stürtz AG. (Würzburg)
Lüling K (1963) The archer fish. Sci Am 209:100–109. https://doi.org/10.1038/scientificamerican0763-100
Marin G, Salas C, Sentis E et al (2007) A cholinergic gating mechanism controlled by competitive interactions in the optic tectum of the pigeon. J Neurosci 27:8112–8121. https://doi.org/10.1523/jneurosci.1420-07.2007
Marois R, Ivanoff J (2005) Capacity limits of information processing in the brain. Trends Cogn Sci 9:296–305. https://doi.org/10.1016/j.tics.2005.04.010
McPeek R, Keller E (2004) Deficits in saccade target selection after inactivation of superior colliculus. Nat Neurosci 7:757–763. https://doi.org/10.1038/nn1269
Miller E, Gochin P, Gross C (1993) Suppression of visual responses of neurons in inferior temporal cortex of the awake macaque by addition of a second stimulus. Brain Res 616:25–29. https://doi.org/10.1016/0006-8993(93)90187-r
Mokeichev A, Segev R, Ben-Shahar O (2010) Orientation saliency without visual cortex and target selection in archer fish. Proc Natl Acad Sci 107:16726–16731. https://doi.org/10.1073/pnas.1005446107
Mysore S, Knudsen E (2011) The role of a midbrain network in competitive stimulus selection. Curr Opin Neurobiol 21:653–660. https://doi.org/10.1016/j.conb.2011.05.024
Mysore S, Asadollahi A, Knudsen E (2010) Global inhibition and stimulus competition in the owl optic tectum. J Neurosci 30:1727–1738. https://doi.org/10.1523/jneurosci.3740-09.2010
Mysore S, Asadollahi A, Knudsen E (2011) Signaling of the strongest stimulus in the owl optic tectum. J Neurosci 31:5186–5196. https://doi.org/10.1523/jneurosci.4592-10.2011
Newport C, Wallis G, Reshitnyk Y, Siebeck U (2016) Discrimination of human faces by archerfish (Toxotes chatareus). Sci Rep. https://doi.org/10.1038/srep27523
Nummela S, Krauzlis R (2010) Inactivation of primate superior colliculus biases target choice for smooth pursuit, saccades, and button press responses. J Neurophysiol 104:1538–1548. https://doi.org/10.1152/jn.00406.2010
Passaglia CL, Enroth-Cugell C, Troy JB (2001) Effects of remote stimulation on the mean firing rate of cat retinal ganglion cells. J Neurosci 15:5794–5803. https://doi.org/10.1523/jneurosci.2115-05794.2001
Plotkin A, Paperno E, Vasserman G, Segev R (2008) Magnetic tracking of eye motion in small, fast-moving animals. IEEE Trans Magn 44:4492–4495. https://doi.org/10.1109/tmag.2008.2002187
Port NL, Wurtz RH (2009) Target selection and saccade generation in monkey superior colliculus. Exp Brain Res 192:465–477. https://doi.org/10.1007/s00221-008-1609-0
R Development Core Team (2018) R: a language and environment for statistical computing. R version 3.4.4. R Foundation for Statistical Computing, Vienna. http://www.R-project.org
Reichenthal A, Ben-Tov M, Segev R (2018) Coding schemes in the archerfish optic tectum. Front Neural Circuits. https://doi.org/10.3389/fncir.2018.00018
Reynolds J, Chelazzi L, Desimone R (1999) Competitive mechanisms subserve attention in macaque Areas V2 and V4. J Neurosci 19:1736–1753. https://doi.org/10.1523/jneurosci.19-05-01736.1999
Rizzolatti G, Camarda R, Grupp L, Pisa M (1974) Inhibitory effect of remote visual stimuli on visual responses of cat superior colliculus: spatial and temporal factors. J Neurophysiol 37:1262–1275. https://doi.org/10.1152/jn.1974.37.6.1262
Schuster S, Rossel S, Schmidtmann A et al (2004) Archer fish learn to compensate for complex optical distortions to determine the absolute size of their aerial prey. Curr Biol 14:1565–1568. https://doi.org/10.1016/j.cub.2004.08.050
Segev R, Goodhouse J, Puchalla J, Berry MJ (2004) Recording spikes from a large fraction of the ganglion cells in a retinal patch. Nat Neurosci 7:1155–1162. https://doi.org/10.1038/nn1323
Solomon SG, Lee BB, Sun H (2006) Suppressive surrounds and contrast gain in magnocellular-pathway retinal ganglion cells of macaque. J Neurosci 34:8715–8726. https://doi.org/10.1523/jneurosci.0821-06.2006
Spiegelhalter DJ, Best NG, Carlin BP, Linde AVD (2002) Bayesian measures of model complexity and fit. J R Stat Soc Ser B (Stat Methodol 64:583–639. https://doi.org/10.1111/1467-9868.00353
Temizer I, Donovan J, Baier H, Semmelhack J (2015) A visual pathway for looming-evoked escape in larval zebrafish. Curr Biol 25:1823–1834. https://doi.org/10.1016/j.cub.2015.06.002
Tsotsos J (1990) Analyzing vision at the complexity level. Behav Brain Sci 13:423–445. https://doi.org/10.1017/s0140525x00079577
Tsvilling V, Donchin O, Shamir M, Segev R (2012) Archer fish fast hunting maneuver may be guided by directionally selective retinal ganglion cells. Eur J Neurosci 35:436–444. https://doi.org/10.1111/j.1460-9568.2011.07971.x
Vasserman G, Shamir M, Ben Simon A, Segev R (2010) Coding “What” and “When” in the Archer Fish Retina. PLoS Comput Biol 6:e1000977. https://doi.org/10.1371/journal.pcbi.1000977
Zahar Y, Lev-Ari T, Wagner H, Gutfreund Y (2018) Behavioral evidence and neural correlates of perceptual grouping by motion in the barn owl. J Neurosci 38:6653–6664. https://doi.org/10.1523/jneurosci.0174-18.2018
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We thank Gustavo Glusman for technical assistance.
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This research was supported by the Israel Science Foundation (Grant No. 211/15), and the Helmsley Charitable Trust through the Agricultural, Biological and Cognitive Robotics Initiative of Ben-Gurion University of the Negev.
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Volotsky, S., Vinepinsky, E., Donchin, O. et al. Long-range neural inhibition and stimulus competition in the archerfish optic tectum. J Comp Physiol A 205, 537–552 (2019). https://doi.org/10.1007/s00359-019-01345-1
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DOI: https://doi.org/10.1007/s00359-019-01345-1