Neural activity in a hippocampus-like region of the teleost pallium is associated with active sensing and navigation
Open accessPublished version of a preprint
Abstract
Most vertebrates use active sensing strategies for perception, cognition and control of motor activity. These strategies include directed body/sensor movements or increases in discrete sensory sampling events. The weakly electric fish, Gymnotus sp., uses its active electric sense during navigation in the dark. Electric organ discharge rate undergoes transient increases during navigation to increase electrosensory sampling. Gymnotus also use stereotyped backward swimming as an important form of active sensing that brings objects toward the electroreceptor dense fovea-like head region. We wirelessly recorded neural activity from the pallium of freely swimming Gymnotus. Spiking activity was sparse and occurred only during swimming. Notably, most units tended to fire during backward swims and their activity was on average coupled to increases in sensory sampling. Our results provide the first characterization of neural activity in a hippocampal (CA3)-like region of a teleost fish brain and connects it to active sensing of spatial environmental features.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Cells fundamental to spatial cognition in mammals-for example, place cells-have yet to be established in any fish species.
“cells fundamental to spatial cognition in mammals—for example, place cells (PCs)5,6—have yet to be established in any fish species”
From A population code for spatial representation in the zebrafish telencephalon (2024) · cites this paper as [23]
The Discussion says that classic mammalian-like spatially tuned neurons may not yet have been sampled in the teleost pallium, and that the recorded DDi cells are not exact matches for place cells. This supports the narrower point that place cells were not established in the teleosts discussed, but the paper does not establish the claim for every fish species. (LLM, conf=0.83)
Experimental — accuracy not yet measuredExperimental studies using well-controlled behavioral procedures combined with brain lesion, neural activity recording, and neuro-morphofunctional techniques have provided evidence on the critical role of the teleost fish hippocampal pallium in spatial cognition.
“A growing number of experimental studies using well-controlled behavioral procedures combined with brain lesion, neural activity recording, and neuro-morphofunctional techniques have provided evidence on the critical role of the teleost fish hippocampal pallium in spatial cognition [28,112,157,180,181,182,183,184,185,186].”
From Spatial Cognition in Teleost Fish: Strategies and Mechanisms (2021) · cites this paper as [28]
Fotowat et al. and Trinh et al. found cells in the hippocampal pallium of an electrosensory gymnotiform that exhibit spatial navigation-related activity.
“Additionally, Fotowat et al. [28] and Trinh et al. [204] found cells in the hippocampal pallium of an electrosensory gymnotiform that presumably exhibit spatial navigation-related activity.”
From Spatial Cognition in Teleost Fish: Strategies and Mechanisms (2021) · cites this paper as [28]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat
O'Keefe, J., & Dostrovsky, J. (1971) · Brain Research · doi:10.1016/0006-8993(71)90358-1 · Cited by 6,151 · see citing works
The hippocampus as a cognitive map
Passingham, R. E. (1979) · Neuroscience · doi:10.1016/0306-4522(79)90015-0 · Cited by 5,128 · see citing works
Dynamics of the Hippocampal Ensemble Code for Space
Wilson, M. A., & McNaughton, B. L. (1993) · Science · doi:10.1126/science.8351520 · Cited by 2,350 · see citing works
The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells
Muller, R., & Kubie, J. (1987) · The Journal of Neuroscience · doi:10.1523/jneurosci.07-07-01951.1987 · Cited by 1,581 · see citing works
Hedrick, T. L. (2008) · Bioinspiration & Biomimetics · doi:10.1088/1748-3182/3/3/034001 · Cited by 1,360 · see citing works
Representation of Geometric Borders in the Entorhinal Cortex
Solstad, T., Boccara, C. N., Kropff, E., Moser, M.-B., & Moser, E. I. (2008) · Science · doi:10.1126/science.1166466 · Cited by 1,213 · see citing works
The Head Direction Signal: Origins and Sensory-Motor Integration
Taube, J. S. (2007) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.29.051605.112854 · Cited by 916 · see citing works
Corollary discharge across the animal kingdom
Crapse, T. B., & Sommer, M. A. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2457 · Cited by 789 · see citing works
Boundary Vector Cells in the Subiculum of the Hippocampal Formation
Lever, C., Burton, S., Jeewajee, A., O'Keefe, J., & Burgess, N. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.1319-09.2009 · Cited by 753 · see citing works
Spatial representation in the hippocampal formation: a history
Moser, E. I., Moser, M.-B., & McNaughton, B. L. (2017) · Nature Neuroscience · doi:10.1038/nn.4653 · Cited by 560 · see citing works
The role of the hippocampus in navigation is memory
Eichenbaum, H. (2017) · Journal of Neurophysiology · doi:10.1152/jn.00005.2017 · Cited by 430 · see citing works
Parallel emergence of stable and dynamic memory engrams in the hippocampus
Hainmueller, T., & Bartos, M. (2018) · Nature · doi:10.1038/s41586-018-0191-2 · Cited by 383 · see citing works
Rearing on Hind Legs, Environmental Novelty, and the Hippocampal Formation
Lever, C., Burton, S., & O'Keefe, J. M. (2006) · Reviews in the Neurosciences · doi:10.1515/revneuro.2006.17.1-2.111 · Cited by 366 · see citing works
Influence of boundary removal on the spatial representations of the medial entorhinal cortex
Savelli, F., Yoganarasimha, D., & Knierim, J. J. (2008) · Hippocampus · doi:10.1002/hipo.20511 · Cited by 363 · see citing works
Gahtan, E., Tanger, P., & Baier, H. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.2678-05.2005 · Cited by 350 · see citing works
Vectorial representation of spatial goals in the hippocampus of bats
Sarel, A., Finkelstein, A., Las, L., & Ulanovsky, N. (2017) · Science · doi:10.1126/science.aak9589 · Cited by 340 · see citing works
How vision and movement combine in the hippocampal place code
Chen, G., King, J. A., Burgess, N., & O'Keefe, J. M. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1215834110 · Cited by 338 · see citing works
Hierarchy of orofacial rhythms revealed through whisking and breathing
Moore, J. D., Deschênes, M., Furuta, T., Huber, D., Smear, M. C., Demers, M., & Kleinfeld, D. (2013) · Nature · doi:10.1038/nature12076 · Cited by 320 · see citing works
Conservation of Spatial Memory Function in the Pallial Forebrain of Reptiles and Ray-Finned Fishes
Rodrı́guez, F., López, J. C., Vargas, J. P., Gómez, Y., Broglio, C., & Salas, C. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-07-02894.2002 · Cited by 316 · see citing works
Place cells in the hippocampus: Eleven maps for eleven rooms
Alme, C. B., Miao, C., Jezek, K., Treves, A., Moser, E. I., & Moser, M.-B. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1421056111 · Cited by 296 · see citing works
Fenton, A. A., & Muller, R. U. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.6.3182 · Cited by 283 · see citing works
Hippocampal cellular and network activity in freely moving echolocating bats
Ulanovsky, N., & Moss, C. F. (2007) · Nature Neuroscience · doi:10.1038/nn1829 · Cited by 283 · see citing works
Social place-cells in the bat hippocampus
Omer, D. B., Maimon, S. R., Las, L., & Ulanovsky, N. (2018) · Science · doi:10.1126/science.aao3474 · Cited by 280 · see citing works
Spatial representations of self and other in the hippocampus
Danjo, T., Toyoizumi, T., & Fujisawa, S. (2018) · Science · doi:10.1126/science.aao3898 · Cited by 257 · see citing works
Nelson, M. E., & MacIver, M. A. (1999) · Journal of Experimental Biology · doi:10.1242/jeb.202.10.1195 · Cited by 251 · see citing works
The Cognitive Architecture of Spatial Navigation: Hippocampal and Striatal Contributions
Chersi, F., & Burgess, N. (2015) · Neuron · doi:10.1016/j.neuron.2015.09.021 · Cited by 240 · see citing works
Pattern separation, completion, and categorisation in the hippocampus and neocortex
Rolls, E. T. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.07.008 · Cited by 234 · see citing works
Fenton, A. A., Kao, H.-Y., Neymotin, S. A., Olypher, A. V., Vayntrub, Y., Lytton, W. W., & Ludvig, N. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.2862-08.2008 · Cited by 208 · see citing works
Peripheral organization and central projections of the electrosensory nerves in gymnotiform fish
Carr, C. E., Maler, L., & Sas, E. (1982) · The Journal of Comparative Neurology · doi:10.1002/cne.902110204 · Cited by 204 · see citing works
Self-citationAttention promotes episodic encoding by stabilizing hippocampal representations
Aly, M., & Turk-Browne, N. (2016) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1518931113 · Cited by 194 · see citing works
Spatial Firing of Hippocampal Place Cells in Blind Rats
Save, É., Cressant, A., Thinus‐Blanc, C., & Poucet, B. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-05-01818.1998 · Cited by 193 · see citing works
The Neurobiology of Mammalian Navigation
Poulter, S. L., Hartley, T., & Lever, C. (2018) · Current Biology · doi:10.1016/j.cub.2018.05.050 · Cited by 171 · see citing works
Neural Mechanisms of Self-Location
Barry, C., & Burgess, N. (2014) · Current Biology · doi:10.1016/j.cub.2014.02.049 · Cited by 168 · see citing works
Attentive scanning behavior drives one-trial potentiation of hippocampal place fields
Monaco, J. D., Rao, G., Roth, E. D., & Knierim, J. J. (2014) · Nature Neuroscience · doi:10.1038/nn.3687 · Cited by 163 · see citing works
Sparse activity of identified dentate granule cells during spatial exploration
Diamantaki, M., Frey, M., Berens, P., Preston‐Ferrer, P., & Burgalossi, A. (2016) · eLife · doi:10.7554/elife.20252 · Cited by 162 · see citing works
A New Perspective on Predictive Motor Signaling
Straka, H., Simmers, J., & Chagnaud, B. P. (2018) · Current Biology · doi:10.1016/j.cub.2018.01.033 · Cited by 152 · see citing works
Muzzio, I. A., Levita, L., Kulkarni, J. E., Monaco, J. D., Kentros, C. G., Stead, M., Abbott, L. F., & Kandel, E. R. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000140 · Cited by 149 · see citing works
Park, E., Dvořák, D., & Fenton, A. A. (2011) · PLoS ONE · doi:10.1371/journal.pone.0022349 · Cited by 146 · see citing works
Shumway, C. A. (1989) · Journal of Neuroscience · doi:10.1523/jneurosci.09-12-04400.1989 · Cited by 144 · see citing works
Neural maps in the electrosensory system of weakly electric fish
Krahe, R., & Maler, L. (2013) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2013.08.013 · Cited by 142 · see citing works
Self-citationEncoding of Head Direction by Hippocampal Place Cells in Bats
Rubin, A., Yartsev, M. M., & Ulanovsky, N. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.5393-12.2014 · Cited by 124 · see citing works
Bastian, J. (1982) · Journal of Comparative Physiology A · doi:10.1007/bf00609662 · Cited by 120 · see citing works
Fish can encode order in their spatial map
de Perera, T. B. (2004) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2004.2867 · Cited by 115 · see citing works
Selective involvement of the goldfish lateral pallium in spatial memory
Broglio, C., Rodríguez, F., Gómez, A., Arias, J. L., & Salas, C. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.02.031 · Cited by 112 · see citing works
Tail and eye movements evoked by electrical microstimulation of the optic tectum in goldfish
Herrero, L., Rodríguez, F., Salas, C., & Torres, B. (1998) · Experimental Brain Research · doi:10.1007/s002210050403 · Cited by 100 · see citing works
Durán, E., Ocaña, F. M., Broglio, C., Rodríguez, F., & Salas, C. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.06.010 · Cited by 90 · see citing works
Castelló, M. E., Aguilera, P. A., Trujillo-Cenóz, O., & Caputi, A. A. (2000) · Journal of Experimental Biology · doi:10.1242/jeb.203.21.3279 · Cited by 89 · see citing works
Vinepinsky, E., Cohen, L., Perchik, S., Ben-Shahar, O., Donchin, O., & Segev, R. (2020) · Scientific Reports · doi:10.1038/s41598-020-71217-1 · Cited by 87 · see citing works
Spatial parameters encoded in the spatial map of the blind Mexican cave fish, Astyanax fasciatus
de Perera, T. B. (2004) · Animal Behaviour · doi:10.1016/j.anbehav.2003.11.009 · Cited by 86 · see citing works
Transformation of the head-direction signal into a spatial code
Peyrache, A., Schieferstein, N., & Buzsáki, G. (2017) · Nature Communications · doi:10.1038/s41467-017-01908-3 · Cited by 83 · see citing works
Passive Transport Disrupts Grid Signals in the Parahippocampal Cortex
Winter, S. S., Mehlman, M. L., Clark, B. J., & Taube, J. S. (2015) · Current Biology · doi:10.1016/j.cub.2015.08.034 · Cited by 81 · see citing works
Vonderschen, K., & Chacron, M. J. (2011) · Journal of Neurophysiology · doi:10.1152/jn.00588.2011 · Cited by 81 · see citing works
Toerring, M.-J., & Moller, P. (1984) · Behavioural Brain Research · doi:10.1016/0166-4328(84)90155-4 · Cited by 68 · see citing works
Framing of grid cells within and beyond navigation boundaries
Savelli, F., Luck, J., & Knierim, J. J. (2017) · eLife · doi:10.7554/elife.21354 · Cited by 64 · see citing works
Giassi, A. C. C., Duarte, T. T., Ellis, W., & Maler, L. (2012) · The Journal of Comparative Neurology · doi:10.1002/cne.23109 · Cited by 61 · see citing works
Self-citationMethods for chronic neural recording in the telencephalon of freely behaving fish
Canfield, J. G., & Mizumori, S. J. Y. (2004) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2003.10.011 · Cited by 61 · see citing works
Elliott, S. B., Harvey‐Girard, E., Giassi, A. C. C., & Maler, L. (2017) · Journal of Comparative Neurology · doi:10.1002/cne.24060 · Cited by 61 · see citing works
Self-citationEnhanced sensory sampling precedes self-initiated locomotion in an electric fish
Jun, J. J., Longtin, A., & Maler, L. (2014) · Journal of Experimental Biology · doi:10.1242/jeb.105502 · Cited by 59 · see citing works
Self-citationActive sensing associated with spatial learning reveals memory-based attention in an electric fish
Jun, J. J., Longtin, A., & Maler, L. (2016) · Journal of Neurophysiology · doi:10.1152/jn.00979.2015 · Cited by 58 · see citing works
Self-citationRole of active movement in place-specific firing of hippocampal neurons
Song, E. Y., Kim, Y. B., Kim, Y. H., & Jung, M. W. (2004) · Hippocampus · doi:10.1002/hipo.20023 · Cited by 57 · see citing works
Saraf‐Sinik, I., Assa, E., & Ahissar, E. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.4149-14.2015 · Cited by 54 · see citing works
Giassi, A. C. C., Ellis, W., & Maler, L. (2012) · The Journal of Comparative Neurology · doi:10.1002/cne.23108 · Cited by 54 · see citing works
Self-citationHarvey‐Girard, E., Giassi, A. C. C., Ellis, W., & Maler, L. (2012) · Journal of Comparative Neurology · doi:10.1002/cne.23107 · Cited by 54 · see citing works
Self-citationWallach, A., Harvey‐Girard, E., Jun, J. J., Longtin, A., & Maler, L. (2018) · eLife · doi:10.7554/elife.36769 · Cited by 48 · see citing works
Self-citationCryptic laminar and columnar organization in the dorsolateral pallium of a weakly electric fish
Trinh, A., Harvey‐Girard, E., Teixeira, F., & Maler, L. (2016) · Journal of Comparative Neurology · doi:10.1002/cne.23874 · Cited by 44 · see citing works
Self-citationHeiligenberg, W., & Rose, G. J. (1987) · Neuroscience · doi:10.1016/0306-4522(87)90224-7 · Cited by 44 · see citing works
Giassi, A. C. C., Harvey‐Girard, E., Valsamis, B., & Maler, L. (2012) · The Journal of Comparative Neurology · doi:10.1002/cne.23097 · Cited by 41 · see citing works
Self-citationDynamics of goldfish subregional hippocampal pallium activity throughout spatial memory formation
Ocaña, F. M., Uceda, S., Arias, J. L., Salas, C., & Rodríguez, F. (2017) · Brain, Behavior and Evolution · doi:10.1159/000478843 · Cited by 41 · see citing works
Emergent Exploration via Novelty Management
Gordon, G., Fonio, E., & Ahissar, E. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1872-14.2014 · Cited by 40 · see citing works
Electroreception inG. carapo: detection of changes in waveform of the electrosensory signals
Aguilera, P. A., & Caputi, A. A. (2003) · Journal of Experimental Biology · doi:10.1242/jeb.00198 · Cited by 40 · see citing works
Rats build and update topological representations through exploration
Alvernhe, A., Sargolini, F., & Poucet, B. (2011) · Animal Cognition · doi:10.1007/s10071-011-0460-z · Cited by 36 · see citing works
Motion parallax in electric sensing
Pedraja, F., Hofmann, V., Lucas, K. M., Young, C., Engelmann, J., & Lewis, J. E. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1712380115 · Cited by 35 · see citing works
Uceda, S., Ocaña, F. M., Martín-Monzón, I., Rodríguez-Expósito, B., Durán, E., & Rodríguez, F. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.06.018 · Cited by 35 · see citing works
Linear Self-Motion Cues Support the Spatial Distribution and Stability of Hippocampal Place Cells
Harvey, R. E., Rutan, S. A., Willey, G. R., Siegel, J. J., Clark, B. J., & Yoder, R. M. (2018) · Current Biology · doi:10.1016/j.cub.2018.04.034 · Cited by 34 · see citing works
Motor patterns during active electrosensory acquisition
Hofmann, V., Geurten, B. R. H., Sanguinetti-Scheck, J. I., Gómez‐Sena, L., & Engelmann, J. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00186 · Cited by 31 · see citing works
The neural dynamics of sensory focus
Clarke, S. E., Longtin, A., & Maler, L. (2015) · Nature Communications · doi:10.1038/ncomms9764 · Cited by 26 · see citing works
Self-citationAmey‐Özel, M., von der Emde, G., Engelmann, J., & Grant, K. (2014) · The Journal of Comparative Neurology · doi:10.1002/cne.23710 · Cited by 25 · see citing works
Stimulus-induced up states in the dorsal pallium of a weakly electric fish
Elliott, S. B., & Maler, L. (2015) · Journal of Neurophysiology · doi:10.1152/jn.00666.2015 · Cited by 24 · see citing works
Self-citationSanguinetti-Scheck, J. I., Pedraja, E. F., Cilleruelo, E., Migliaro, A., Aguilera, P. A., Caputi, A. A., & Budelli, R. (2011) · PLoS ONE · doi:10.1371/journal.pone.0027470 · Cited by 20 · see citing works
Neural Substrate of an Increase in Sensory Sampling Triggered by a Motor Command in a Gymnotid Fish
Comas, V., & Borde, M. (2010) · Journal of Neurophysiology · doi:10.1152/jn.00076.2010 · Cited by 19 · see citing works
Stereotaxic atlas of the telencephalon of the weakly electric fish Gymnotus carapo
Corrêa, S. A. L., Corrêa, F. M. D. A., & Hoffmann, A. (1998) · Journal of Neuroscience Methods · doi:10.1016/s0165-0270(98)00098-3 · Cited by 17 · see citing works
Long-term Behavioral Tracking of Freely Swimming Weakly Electric Fish
Jun, J. J., Longtin, A., & Maler, L. (2014) · Journal of Visualized Experiments · doi:10.3791/50962 · Cited by 15 · see citing works
Self-citationSchumacher, S., de Perera, T. B., & von der Emde, G. (2016) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2016.11.008 · Cited by 13 · see citing works
Afferent and efferent connections of the mesencephalic reticular formation in goldfish
Luque, M. A., Pérez-Pérez, M. P., Herrero, L., & Torres, B. (2007) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2007.10.018 · Cited by 9 · see citing works
Representation of object’s shape by multiple electric images in electrolocation
Fujita, K., & Kashimori, Y. (2019) · Biological Cybernetics · doi:10.1007/s00422-018-00790-6 · Cited by 9 · see citing works
Lannoo, M. J., & Maler, L. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.902940112 · Cited by 8 · see citing works
Self-citation線形自己運動キューは海馬場所細胞の空間分布と安定性をサポートする【JST・京大機械翻訳】
Ryan, E. H., Stephanie, A., Gabrielle, R., Jennifer, J. S., Benjamin, J., & Ryan, M. Y. (2018) · Current Biology · Cited by 6 · see citing works
Flagged first, then by citations
2 of the 90 references couldn’t be matched to a known paper.
Research works printed but not linked: 2
- Fotowat H Lee C Jun JJ Maler L 2019 Neural activity in a hippocampus-like region of the teleost pallium is associated with active sensing and navigation uO Research 10.20381/38902 PMC6469930 30942169 · DOI
- Vinepinsky E Perchik S Ben-Shahar O Donchin O Segev R 2018 Representation of border, velocity and speed in the goldfish brain bioRxiv 10.1101/291013 · DOI
Cited by
Sorted by citations
Neural representations of space in the hippocampus of a food-caching bird
Payne, H. L., Lynch, G. F., & Aronov, D. (2021) · Science · doi:10.1126/science.abg2009 · Cited by 163 · see citing works
Jurisch‐Yaksi, N., Yaksi, E., & Kızıl, Ç. (2020) · Glia · doi:10.1002/glia.23849 · Cited by 156 · see citing works
Vinepinsky, E., Cohen, L., Perchik, S., Ben-Shahar, O., Donchin, O., & Segev, R. (2020) · Scientific Reports · doi:10.1038/s41598-020-71217-1 · Cited by 87 · see citing works
Impact of noise on development, physiological stress and behavioural patterns in larval zebrafish
Lara, R. A., & Vasconcelos, R. O. (2021) · Scientific Reports · doi:10.1038/s41598-021-85296-1 · Cited by 72 · see citing works
Spatial Cognition in Teleost Fish: Strategies and Mechanisms
Rodríguez, F., Quintero, B., Amores, L., Madrid, D., Salas-Peña, C., & Salas, C. (2021) · Animals · doi:10.3390/ani11082271 · Cited by 59 · see citing works
Avian pallial circuits and cognition: A comparison to mammals
Güntürkün, O., von Eugen, K., Packheiser, J., & Pusch, R. (2021) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2021.08.007 · Cited by 59 · see citing works
A population code for spatial representation in the zebrafish telencephalon
Yang, C., Mammen, L., Kim, B., Li, M., Robson, D. N., & Li, J. M. (2024) · Nature · doi:10.1038/s41586-024-07867-2 · Cited by 38 · see citing works
“In teleost fish, which shared a common ancestor with mammals around 450 million years ago 18 , the location or even existence of the hippocampus is an area of active debate 2,19 , particularly given the lack of clear functional evidence for PCs 20–23 .”
Cellular profiling of a recently-evolved social behavior in cichlid fishes
Johnson, Z. V., Hegarty, B. E., Gruenhagen, G. W., Lancaster, T. J., McGrath, P. T., & Streelman, J. T. (2023) · Nature Communications · doi:10.1038/s41467-023-40331-9 · Cited by 36 · see citing works
Motion parallax in electric sensing
Pedraja, F., Hofmann, V., Lucas, K. M., Young, C., Engelmann, J., & Lewis, J. E. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1712380115 · Cited by 35 · see citing works
Eye movements reveal spatiotemporal dynamics of visually-informed planning in navigation
Zhu, S. L., Lakshminarasimhan, K. J., Arfaei, N., & Angelaki, D. E. (2022) · eLife · doi:10.7554/elife.73097 · Cited by 30 · see citing works
Ongoing habenular activity is driven by forebrain networks and modulated by olfactory stimuli
Bartoszek, E. M., Ostenrath, A. M., Jetti, S. K., Serneels, B., Mutlu, A. K., Chau, K. T. P., & Yaksi, E. (2021) · Current Biology · doi:10.1016/j.cub.2021.08.021 · Cited by 29 · see citing works
Visually guided and context-dependent spatial navigation in the translucent fish Danionella cerebrum
Lee, T. J., & Briggman, K. L. (2023) · Current Biology · doi:10.1016/j.cub.2023.11.030 · Cited by 28 · see citing works
Linking active sensing and spatial learning in weakly electric fish.
Engelmann, J., Wallach, A., & Maler, L. (2021) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2021.07.002 · Cited by 25 · see citing works
Self-citationComputational cross‐species views of the hippocampal formation
Zhu, S. L., Lakshminarasimhan, K. J., & Angelaki, D. E. (2023) · Hippocampus · doi:10.1002/hipo.23535 · Cited by 24 · see citing works
Peripheral and central sensation: multisensory orienting and recognition across species
Li Zhaoping, A. (2023) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2023.03.001 · Cited by 23 · see citing works
Wallach, A., Melanson, A., Longtin, A., & Maler, L. (2021) · Current Biology · doi:10.1016/j.cub.2021.10.034 · Cited by 20 · see citing works
Self-citationPopulation Coding of Natural Electrosensory Stimuli by Midbrain Neurons
Metzen, M. G., & Chacron, M. J. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.2232-20.2021 · Cited by 19 · see citing works
Trinh, A., Clarke, S. E., Harvey‐Girard, E., & Maler, L. (2019) · eNeuro · doi:10.1523/eneuro.0108-19.2019 · Cited by 18 · see citing works
Self-citationWagner, H., Egelhaaf, M., & Carr, C. E. (2024) · Journal of Comparative Physiology A · doi:10.1007/s00359-023-01685-z · Cited by 16 · see citing works
Zabegalov, K. N., Costa, F. V., Kolesnikova, T. O., de Abreu, M. S., Petersen, E. V., Yenkoyan, K. B., & Kalueff, A. V. (2024) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2024.110964 · Cited by 15 · see citing works
Zebrafish models for studying cognitive enhancers
Kolesnikova, T. O., Demin, K. A., Costa, F. V., de Abreu, M. S., & Kalueff, A. V. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105797 · Cited by 15 · see citing works
Spatial Learning Promotes Adult Neurogenesis in Specific Regions of the Zebrafish Pallium
Mazzitelli-Fuentes, L., Román, F. R., Elías, J. R. C., Deleglise, E. B., & Mongiat, L. A. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.840964 · Cited by 15 · see citing works
Task-Related Sensorimotor Adjustments Increase the Sensory Range in Electrolocation
Pedraja, F., Hofmann, V., Goulet, J., & Engelmann, J. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.1024-19.2019 · Cited by 15 · see citing works
Bennett, M. S. (2021) · Frontiers in Psychology · doi:10.3389/fpsyg.2021.685853 · Cited by 13 · see citing works
Novel Functions of Feedback in Electrosensory Processing
Hofmann, V., & Chacron, M. J. (2019) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2019.00052 · Cited by 12 · see citing works
Navigational roots of spatial and temporal memory structure
Lee, S. A. (2022) · Animal Cognition · doi:10.1007/s10071-022-01726-1 · Cited by 11 · see citing works
Serotonergic Modulation of Sensory Neuron Activity and Behavior in Apteronotus albifrons
Márquez, M. M., & Chacron, M. J. (2020) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2020.00038 · Cited by 10 · see citing works
Trinh, A., Girardi‐Schappo, M., Béïque, J.-C., Longtin, A., & Maler, L. (2023) · The Journal of Physiology · doi:10.1113/jp283728 · Cited by 9 · see citing works
Self-citationNeural mechanisms for spatial cognition across vertebrates
Vinepinsky, E., & Segev, R. (2023) · Molecular Psychology Brain Behavior and Society · doi:10.12688/molpsychol.17503.1 · Cited by 8 · see citing works
Has the hippocampus really forgotten about space?
Fiedler, J., Leonibus, E. D., & Treves, A. (2021) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2021.11.009 · Cited by 8 · see citing works
Mitigation of avermectin exposure-induced brain tissue damage in carp by quercetin
Xu, X., Zhou, M., Xie, K., Zhang, S., Ji, X., Ying, S., Li, Q., & Dong, Z. (2023) · Fish Physiology and Biochemistry · doi:10.1007/s10695-023-01249-7 · Cited by 8 · see citing works
Shao, J.-W., Wang, J.-D., He, Q., Yang, Y., Zou, Y., Su, W., Xiang, S., Li, J., & Fang, J. (2021) · World Journal of Diabetes · doi:10.4239/wjd.v12.i4.499 · Cited by 7 · see citing works
Finding food in the dark: how trajectories of a gymnotiform fish change with spatial learning
Mirmiran, C., Fraser, M., & Maler, L. (2022) · Journal of Experimental Biology · doi:10.1242/jeb.244590 · Cited by 6 · see citing works
Self-citationTrinh, A.-T., Clarke, S. E., Harvey-Girard, E., & Maler, L. (2019) · doi:10.1101/571414 · Cited by 6 · see citing works
Self-citationHierarchical sensory processing in zebrafish thalamocortical-like circuits
Trinh, A.-T., Ostenrath, A. M., del Castillo-Berges, I., Cachin, F., Koç, M., Kraus, S., Serneels, B., Kawakami, K., & Yaksi, E. (2026) · Science · doi:10.1126/science.aec2171 · Cited by 5 · see citing works
Mutlu, A. K., Serneels, B., Wiest, C., Trinh, A., Bardenhewer, R., Palumbo, F., Frisvold, O. B., Aukrust, I. K. F., Ostenrath, A. M., & Yaksi, E. (2026) · Nature Communications · doi:10.1038/s41467-026-75490-y · Cited by 5 · see citing works
Kwon, V., Cai, P., Dixon, C. T., Hamlin, V., Spencer, C. G., Rojas, A. M., Hamilton, M., & Shiau, C. E. (2022) · Communications Biology · doi:10.1038/s42003-022-03410-z · Cited by 5 · see citing works
Rodríguez-Cattáneo, A., Pereira, A.-C., Aguilera, P. A., & Caputi, A. A. (2020) · Experimental Results · doi:10.1017/exp.2020.20 · Cited by 5 · see citing works
An end-to-end model of active electrosensation
Turcu, D., Zadina, A. N., Abbott, L. F., & Sawtell, N. B. (2024) · Current Biology · doi:10.1016/j.cub.2025.03.074 · Cited by 4 · see citing works
The sensory effects of light on the electric organ discharge rate of Gymnotus omarorum
Camargo, A. S., Caputi, A. A., & Aguilera, P. A. (2023) · Journal of Experimental Biology · doi:10.1242/jeb.245489 · Cited by 4 · see citing works
Lee, H. (2025) · Sensors · doi:10.3390/s25030979 · Cited by 3 · see citing works
Multimodal reference brain atlas of adult Danionella cerebrumPreprint
Kadobianskyi, M., Henninger, J., Markov, D. A., Groneberg, A. H., Veith, J., Renz, M., Atabay, K. D., Reddien, P. W., Maler, L., & Judkewitz, B. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.03.09.710483 · Cited by 3 · see citing works
Self-citationA framework for a low‐cost system of automated gate control in assays of spatial cognition in fishes
Lucks, V., Theine, J., Avendaño, M. P. A., & Engelmann, J. (2024) · Journal of Fish Biology · doi:10.1111/jfb.15958 · Cited by 2 · see citing works
Gutjahr, R., Bothe, M. S., Hofmann, M. H., & Chagnaud, B. P. (2025) · The Journal of Comparative Neurology · doi:10.1002/cne.70064 · Cited by 2 · see citing works
The Active Electric Sense of Pulse Gymnotiformes
Caputi, A. A. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.24200-4 · Cited by 2 · see citing works
Teleost Fish and Organoids: Alternative Windows Into the Development of Healthy and Diseased Brains
Fasano, G., Compagnucci, C., Dallapiccola, B., Tartaglia, M., & Lauri, A. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.855786 · Cited by 2 · see citing works
Vurmaz, A., Atay, E., Rakip, U., & Koca, T. (2023) · Journal of Biochemical and Molecular Toxicology · doi:10.1002/jbt.23609 · Cited by 2 · see citing works
Relational Memory Functions of the Hippocampal Pallium in Teleost Fish
Gómez, A., Ocaña, F. M., Puntas, T. D. Á., Rodrı́guez, F., & Salas, C. (2022) · Cambridge University Press eBooks · doi:10.1017/9781108768450.012 · Cited by 2 · see citing works
Sy, S. K. H., Chan, D. C. W., Zhang, J. J., Lyu, J., Feng, C., Wang, K., Mok, V., Wong, K. K. Y., Mu, Y., Hu, Y., et al. (2026) · eLife · doi:10.7554/elife.109494.1 · Cited by 2 · see citing works
Packet information encoding in a cerebellum-like circuit
Rodríguez-Cattáneo, A., Pereira, A. C., Aguilera, P. A., & Caputi, A. A. (2024) · PLoS ONE · doi:10.1371/journal.pone.0308146 · Cited by 1 · see citing works
Molecular Characterization of Neurogranin (NRGN) Gene from Red‑Bellied Pacu (Piaractus brachypomus)
Rueda-García, V., & Rondón‐Barragán, I. S. (2023) · Molecular Neurobiology · doi:10.1007/s12035-023-03700-5 · Cited by 1 · see citing works
Editorial: Recent Advances in Electroreception and Electrogeneration
Chacron, M. J., & Markham, M. R. (2021) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2021.668677 · Cited by 1 · see citing works
Sy, S. K. H., Chan, D. C. W., Zhang, J. J., Lyu, J., Feng, C., Wang, K., Mok, V., Wong, K. K. Y., Mu, Y., Hu, Y., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.10.27.620486 · Cited by 1 · see citing works
Active Control of Sensing Through Movements in Active Electrolocation
Engelmann, J., & Lucks, V. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.24212-0
Sensory System Function: A Historical and Integrative Perspective
Bleckmann, H. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.24264-8
Trinh, A. (2021) · uO Research (University of Ottawa) · doi:10.20381/ruor-26756
Evolution of Learning Processes
(2022) · Cambridge University Press eBooks · doi:10.1017/9781108768450.003
Upshall, M. (2023) · Elsevier eBooks · doi:10.1016/b978-0-323-90801-6.00121-x
Sy, S. K. H., Chan, D. C. W., Zhang, J. J., Lyu, J., Feng, C., Wang, K., Mok, V., Wong, K. K. Y., Mu, Y., Hu, Y., et al. (2026) · eLife · doi:10.7554/elife.109494
Zabegalov, K. N. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.09.24.754169
Sy, S. K. H., Chan, D. C. W., Zhang, J. J., Lyu, J., Feng, C., Wang, K., Mok, V., Wong, K. K. Y., Mu, Y., Hu, Y., et al. (2026) · eLife · doi:10.7554/elife.109494.2
- Authors
- Fotowat, H., Lee, C., Jun, J. J., & Maler, L.
- Affiliations
- Harvard University (US)
- University of Ottawa (CA)
- Flatiron Institute (US)
- Department of Cellular and Molecular Medicine, Brain and Mind Institute and Centre for Neural Dynamics, University of Ottawa, Ottawa, Canada
- Venue
- eLife
- Publisher
- eLife Sciences Publications, Ltd
- Published
- 2019-04-03
- Volume
- 8
- ISSN
- 2050-084X (ISSN-L)
- PMC
- PMC6469930
- OpenAlex
- W2934040352
- Cited by
- 69
- References
- 90
- Citations by year
- 2026: 6 · 2025: 4 · 2024: 9 · 2023: 12 · 2022: 10 · 2021: 14 · 2020: 9 · 2019: 4 · 2018: 1
- FWCI
- 6.62
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- eLife (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- uO Research (University of Ottawa) (submittedVersion, public-domain)
- Funders
- Natural Sciences and Engineering Research Council of Canada (04336)
- Canadian Institutes of Health Research (153143)
- Topics
- Physical Sciences › Environmental Science › Nature and Landscape Conservation › Fish biology, ecology, and behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- active sensing, active navigation, weakly electric fish, Gymnotus, pallium, electric organ discharge, backward swimming, neuronal activity, wireless recording, teleost brain, spatial navigation
- MeSH terms
- Action Potentials, Animals, Electric Organ, Hippocampus, Neurons, Perception, Swimming, Gymnotiformes, Spatial Navigation
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review