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Dr Joseph O'Neill
Ser Cymru Fellow
- ONeillJ9@cardiff.ac.uk
- +44 29206 88916
- Tower Building, 70 Park Place, Cardiff, CF10 3AT
Overview
Research summary
My research addresses how networks of neurons encode memory in the brain. A particular interest is to identify how the hippocampus and parahippocampal areas of the brain support the formation and consolidation of memory for places and events. An additional goal is to understand how memories for textures are stored and processed, when they are required to solve a task. Overall our approach is to delineate the what, where and when of memory; that is, what neurons are ‘saying’, where they are sending this information and when this code is transmitted during memory processing.
Publication
2024
- Zheng, Y., Kang, S., O'Neill, J. and Bojak, I. 2024. Spontaneous slow wave oscillations in extracellular field potential recordings reflect the alternating dominance of excitation and inhibition. The Journal of Physiology 602(4), pp. 713-736. (10.1113/jp284587)
2023
- Pandey, A. et al. 2023. Interdependence of primary and secondary somatosensory cortices for plasticity and texture discrimination learning. [Online]. BioXiv. (10.1101/2023.04.25.538217v1) Available at: https://www.biorxiv.org/content/10.1101/2023.04.25.538217v1
2020
- Gridchyn, I., Schoenenberger, P., O'Neill, J. and Csicsvari, J. 2020. Optogenetic inhibition-mediated activity-dependent modification of CA1 pyramidal-interneuron connections during behavior. eLife 2020(9), article number: e61106. (10.7554/eLife.61106)
2019
- Kaefer, K., Malagon-Vina, H., Dickerson, D. D., O'Neill, J., Trossbach, S. V., Korth, C. and Csicsvari, J. 2019. Disrupted-in-schizophrenia 1 overexpression disrupts hippocampal coding and oscillatory synchronization. Hippocampus 29(9), pp. 802-816. (10.1002/hipo.23076)
- Stella, F., Baracskay, P., O'Neill, J. and Csicsvari, J. 2019. Hippocampal reactivation of random trajectories resembling Brownian Diffusion. Neuron 102(2), pp. 450-461.e7. (10.1016/j.neuron.2019.01.052)
- Boccara, C. N., Nardin, M., Stella, F., O'Neill, J. and Csicsvari, J. 2019. The entorhinal cognitive map is attracted to goals. Science 363(6434), pp. 1443-1447. (10.1126/science.aav4837)
- Xu, H., Baracskay, P., O'Neill, J. and Csicsvari, J. 2019. Assembly responses of hippocampal CA1 place cells predict learned behavior in goal-directed spatial tasks on the radial eight-arm maze. Neuron 101(1), pp. 119-132. (10.1016/j.neuron.2018.11.015)
2017
- O'Neill, J., Boccara, C. N., Stella, F., Schoenenberger, P. and Csicsvari, J. 2017. Superficial layers of the medial entorhinal cortex replay independently of the hippocampus. Science 355(6321), pp. 184-188. (10.1126/science.aag2787)
2016
- Kovács, K. A., O'Neill, J., Schoenenberger, P., Penttonen, M., Ranguel Guerrero, D. K. and Csicsvari, J. 2016. Optogenetically blocking sharp wave ripple events in sleep does not interfere with the formation of stable spatial representation in the CA1 area of the hippocampus. PLoS ONE 11(10), article number: e0164675. (10.1371/journal.pone.0164675)
- Schoenenberger, P., O'Neill, J. and Csicsvari, J. 2016. Activity-dependent plasticity of hippocampal place maps. Nature Communications 7, article number: 11824. (10.1038/ncomms11824)
2013
- Dupret, D., O'Neill, J. and Csicsvari, J. 2013. Dynamic reconfiguration of hippocampal interneuron circuits during spatial learning. Neuron -Cambridge Ma- 78(1), pp. 166-180. (10.1016/j.neuron.2013.01.033)
2012
- Molter, C., O'Neill, J., Yamaguchi, Y., Hirase, H. and Leinekugel, X. 2012. Rhythmic modulation of theta oscillations supports encoding of spatial and behavioral information in the rat hippocampus. Neuron 75(5), pp. 889-903. (10.1016/j.neuron.2012.06.036)
2010
- Dupret, D., O'Neill, J., Pleydell-Bouverie, B. and Csicsvari, J. 2010. The reorganization and reactivation of hippocampal maps predict spatial memory performance. Nature Neuroscience 13(8), pp. 995-1002. (10.1038/nn.2599)
- O'Neill, J., Pleydell-Bouverie, B., Dupret, D. and Csicsvari, J. 2010. Play it again: reactivation of waking experience and memory. Trends in Neurosciences 33(5), pp. 220-229. (10.1016/j.tins.2010.01.006)
2008
- Senior, T. J., Huxter, J. R., Allen, K., O'Neill, J. and Csicsvari, J. 2008. Gamma oscillatory firing reveals distinct populations of pyramidal cells in the CA1 region of the hippocampus. Journal of Neuroscience 28(9), pp. 2274-2286. (10.1523/JNEUROSCI.4669-07.2008)
- O'Neill, J., Senior, T. J., Allen, K., Huxter, J. R. and Csicsvari, J. 2008. Reactivation of experience-dependent cell assembly patterns in the hippocampus. Nature Neuroscience 11(2), pp. 209-215. (10.1038/nn2037)
2007
- Csicsvari, J., O'Neill, J., Allen, K. and Senior, T. 2007. Place-selective firing contributes to the reverse-order reactivation of CA1 pyramidal cells during sharp waves in open-field exploration. European Journal of Neuroscience 26(3), pp. 704-716. (10.1111/j.1460-9568.2007.05684.x)
2006
- O'Neill, J., Senior, T. and Csicsvari, J. 2006. Place-selective firing of CA1 pyramidal cells during sharp wave/ripple network patterns in exploratory behavior. Neuron 49(1), pp. 143-155. (10.1016/j.neuron.2005.10.037)
2005
- Klausberger, T. et al. 2005. Complementary roles of Cholecystokinin- and Parvalbumin-expressing GABAergic neurons in hippocampal network oscillations. Journal of Neuroscience 25(42), pp. 9782-9793. (10.1523/JNEUROSCI.3269-05.2005)
Articles
- Zheng, Y., Kang, S., O'Neill, J. and Bojak, I. 2024. Spontaneous slow wave oscillations in extracellular field potential recordings reflect the alternating dominance of excitation and inhibition. The Journal of Physiology 602(4), pp. 713-736. (10.1113/jp284587)
- Gridchyn, I., Schoenenberger, P., O'Neill, J. and Csicsvari, J. 2020. Optogenetic inhibition-mediated activity-dependent modification of CA1 pyramidal-interneuron connections during behavior. eLife 2020(9), article number: e61106. (10.7554/eLife.61106)
- Kaefer, K., Malagon-Vina, H., Dickerson, D. D., O'Neill, J., Trossbach, S. V., Korth, C. and Csicsvari, J. 2019. Disrupted-in-schizophrenia 1 overexpression disrupts hippocampal coding and oscillatory synchronization. Hippocampus 29(9), pp. 802-816. (10.1002/hipo.23076)
- Stella, F., Baracskay, P., O'Neill, J. and Csicsvari, J. 2019. Hippocampal reactivation of random trajectories resembling Brownian Diffusion. Neuron 102(2), pp. 450-461.e7. (10.1016/j.neuron.2019.01.052)
- Boccara, C. N., Nardin, M., Stella, F., O'Neill, J. and Csicsvari, J. 2019. The entorhinal cognitive map is attracted to goals. Science 363(6434), pp. 1443-1447. (10.1126/science.aav4837)
- Xu, H., Baracskay, P., O'Neill, J. and Csicsvari, J. 2019. Assembly responses of hippocampal CA1 place cells predict learned behavior in goal-directed spatial tasks on the radial eight-arm maze. Neuron 101(1), pp. 119-132. (10.1016/j.neuron.2018.11.015)
- O'Neill, J., Boccara, C. N., Stella, F., Schoenenberger, P. and Csicsvari, J. 2017. Superficial layers of the medial entorhinal cortex replay independently of the hippocampus. Science 355(6321), pp. 184-188. (10.1126/science.aag2787)
- Kovács, K. A., O'Neill, J., Schoenenberger, P., Penttonen, M., Ranguel Guerrero, D. K. and Csicsvari, J. 2016. Optogenetically blocking sharp wave ripple events in sleep does not interfere with the formation of stable spatial representation in the CA1 area of the hippocampus. PLoS ONE 11(10), article number: e0164675. (10.1371/journal.pone.0164675)
- Schoenenberger, P., O'Neill, J. and Csicsvari, J. 2016. Activity-dependent plasticity of hippocampal place maps. Nature Communications 7, article number: 11824. (10.1038/ncomms11824)
- Dupret, D., O'Neill, J. and Csicsvari, J. 2013. Dynamic reconfiguration of hippocampal interneuron circuits during spatial learning. Neuron -Cambridge Ma- 78(1), pp. 166-180. (10.1016/j.neuron.2013.01.033)
- Molter, C., O'Neill, J., Yamaguchi, Y., Hirase, H. and Leinekugel, X. 2012. Rhythmic modulation of theta oscillations supports encoding of spatial and behavioral information in the rat hippocampus. Neuron 75(5), pp. 889-903. (10.1016/j.neuron.2012.06.036)
- Dupret, D., O'Neill, J., Pleydell-Bouverie, B. and Csicsvari, J. 2010. The reorganization and reactivation of hippocampal maps predict spatial memory performance. Nature Neuroscience 13(8), pp. 995-1002. (10.1038/nn.2599)
- O'Neill, J., Pleydell-Bouverie, B., Dupret, D. and Csicsvari, J. 2010. Play it again: reactivation of waking experience and memory. Trends in Neurosciences 33(5), pp. 220-229. (10.1016/j.tins.2010.01.006)
- Senior, T. J., Huxter, J. R., Allen, K., O'Neill, J. and Csicsvari, J. 2008. Gamma oscillatory firing reveals distinct populations of pyramidal cells in the CA1 region of the hippocampus. Journal of Neuroscience 28(9), pp. 2274-2286. (10.1523/JNEUROSCI.4669-07.2008)
- O'Neill, J., Senior, T. J., Allen, K., Huxter, J. R. and Csicsvari, J. 2008. Reactivation of experience-dependent cell assembly patterns in the hippocampus. Nature Neuroscience 11(2), pp. 209-215. (10.1038/nn2037)
- Csicsvari, J., O'Neill, J., Allen, K. and Senior, T. 2007. Place-selective firing contributes to the reverse-order reactivation of CA1 pyramidal cells during sharp waves in open-field exploration. European Journal of Neuroscience 26(3), pp. 704-716. (10.1111/j.1460-9568.2007.05684.x)
- O'Neill, J., Senior, T. and Csicsvari, J. 2006. Place-selective firing of CA1 pyramidal cells during sharp wave/ripple network patterns in exploratory behavior. Neuron 49(1), pp. 143-155. (10.1016/j.neuron.2005.10.037)
- Klausberger, T. et al. 2005. Complementary roles of Cholecystokinin- and Parvalbumin-expressing GABAergic neurons in hippocampal network oscillations. Journal of Neuroscience 25(42), pp. 9782-9793. (10.1523/JNEUROSCI.3269-05.2005)
Websites
- Pandey, A. et al. 2023. Interdependence of primary and secondary somatosensory cortices for plasticity and texture discrimination learning. [Online]. BioXiv. (10.1101/2023.04.25.538217v1) Available at: https://www.biorxiv.org/content/10.1101/2023.04.25.538217v1
Research
Research topics and related papers
Working in the Behavioural Neuroscience Laboratory, our research forms part of one of its core themes, namely understanding the neural basis of learning and memory. Currently, our work focusses on the role of the subiculum in spatial memory, as well as how tactile information is encoded, stored and utilised in a task.
Mapping subicular mnemonic circuitry
The formation of memory for places and events represents a systems level process that engages multiple parahippocampal and extra-hippocampal brain regions, coordinated by the output from the CA1 region of the hippocampus and the subiculum. In contrast to CA3 and CA1 area place coding, the subiculum code shows diverse spatial properties, providing downstream targets with a complex mix of information. How does this subicular code represent mnemonic information? How does it interact with the CA1 area during learning? How is this information routed to the rest of the brain during different stages of memory formation? To answer these questions, we use multichannel recordings in freely moving rats combined with optogenetics and chemogenetics.
Cell assembly reactivation/replay in the hippocampus and parahippocampal areas
A growing body of evidence suggests sleep plays a critical role in memory consolidation. The hippocampus partially coordinates this process by reactivating or replaying memory traces, as part of an offline ‘rehearsal’ mechanism. The subiculum projects to the overwhelming majority of hippocampal target structures and so likely conveys replayed memory traces to parahippocamal regions and beyond. An important goal for the group is to identify how the subiculum supports consolidation and how this is coordinated with the CA1.
Cortical pathways and synaptic mechanisms for texture discrimination learning in rodents
In collaboration with Kevin Fox and Rob Honey, we aim to apply techniques that can resolve information from the level of the synapse up to the whole brain to understanding the physical basis of learning and memory. Our component of this project is to discover how network dynamics in the brain subserves learning, consolidation and recall in tasks that requires memory of textures to solve. To do this we employ multichannel recordings (350 channel neuropixel probes) to record both single unit and local field potential activity across multiple brains structures simultaneously.
Funding
Ser Cymru II, Rising star fellowship (2018-2022) Mapping subicular mnemonic circuitry
BBSRC research grant, co-applicant (2020- 2023) Cortical pathways and synaptic mechanisms for texture discrimination learning in rodents
Research group
Team members:
Dr Jon Wilson (post-doc)
Dr Sungmin Kang (post-doc)
Harriet Hallum (Senior Technician)
Research collaborators
Dr Andrew Nelson
Prof. John Aggleton
Prof. Seralynne Vann
Prof. Rob Honey
Prof. Kevin Fox
Biography
Undergraduate education
Aberdeen, 1994-1998 BSc (Hons) Neuroscience
Postgraduate education
2002: MSc Neuroscience, University College London, thesis supervisor Dr Francis Edwards
2003-2007: D.Phil., Wolfson College, University of Oxford, Thesis: Reactivation of waking firing patterns during sleep. Supervisor: Dr. Jozsef Csicsvari
Employment
2018, Ser Cymru II Fellow, School of Psychology, Cardiff University
2011-2017 Post-doctoral researcher, Institute of Science and Technology (IST) Austria
2009 - 2011 Investigator Scientist, MRC Anatomical Neuropharmacology Unit, University of Oxford
2008 – 2009: CNRS post-doctoral researcher, Institut des Maladies Neurodégénératives, Université Bordeaux Segalen, France
Supervisions
Postgraduate research interests
If you are interested in applying for a PhD, or for further information regarding my postgraduate research, please contact me directly (contact details available on the 'Overview' page), or submit a formal application.