Joseph D. Monaco, Ph.D.

As a research associate faculty scientist at Johns Hopkins University, I've been working jointly with the Zhang laboratory at the Biomedical Engineering Department and the Knierim laboratory at the Mind/Brain Institute. I develop computational models in collaboration with the Zhang lab to understand the neural codes of the networks underlying spatial memory and cognition. The Knierim lab uses single-unit electrophysiology to record from the hippocampus and related brain areas of navigating rats to reveal neural representations of space. My overarching research objective is to discover mechanistic models of neural circuits and systems that explain how the dynamical coordination between brain areas produces cognition and, ultimately, adaptive behavior.

Latest

• Monaco JD, De Guzman RM, Blair HT, Zhang K. (2019) Spatial synchronization codes from coupled rate-phase neurons. PLOS Computational Biology. 15(1): e1006741. doi: 10.1371/journal.pcbi.1006741
  • Summary Spatial cognition in mammals depends on position-related activity in the hippocampus and entorhinal cortex. Hippocampal place cells and entorhinal grid cells carry distinct maps as rodents move around. The grid cell map is thought to measure angles and distances from previous locations using path integration, a strategy of internally tracking self motion. However, path integration accumulates errors and must be ‘reset’ by external sensory cues. Allowing rats to explore an open arena, we recorded spiking neurons from areas interconnected with the entorhinal cortex, including subcortical structures and the hippocampus. Many of these subcortical regions help coordinate the hippocampal theta rhythm. Thus, we looked for spatial information in theta-rhythmic spiking and discovered ‘phaser cells’ in the lateral septum, which receives dense hippocampal input. Phaser cells encoded the rat’s position by shifting spike timing in symmetry with spatial changes in firing rate. We theorized that symmetric rate-phase coupling allows downstream networks to flexibly learn spatial patterns of synchrony. Using dynamical models and simulations, we showed that phaser cells may collectively transmit a fast, oscillatory reset signal. Our findings develop a new perspective on the temporal coding of space that may help disentangle competing models of path integration and cross-species differences in navigation.

• Tabuchi M, Monaco JD, Duan G, Bell BJ, Liu S, Zhang K, Wu MN. (2018). Clock-generated temporal codes determine synaptic plasticity to control sleep. Cell, 175(5): 1213-27. doi: 10.1016/j.cell.2018.09.016
  • Summary Neurons use two main schemes to encode information: rate coding (frequency of firing) and temporal coding (timing or pattern of firing). While the importance of rate coding is well established, it remains controversial whether temporal codes alone are sufficient for controlling behavior. Moreover, the molecular mechanisms underlying the generation of specific temporal codes are enigmatic. Here, we show in Drosophila clock neurons that distinct temporal spike patterns, dissociated from changes in firing rate, encode time-dependent arousal and regulate sleep. From a large-scale genetic screen, we identify the molecular pathways mediating the circadian-dependent changes in ionic flux and spike morphology that rhythmically modulate spike timing. Remarkably, the daytime spiking pattern alone is sufficient to drive plasticity in downstream arousal neurons, leading to increased firing of these cells. These findings demonstrate a causal role for temporal coding in behavior and define a form of synaptic plasticity triggered solely by temporal spike patterns.

Preprints

• Monaco JD, Hwang GM, Schultz KM, Zhang K. (2019). Cognitive swarming in complex environments with attractor dynamics and oscillatory computing. arXiv. abs: 1909.06711
• Wang CH, Monaco JD, Knierim JJ. (2019). Hippocampal place cells encode local surface texture boundaries. bioRxiv. doi: 10.1101/764282
• Monaco JD, Blair HT, and Zhang K. (2017). Spatial theta cells in competitive burst synchronization networks: Reference frames from phase codes. bioRxiv. doi: 10.1101/211458.

(Re)Views

• News & Views: Colwell CS, Donlea J. (2018). “Temporal coding of sleep”. Cell, 175(5): 1177-9. doi: 10.1016/j.cell.2018.10.047
• News & Views: Dupret D and Csicsvari J. (2014). “Turning heads to remember places”. Nature Neuroscience, 17(5), 643–644. doi: 10.1038/nn.3700
• F1000Prime: Moser E and Rowland D: “This exciting study finds an unexpected relationship between exploratory head scanning behavior and the development of new place fields in the rat hippocampus…” Faculty of 1000, May 12, 2014.
• F1000Prime: Maler L: “This elegant and original study has demonstrated a strong link between the neural activity of hippocampal pyramidal neurons (PNs) during head scanning behavior and their subsequent acquisition of a new place field…” Faculty of 1000, April 10, 2014.
• F1000Prime: Giocomo L, Moser E: “This paper presents an interesting computational model which utilizes grid-cell modularity to generate robust remapping…” Faculty of 1000, June 29, 2011.

Previously

• Monaco J, Blair HT, and Zhang K. (2017). Decoding septohippocampal theta cells during exploration reveals unbiased environmental cues in firing phase. Society for Neuroscience 2017. Washington, D.C. November 2017. [poster]
• Monaco JD, Blair HT, and Zhang K. (2017). Spatial theta cells in competitive burst synchronization networks: Reference frames from phase codes. bioRxiv. doi: 10.1101/211458.
  • Abstract Spatial cells of the hippocampal formation are embedded in networks of theta cells. The septal theta rhythm (6—10 Hz) organizes the spatial activity of place and grid cells in time, but it remains unclear how spatial reference points organize the temporal activity of theta cells in space. We study spatial theta cells in simulations and single-unit recordings from exploring rats to ask whether temporal phase codes may anchor spatial representations to the outside world. We theorize that an experience-independent mechanism for temporal coding may combine with burst synchronization to continuously calibrate self-motion to allocentric reference frames. Subcortical recordings revealed spatial theta cells with strong rate-phase correlations related to distinct theta phases. Simulations of bursting neurons and networks explained that relationship and, with competitive learning, demonstrated flexible spatial synchronization patterns when driven by low-dimensional spatial components from the recording data. Thus temporal coding synchrony may reconcile extrinsic and intrinsic neural codes.

• Monaco JD, Blair HT, and Zhang K. (2015). Spatial rate/phase correlations in theta cells can stabilize randomly drifting path integrators. COSYNE 2015. Salt Lake City, UT. March 2015. [poster] [session]

• Monaco J, Blair HT, and Zhang K. (2014). Spatial rate/phase codes provide landmark-based error correction in a temporal model of theta cells. Society for Neuroscience 2014, 752.07/UU25. Washington, D.C. November 2014. [poster] [figshare] [github]

  • […] Preliminary data from subcortical regions in rats suggest that some theta cells exhibit spatially selective firing similar to hippocampal place fields or entorhinal/subicular boundary fields. These cells also demonstrate a consistent phase relationship across space, relative to ongoing hippocampal theta and to other simultaneously recorded cells, that is correlated with the firing rate at a given location. Inspired by this data, we present a novel synchronization model in which place cells or boundary-vector cells provide a stable, landmark-based excitatory input that drives a rate-to-phase mechanism to generate a population of cells that act as location-controlled oscillators. […]

• Monaco JD, Rao G, Roth ED, and Knierim JJ. (2014). Attentive scanning behavior drives one-trial potentiation of hippocampal place fields. Nature Neuroscience, 17(5), 725–731. doi: 10.1038/nn.3687

  • Abstract The hippocampus is thought to have a critical role in episodic memory by incorporating the sensory input of an experience onto a spatial framework embodied by place cells. Although the formation and stability of place fields requires exploration, the interaction between discrete exploratory behaviors and the specific, immediate and persistent modifications of neural representations required by episodic memory has not been established. We recorded place cells in rats and found that increased neural activity during exploratory head-scanning behaviors predicted the formation and potentiation of place fields on the next pass through that location, regardless of environmental familiarity and across multiple testing days. These results strongly suggest that, during the attentive behaviors that punctuate exploration, place cell activity mediates the one-trial encoding of ongoing experiences necessary for episodic memory.

• Monaco J, Rao G, and Knierim JJ. (2013). Scanning behavior in novel environments promotes de novo formation of hippocampal place fields in rats(). Society for Neuroscience 2013, 670.07/JJJ44. San Diego, CA. November 2013. [poster]

  • We previously examined the relationship between place-field potentiation, a form of rate remapping, and head scanning behavior [1]. Here we investigate whether there is a similar interaction between head scanning and the formation of de novo place fields when the animals are first introduced to a completely novel environment. Place fields recorded in novel rooms [2] demonstrate both onset and, in some recordings, additional post-onset potentiation related to colocalized scanning activity on the prior lap.

[1] Monaco JD, Rao G, Knierim JJ. Soc Neurosci Abstr 97.13 (2011)
[2] Roth ED, Yu X, Rao G, Knierim JJ. PLoS One 7(4), e36035 (2012)