skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.

Explore Research Products in the PAR
It may take a few hours for recently added research products to appear in PAR search results.


Title: Temporal context and latent state inference in the hippocampal splitter signal
The hippocampus is thought to enable the encoding and retrieval of ongoing experience, the organization of that experience into structured representations like contexts, maps, and schemas, and the use of these structures to plan for the future. A central goal is to understand what the core computations supporting these functions are, and how these computations are realized in the collective action of single neurons. A potential access point into this issue is provided by ‘splitter cells’, hippocampal neurons that fire differentially on the overlapping segment of trajectories that differ in their past and/or future. However, the literature on splitter cells has been fragmented and confusing, owing to differences in terminology, behavioral tasks, and analysis methods across studies. In this review, we synthesize consistent findings from this literature, establish a common set of terms, and translate between single-cell and ensemble perspectives. Most importantly, we examine the combined findings through the lens of two major theoretical ideas about hippocampal function: representation of temporal context and latent state inference. We find that unique signature properties of each of these models are necessary to account for the data, but neither theory, by itself, explains all of its features. Specifically, the temporal gradedness of the splitter signal is strong support for temporal context, but is hard to explain using state models, while its flexibility and task-dependence is naturally accounted for using state inference, but poses a challenge otherwise. These theories suggest a number of avenues for future work, and we believe their application to splitter cells is a timely and informative domain for testing and refining theoretical ideas about hippocampal function.  more » « less
Award ID(s):
1844935
PAR ID:
10412030
Author(s) / Creator(s):
; ;
Date Published:
Journal Name:
eLife
Volume:
12
ISSN:
2050-084X
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. ; ; ; ; ; ; ; ; ; ; et al (, PLOS Biology)
    Klausberger, Thomas (Ed.)
    Understanding brain operation demands linking basic behavioral traits to cell-type specific dynamics of different brain-wide subcircuits. This requires a system to classify the basic operational modes of neurons and circuits. Single-cell phenotyping of firing behavior during ongoing oscillations in vivo has provided a large body of evidence on entorhinal–hippocampal function, but data are dispersed and diverse. Here, we mined literature to search for information regarding the phase-timing dynamics of over 100 hippocampal/entorhinal neuron types defined in Hippocampome.org . We identified missing and unresolved pieces of knowledge (e.g., the preferred theta phase for a specific neuron type) and complemented the dataset with our own new data. By confronting the effect of brain state and recording methods, we highlight the equivalences and differences across conditions and offer a number of novel observations. We show how a heuristic approach based on oscillatory features of morphologically identified neurons can aid in classifying extracellular recordings of single cells and discuss future opportunities and challenges towards integrating single-cell phenotypes with circuit function. 
    more » « less
  2. ; ; ; (, Science Advances)
    null (Ed.)
    The theory that the hippocampus is critical for visual memory and relational cognition has been challenged by discovery of more spared hippocampal tissue than previously reported in H.M., previously unreported extra-hippocampal damage in developmental amnesiacs, and findings that the hippocampus is unnecessary for object-in-context memory in monkeys. These challenges highlight the need for causal tests of hippocampal function in nonhuman primate models. Here, we tested rhesus monkeys on a battery of cognitive tasks including transitive inference, temporal order memory, shape recall, source memory, and image recognition. Contrary to predictions, we observed no robust impairments in memory or relational cognition either within- or between-groups following hippocampal damage. These results caution against over-generalizing from human correlational studies or rodent experimental studies, compel a new generation of nonhuman primate studies, and indicate that we should reassess the relative contributions of the hippocampus proper compared to other regions in visual memory and relational cognition. 
    more » « less
  3. ; ; ; ; ; (, Hippocampus)
    Abstract Investigations of hippocampal functions have revealed a dizzying array of findings, from lesion‐based behavioral deficits, to a diverse range of characterized neural activations, to computational models of putative functionality. Across these findings, there remains an ongoing debate about the core function of the hippocampus and the generality of its representation. Researchers have debated whether the hippocampus's primary role relates to the representation of space, the neural basis of (episodic) memory, or some more general computation that generalizes across various cognitive domains. Within these different perspectives, there is much debate about the nature of feature encodings. Here, we suggest that in order to evaluate hippocampal responses—investigating, for example, whether neuronal representations are narrowly targeted to particular tasks or if they subserve domain‐general purposes—a promising research strategy may be the use of multi‐task experiments, or more generally switching between multiple task contexts while recording from the same neurons in a given session. We argue that this strategy—when combined with explicitly defined theoretical motivations that guide experiment design—could be a fruitful approach to better understand how hippocampal representations support different behaviors. In doing so, we briefly review key open questions in the field, as exemplified by articles in this special issue, as well as previous work using multi‐task experiments, and extrapolate to consider how this strategy could be further applied to probe fundamental questions about hippocampal function. 
    more » « less
  4. ; ; ; (, Proceedings of SPIE)
    The rise of mobile multi-agent robotic platforms is outpacing control paradigms for tasks that require operating in complex, realistic environments. To leverage inertial, energetic, and cost bene fits of small-scale robots, critical future applications may depend on coordinating large numbers of agents with minimal onboard sensing and communication resources. In this article, we present the perspective that adaptive and resilient autonomous control of swarms of minimal agents might follow from a direct analogy with the neural circuits of spatial cognition in rodents. We focus on spatial neurons such as place cells found in the hippocampus. Two major emergent hippocampal phenomena, self-stabilizing attractor maps and temporal organization by shared oscillations, reveal theoretical solutions for decentralized self-organization and distributed communication in the brain. We consider that autonomous swarms of minimal agents with low-bandwidth communication are analogous to brain circuits of oscillatory neurons with spike-based propagation of information. The resulting notion of `neural swarm control' has the potential to be scalable, adaptive to dynamic environments, and resilient to communication failures and agent attrition. We illustrate a path toward extending this analogy into multi-agent systems applications and discuss implications for advances in decentralized swarm control. 
    more » « less
  5. ; ; ; (, The Journal of Neuroscience)
    Although much is known about how single neurons in the hippocampus represent an animal's position, how circuit interactions contribute to spatial coding is less well understood. Using a novel statistical estimator and theoretical modeling, both developed in the framework of maximum entropy models, we reveal highly structured CA1 cell-cell interactions in male rats during open field exploration. The statistics of these interactions depend on whether the animal is in a familiar or novel environment. In both conditions the circuit interactions optimize the encoding of spatial information, but for regimes that differ in the informativeness of their spatial inputs. This structure facilitates linear decodability, making the information easy to read out by downstream circuits. Overall, our findings suggest that the efficient coding hypothesis is not only applicable to individual neuron properties in the sensory periphery, but also to neural interactions in the central brain. SIGNIFICANCE STATEMENTLocal circuit interactions play a key role in neural computation and are dynamically shaped by experience. However, measuring and assessing their effects during behavior remains a challenge. Here, we combine techniques from statistical physics and machine learning to develop new tools for determining the effects of local network interactions on neural population activity. This approach reveals highly structured local interactions between hippocampal neurons, which make the neural code more precise and easier to read out by downstream circuits, across different levels of experience. More generally, the novel combination of theory and data analysis in the framework of maximum entropy models enables traditional neural coding questions to be asked in naturalistic settings. 
    more » « less
  • Citation Formats
  • MLA
  • APA
  • Chicago
  • BibTeX
  • Save / Share this Record
  • Send to Email