The Integration of Goal-Directed Signals onto Spatial Maps of Hippocampal Place Cells

Aoki, Yuki; Igata, Hideyoshi; Ikegaya, Yuji; Sasaki, Takuya

doi:10.1016/j.celrep.2019.04.002

Cited by 45 publications

(44 citation statements)

References 35 publications

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“…Optogenetic perturbation of the MS does not alter place cell firing field properties. This finding is in agreement with pharmacological inactivation studies that propose endogenous MS signals are not necessary for the generation of hippocampal place fields (Aoki et al, 2019;Bolding et al, 2019;Brandon et al, 2014;Koenig et al, 2011). Yet, the endogenous theta frequency range in relation to movement speed is proposed to provide an egocentric metric frame that translates synaptic strengths to perceived spatial displacement within the coordinate system provided by place cells and grid cells (Burgess, 2008;Buzsaki, 2005;Hasselmo & Brandon, 2008;O'Keefe & Nadel, 1978;Welday, Shlifer, Bloom, Zhang, & Blair, 2011).…”

Section: Discussionsupporting

confidence: 92%

“…However, although septal inactivation does not affect the spatial firing properties of hippocampal place cells in familiar or novel environments (Aoki et al, 2019;Bolding, Ferbinteanu, Fox, & Muller, 2019;Brandon, Koenig, Leutgeb, & Leutgeb, 2014;Koenig et al, 2011), the loss of the MS and hippocampal theta significantly interferes with navigation to a hidden goal and spatial reference memory (Bolding et al, 2019;Hagan, Salamone, Simpson, Iversen, & Morris, 1988;Winson, 1978) as well as working memory (Wang, Romani, Lustig, Leonardo, & Pastalkova, 2015).…”

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confidence: 99%

“…The MS has been proposed to act as a pacemaker for theta oscillations in the hippocampus (Stewart & Fox, 1989;Stewart & Fox, 1990;Zutshi et al, 2018) by generating rhythmic disinhibition at the synapses of hippocampal pyramidal neurons via long-range axons to hippocampal GABAergic neurons (Freund & Antal, 1988;Fuhrmann et al, 2015;Gulyas, Gorcs, & Freund, 1990;Hangya, Borhegyi, Szilagyi, Freund, & Varga, 2009;Petsche, Stumpf, & Gogolak, 1962;Toth, Freund, & Miles, 1997). Pharmacological inactivation of the MS and subsequent loss of theta oscillations in the hippocampus alter spatially tuned cells in the hippocampal-entorhinal circuit, where grid cell spacing (Brandon et al, 2011;Koenig, Linder, Leutgeb, & Leutgeb, 2011) and the goal-directed increase of in-field place cell firing rates are both disrupted (Aoki, Igata, Ikegaya, & Sasaki, 2019).…”

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confidence: 99%

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Optogenetic “low‐theta” pacing of the septohippocampal circuit is sufficient for spatial goal finding and is influenced by behavioral state and cognitive demand

et al. 2020

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Hippocampal theta oscillations show prominent changes in frequency and amplitude depending on behavioral state or cognitive demands. How these dynamic changes in theta oscillations contribute to the spatial and temporal organization of hippocampal cells, and ultimately behavior, remain unclear. We used low-theta frequency optogenetic stimulation to pace coordination of cellular and network activity between the medial septum (MS) and hippocampus during baseline and MS stimulation while rats were at rest or performing a spatial accuracy task with a visible or hidden goal zone. Hippocampal receptivity to pan-neuronal septal stimulation at low-theta frequency was primarily determined by speed and secondarily by task demands. Competition between artificial and endogenous field potentials at theta frequency attenuated hippocampal phase preference relative to local theta, but the spike-timing activity of hippocampal pyramidal cells was effectively driven by artificial septal output, particularly during the hidden goal task. Notwithstanding temporal reorganization by artificial theta stimulation, place field properties were unchanged and alterations to spatial behavior were limited to goal zone approximation. Our results indicate that even a low-theta frequency timing signal in the septohippocampal circuit is sufficient for spatial goal finding behavior. The results also advance a mechanistic understanding of how endogenous or artificial somatodendritic timing signals relate to displacement computations during navigation and spatial memory.

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Section: Discussionsupporting

confidence: 92%

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confidence: 99%

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confidence: 99%

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Optogenetic “low‐theta” pacing of the septohippocampal circuit is sufficient for spatial goal finding and is influenced by behavioral state and cognitive demand

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“…Interestingly, we saw evidence for increases in pattern similarity despite using a low-level attentional task, speaking to the potential automaticity of retrieving more location-based representations. Across the literature there are numerous examples of evidence for spatial learning in humans and rodents during goal directed navigation (Aoki, Igata, Ikegaya, & Sasaki, 2019;Howard et al, 2014), non-goal directed navigation (e.g. O' Keefe & Dostrovsky, 1971;Tolman, 1948), mental imagery (e.g.…”

Section: Discussionmentioning

confidence: 99%

Tracking the emergence of location-based spatial representations in human scene-selective cortex

Berens

Joensen

Horner

2019

Preprint

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AbstractScene-selective regions of the human brain form allocentric representations of locations in our environment. These representations are independent of heading direction and allow us to know where we are regardless of our direction of travel. However, we know little about how these location-based representations are formed. Using fMRI representational similarity analysis and generalised linear mixed models, we tracked the emergence of location-based representations in scene-selective brain regions. We estimated patterns of activity for two distinct scenes, taken before and after participants learnt they were from the same location. During a learning phase, we presented participants with two types of panoramic videos: (1) an overlap video condition displaying two distinct scenes (0° and 180°) from the same location, and (2) a no-overlap video displaying two distinct scenes from different locations (that served as a control condition). In the parahippocampal cortex (PHC) and retrosplenial cortex (RSC), representations of scenes from the same location became more similar to each other only after they had been shown in the overlap condition, suggesting the emergence of location-based viewpoint-independent representations. Whereas potential location-based representations emerged in the PHC regardless of task performance, RSC representations only emerged for locations where participants could behaviourally identify the two scenes as belonging to the same location. The results suggest that we can track the emergence of location-based representations in the PHC and RSC in a single fMRI session and support computational models that propose the RSC plays a key role in using such representations to locate ourselves in space.

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“…Experimental recordings from rodent hippocampus suggest that individual pyramidal cells in area CA3 show location-specific (place cell) firing during free exploration (Fenton and Muller, 1998;Mizuseki et al, 2012). Further, it has been argued that variability seen in these brief increases in firing during individual passes through the preferred location may encode additional attributes, such as aspects of the animal's trajectory (Allen et al, 2012;Grieves et al, 2016), its motion relative to goal direction (Aoki et al, 2019), variable attentional state of the animal (Olypher et al, 2002;Fenton et al, 2010), modulation by Figure 1. Modeling short-term plasticity (STP) at stochastic hippocampal synapses.…”

Section: Estimating Synaptic Information Ratesmentioning

confidence: 99%

Local Design Principles at Hippocampal Synapses Revealed by an Energy-Information Trade-Off

Mahajan¹,

Nadkarni²

2020

eNeuro

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Synapses across different brain regions display distinct structure-function relationships. We investigated the interplay of fundamental design constraints that shape the transmission properties of the excitatory CA3-CA1 pyramidal cell connection, a prototypic synapse for studying the mechanisms of learning in the mammalian hippocampus. This small synapse is characterized by probabilistic release of transmitter, which is markedly facilitated in response to naturally occurring trains of action potentials. Based on a physiologically motivated computational model of the rat CA3 presynaptic terminal, we show how unreliability and short-term dynamics of vesicular release work together to regulate the trade-off of information transfer versus energy use. We propose that individual CA3-CA1 synapses are designed to operate near the maximum possible capacity of information transmission in an efficient manner. Experimental measurements reveal a wide range of vesicular release probabilities at hippocampal synapses, which may be a necessary consequence of long-term plasticity and homeostatic mechanisms that manifest as presynaptic modifications of the release probability. We show that the timescales and magnitude of short-term plasticity (STP) render synaptic information transfer nearly independent of differences in release probability. Thus, individual synapses transmit optimally while maintaining a heterogeneous distribution of presynaptic strengths indicative of synaptically-encoded memory representations. Our results support the view that organizing principles that are evident on higher scales of neural organization percolate down to the design of an individual synapse.

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The Integration of Goal-Directed Signals onto Spatial Maps of Hippocampal Place Cells

Abstract: Highlights d In-field firing rates of hippocampal cells increase during goaldirected behavior d Internally motivated goal-directed behavior boosts in-field firing d Medial septal inactivation reduces goal-directed firing

Cited by 45 publications

References 35 publications

Optogenetic “low‐theta” pacing of the septohippocampal circuit is sufficient for spatial goal finding and is influenced by behavioral state and cognitive demand

Optogenetic “low‐theta” pacing of the septohippocampal circuit is sufficient for spatial goal finding and is influenced by behavioral state and cognitive demand

Tracking the emergence of location-based spatial representations in human scene-selective cortex

Local Design Principles at Hippocampal Synapses Revealed by an Energy-Information Trade-Off

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